Polyvagal-Theory_Porges.md

The Polyvagal Theory

by Stephen W Porges

This book compiles, for the first time, Stephen W. Porges’s decades of research. A leading expert in developmental psychophysiology and developmental behavioral neuroscience, Porges is the mind behind the groundbreaking Polyvagal Theory, which has startling implications for the treatment of anxiety, depression, trauma, and autism. Adopted by clinicians around the world, the Polyvagal Theory has provided exciting new insights into the way our autonomic nervous system unconsciously mediates social engagement, trust, and intimacy. - Polyvagal Theory (Amazon)

Contents

• Summary
  • Foreword, by Bessel A. van der Kolk
  • Introduction: Why Is There a Polyvagal Theory?
• PART I: THEORETICAL PRINCIPLES
  • 1. Neuroception: A Subconscious System for Detecting Threat and Safety
  • 2. Orienting in a Defensive World: Mammalian Modifications of Our Evolutionary Heritage. A Polyvagal Theory
  • 3. The Polyvagal Theory: New Insights Into Adaptive Reactions of the Autonomic Nervous System
• PART II: BIOBEHAVIORAL REGULATION DURING EARLY DEVELOPMENT
  • 4. Vagal Tone: A Physiological Marker of Stress Vulnerability
  • 5. The Infant’s Sixth Sense: Awareness and Regulation of Bodily Processes
  • 6. Physiological Regulation in High-Risk Infants: A Model for Assessment and Potential Intervention
  • 7. Infant Regulation of the Vagal “Brake” Predicts Child Behavior Problems: A Psychobiological Model of Social Behavior
  • 8. The Early Development of the Autonomic Nervous System Provides a Neural Platform for Social Behavior
• PART III: SOCIAL COMMUNICATION AND RELATIONSHIPS
  • 9. Vagal Tone and the Physiological Regulation of Emotion
  • 10. Emotion: An Evolutionary By-Product of the Neural Regulation of the Autonomic Nervous System
  • 11. Love: An Emergent Property of the Mammalian Autonomic Nervous System
  • 12. Social Engagement and Attachment: A Phylogenetic Perspective
  • 13. The Polyvagal Hypothesis: Common Mechanisms Mediating Autonomic Regulation, Vocalizations, and Listening
• PART IV: THERAPEUTIC AND CLINICAL PERSPECTIVES
  • 14. The Vagus: A Mediator of Behavioral and Physiological Features Associated With Autism
  • 15. Borderline Personality Disorder and Emotion Regulation
  • 16. Abuse History Is Related to Autonomic Regulation
  • 17. Music Therapy, Trauma, and the Polyvagal Theory
• PART V: SOCIAL BEHAVIOR AND HEALTH
  • 18. Reciprocal Influences Between Body and Brain in the Perception and Expression of Affect
  • 19. Neurobiology and Evolution: Mechanisms, Mediators, and Adaptive Consequences of Caregiving
  • Epilogue

Summary

Foreword, by Bessel A. van der Kolk

Chapter: Trauma and Affect Regulation

• Series of unforgettable events that changed understanding of life: music, novel ideas, lectures
  • Peter Sellers' production of "Marriage of Figaro"
  • Elisabeth Kübler-Ross lecture on schizophrenia
  • Steve Maier's talk on neurobiology of inescapable shock at ACNP 1984
• May 21, 1999: significant day for understanding trauma and emotions
  • Bruce McEwen: stress and hippocampus, neuroplasticity
  • Jaak Panksepp: brain circuits of nurturance, fear, rage, and play
  • Stephen Porges: polyvagal theory of emotions
• Clinicians and researchers face challenges with fight/flight reactions from patients with trauma histories
  • Minor irritations escalate into catastrophes
  • Communication difficulties leading to interpersonal conflicts
• PTSD's origins expanded beyond dramatic incidents to include emotional abuse, loss of caregivers, inconsistency, and chronic misattunement
• Failure in establishing secure early attachment bonds leads to a diminished capacity to regulate negative emotions
  • Harlow's research on abandonment and affect regulation in nonhuman primates
  • Attachment research shows internal regulatory processes reflect external sources of regulation early in life
• People with chronic misattunement with caregivers have difficulties managing negative emotions later in life
  • Deficient affect regulation leads to vicious circle of deficient self-control and abandonment
• Traditional psychiatric interventions and medications are not effective for managing emotions in people with trauma histories
• Problems caused by dysregulated behavior have pervasive effects on development of mind and brain, leading to increased utilization of various services
• Study of patients with abuse and neglect histories helped by developments in affective neuroscience, particularly Panksepp's work on basic emotional systems.
• Role of heart rate variability (HRV) in maintaining emotional roller coasters became a focus.

Polyvagal Theory: Social Vagus and Visceral Experiences in Emotional Regulation

Porges's Polyvagal Theory: Understanding Emotional Regulation

• First exposure to Porges’s polyvagal theory in understanding HRV (heart rate variability) and its role in emotional regulation
• People with stable HRV do not develop PTSD, while those with poor HRV have PTSD
• Expanded the previous model of autonomic nervous system functioning by emphasizing the social, myelinated vagus as a fine-tuning regulatory system
• Social engagement system relies on facial expressions, speech, and prosody for stress management through social interaction

Theory Breakdown: Affect Regulation

• Mammals need to distinguish friend from foe and adjust behavior based on social group demands
• When the social vagus no longer can stabilize the organism under extreme stress, older systems are recruited to regulate metabolic output
• Social engagement system breaks down, leading to fight-or-flight behaviors, immobilization, and syncope (behavioral shutdown)

Visceral Experiences: Relation between Visceral State and Emotional Expression

• Trauma researchers have long understood that "the body keeps the score" in encoding memories of trauma through visceral experiences, emotions, autoimmune disorders, and skeletal-muscular problems
• Porges proposed that afferent feedback from the viscera contributes significantly to accessibility of prosocial circuits associated with social engagement
• Mobilization changes ability to detect positive social cues, while immobilization may make a person impervious to positive input. Visceral states color perception of self and surroundings.
• People with impaired social engagement systems have trouble interpreting safety as a threat or objective danger as safe due to their malfunctioning visceral feedback system. They tend to inhibit sensory feedback from their bodies and experience the feedback from both their bodies and the world around them as bland and meaningless.

Polyvagal Theory Contributions:

• Clarified mechanisms that allow humans and animals to distinguish friend from foe, adjust behavior based on social group demands, and manage stress through social engagement
• Understood capacity of tone of voice and rhythms of speech, as well as faces of loved ones, in restoring physiological equilibrium.

Polyvagal Theory Influencing Holistic Treatment Approaches

Observation of Body-Based Defensive Maneuvers and Trauma

• Observed traumatized individuals engage in body-based defensive maneuvers
• Incorporated work of body-based therapists, including Peter Levine and Pat Ogden
• Polyvagal theory helped organize treatment for abused children and traumatized adults

Implications for Treatment

• Polyvagal Theory: profound effect on understanding emotional states, biological systems, and mental constructs
• Understanding physiological states as flexible based on relationship to visceral experiences and relationships
• Shift in therapeutic approaches towards nonpharmacological treatments: interpersonal rhythms, vocal/facial communication, breath exercises, body movements (chi qong, tai chi), rhythmical activities (kendo drumming)
• Potential benefits for psychiatric disorders like anxiety, ADHD, autism, trauma-related psychopathology
• Increasing support and funding for these nontraditional interventions from the Department of Defense and National Institutes of Health
• Shift towards promoting social vagus activation or dampening sympathetic tone through play and rough/tumble behaviors.

Introduction: Why Is There a Polyvagal Theory?

The Polyvagal Theory: Emergence and Background

• The polyvagal theory emerged from a dialectic between author's curiosity in biobehavioral systems and dissatisfaction with prevalent models integrating physiological state and behavior.
• In the late 1960s, constructs relating physiology to behavior were limited, with arousal as a dominant concept.
• Psychophysiologists assumed arousal was mediated by sympathetic nervous system (SNS) and HPA axis mechanisms.
• Arousal's specific neural mechanisms were not well understood, limiting research on psychological processes.
• The author was intrigued with physiological measures as a guide for therapists during clinical interactions.

Background of Psychophysiology:

• Established in early 1960s as interdisciplinary field merging psychology, medicine, physiology, and engineering.
• Society for Psychophysiological Research formed in 1960; first issue of journal published in 1964.
• Initially focused on physiology as a dependent variable, psychological factors as independent variables.
• Early meetings attracted successful scientists from various domains.
• Shifted research focus towards measures of brain function using EEG, ERPs, and fMRI methods during cognitive and affective challenges.

Limitations of Correlating Physiology and Behavior:

• Physiological variables seen as correlates without underlying relationship between physiology and behavior or psychology.
• Two global domains in biobehavioral sciences: observable behavior/subjective psychology, peripheral autonomic/neural brain.
• Consequence of modern Western scientific solution to historical mind–body problem.

Porges' Development of Vagal Tone Quantification in Psychophysiological Research.

Polyvagal Theory: Emergence and Impact

Challenging Dualism in Science

• Theories challenge implicit dualism by providing bidirectional brain–body model (polyvagal theory)
• Brain regulates peripheral physiology as a neural platform for social behaviors
• Scientific solutions of dualism are not true solutions, merely objective descriptions with exquisite technologies
• Limited conceptualization of brain's role in regulating peripheral physiology in the late 1960s
• Measures like heart rate variability and neuroendocrine activity are potential biomarkers of clinical health and risk

Polyvagal Theory Roots

• Porges' master's thesis: Stabilized heart rate pattern linked to attention
• Publication first quantitative description of heart rate variability as a response variable sensitive to psychological manipulations
• Dissertation confirmed individual differences in heart rate variability predicted reaction time performance and degree of suppression during attending
• Research continued exploring heart rate and heart rate variability for 40 years

Linking Changes in Heart Rate Variability to Vagal Mechanisms

• Quantification techniques developed to characterize rhythms in beat-to-beat heart rate pattern (respiratory rhythm = respiratory sinus arrhythmia)
• Validation studies demonstrated vagal influences on the heart through quantifying amplitude of respiratory rhythm

Heart Rate Variability Method Advantages

1. Dynamic monitoring of shifts in vagal control over short periods
2. Conforms to statistical assumptions for parametric statistics
3. Reliable estimates even when baseline heart rate drifts and violates stationarity assumption
4. Not moderated by respiration rate
5. Reflects the same changes in vagal function across time and laboratories

Impact of Polyvagal Theory Research

• Enabled dynamic investigation of sympathetic and parasympathetic components in autonomic nervous system
• Vagal tone became a familiar measure in psychological and psychophysiological research
• Dozens of studies conducted around the world using the same metric
• Other metrics of vagal tone derived from heart rate variability developed by other scientists
• Provided critical measurement tool to study interplay between sympathetic and parasympathetic components.

Solving Vagal Paradox Led to Polyvagal Theory and Clinical Applications

Cardiac Vagal Tone and Polyvagal Theory:

Background:

• Conceptualization of cardiac vagal tone didn't challenge existing dogma on autonomic nervous system
• Importance of tonic levels of vagal activity as an index of general neural health and protective feature
• Early 1990s, saw myself contributing to understanding the other side of autonomic function for sympathetic-centric research world

Vagal Paradox:

• Realized that my perspective was missing three crucial points leading to Polyvagal Theory
  1. Lack of hierarchical conceptualization of autonomic reactions (inhibitory role of vagus on sympathetic regulation)
  2. Understanding neural regulation changes during evolution and its relation to adaptive functions in mammals
  3. Two vagal pathways originating from different brainstem nuclei and their relative functions
• Intellectual complacency ended with a letter from neonatologist questioning relationship between high cardiac vagal tone and newborn health
• Contradiction in understanding of vagus regulation as both protective and potentially lethal (vagal paradox)

Development of Polyvagal Theory:

• Worked on integrating literature on autonomic nervous system to extract organizing principles
  • Access to resources at National Institutes of Health library and National Library of Medicine
• Initial presentation of theory in October 1994, refined and expanded since then (Porges, 2001a, 2007a)
• Chapters in this book provide insight into developments dependent on the theory including vagal brake, self-regulation, development, emotion, evolution and dissolution, immobilization without fear, social engagement system, attachment, love and monogamy, neuroception, prosody and vocal communication, clinical applications, redefining social neuroscience.

PART I: THEORETICAL PRINCIPLES

1. Neuroception: A Subconscious System for Detecting Threat and Safety

Part I: Theoretical Principles

• Part I introduces the theoretical framework of neuroception, a subconscious system for detecting threat and safety
• Neuroception distinguishes between safe, dangerous, or life-threatening situations without conscious awareness
• Detection of danger triggers neural circuits that facilitate social behavior or defensive behaviors (fight, flight, freeze)
• Human beings' initial response to each other is influenced by neurobiological processes and not just learning and socialization

Chapter 1: Neuroception: A Subconscious System for Detecting Threat and Safety

• Human behavior towards others determined by neurobiological processes, including DNA
• Triggers and mechanisms of behaviors during normal development studied to help children with severe disabilities (e.g., autism) improve social behavior
• Senses used by the nervous system to evaluate risk constantly
• Coined term "neuroception" to describe how neural circuits distinguish safe vs dangerous situations or people
• Defense reactions may occur even if one is not aware of danger on a cognitive level but neurophysiologically, body starts neural processes for adaptive defense behaviors.

Neuroception Process

1. Nervous system evaluates risk in environment through senses
2. Neural circuits distinguish safe vs dangerous or life-threatening situations
3. Triggers neurobiologically determined prosocial or defensive behaviors based on the assessment
4. Defensive reactions may hinder social engagement and forming lasting bonds if not inhibited effectively.

Social Engagement and Defense Behaviors: Adaptive or Maladaptive Strategies?

• Social engagement and defense behaviors can be adaptive or maladaptive depending on the level of risk present in the environment
• Clinical perspective focuses on a person's ability to inhibit defensive systems in safe environments or activate defense systems in risky situations or both.

Understanding Social Engagement in Humans: Immobilization, Oxytocin, and Bond Formation

Neuroception and Social Engagement Behavior

Safe Environment:

• Adaptive to inhibit defense systems and exhibit positive social engagement behavior
• Faulty neuroception (inaccurate assessment of safety or danger) may contribute to maladaptive physiological reactivity and defensive behaviors in psychiatric disorders
• In typically developing children, neuroception accurately detects risk

Neuroception and Physiological Responses:

• When nervous system detects safety: stress responses dampened, avoid physiological states associated with "freezing" and "shutdown" behaviors
• Neural mechanisms evaluate features like facial expressions and vocalizations to determine safety or trustworthiness
• Identification of familiar people and evaluating their intentions activates brain structures that inhibit defensive strategies

Immobilization Without Fear:

• Humans have three defense strategies: fight, flight, freeze
• Immobilization (freezing) is an ancient mechanism to reduce metabolism and raise pain threshold
• Can also occur for prosocial activities like conception, childbirth, nursing, and bonding
• Immobilization with fear elicits profound physiological changes that can be lethal

Social Engagement: The Preamble to a Social Bond:

• To develop a social bond, not just inhibit defense systems but also physical closeness is required
• Differences between mother–infant attachment and adult partnerships in terms of mobility and behavioral repertoires
• Infants have immature neural regulation of spinal motor pathways that takes years to fully develop.

Neuroception of Safety and Social Engagement in Humans

Social Engagement and Polyvagal Theory

• Social engagement not dependent on limb regulation, but facial muscles
• Corticobulbar pathways regulate face/head muscles for social interaction
  • Eye contact
  • Vocalizing with appealing inflection and rhythm
  • Displaying contingent facial expressions
  • Modulating middle ear muscles to distinguish human voice
• Neuroception influences perception of engagement behaviors
  • Make eye contact
  • Appalling vocalization
  • Displaying facial expressions
  • Hearing human voice efficiently

Polyvagal Theory: Three Neural Circuits That Regulate Reactivity

• Humans evolved neural structures for social behavior and defense
• Polyvagal theory links evolution of heart regulation to affective experience, emotional expression, facial gestures, vocal communication, and social behavior
• Three stages in mammalian autonomic nervous system development: immobilization, mobilization, social engagement

Immobilization: feigning death or shutdown (shared with most vertebrates)

• Oldest component
• Dependent on unmyelinated vagus nerve branch originating from the dorsal motor nucleus of the vagus

Mobilization: fight-or-flight behaviors

• Dependent on sympathetic nervous system
• Increases metabolic activity and cardiac output (faster heart rate, greater ability to contract)

Social Communication or Social Engagement: facial expression, vocalization, listening (primarily mammals)

• Dependent on myelinated vagus nerve originating from the nucleus ambiguus
• Fosters calm behavioral states by inhibiting sympathetic nervous system's influence on heart

Infants and Social Engagement Strategies: form positive attachments, social bonds

• Three well-defined neural circuits support social engagement behaviors, mobilization, and immobilization
• Neuroception of safety necessary before social engagement occurs
• Benefits include physiological states associated with social support
• Social behaviors involving nursing, reproduction, and pair bonding require immobilization without fear
• Oxytocin, a neuropeptide involved in social bond formation, makes immobilization without fear possible by blocking defensive freezing behaviors.

Neuroception and Social Behavior in Psychiatric Disorders

Polyvagal Theory and Neuroception:

• Ideally, neuroception helps babies detect safe environments for exploration
• Faulty neuroception may contribute to psychiatric disorders like autism, schizophrenia, anxiety disorders, depression
• Social engagement systems in individuals with these disorders are not activated as they should be due to impaired neuroception

Impact of Environment:

• Children raised in orphanages: higher incidence of reactive attachment disorder when cared for by many caregivers versus fewer, more consistent ones
• Pilot unit children had better social behavior outcomes than standard unit children

Intervention and Polyvagal Theory:

• Biologically based interventions designed to stimulate neural circuits responsible for social engagement
• Preliminary results suggest promising outcomes in children with autism or language/social communication issues

Conclusions:

• Social behavior limited by human physiology and the evolution of defensive behaviors from primitive vertebrates
• Focusing on biologically based behaviors allows for new intervention paradigms to help children with compromised social behavior and attachment.

2. Orienting in a Defensive World: Mammalian Modifications of Our Evolutionary Heritage. A Polyvagal Theory

Chapter 2: Orienting in a Defensive World: Mammalian Modifications of Our Evolutionary Heritage

Polyvagal Theory:

• Systematic investigation of mind–body relations forms the scientific basis for psychophysiology
• Psychophysiologists assume that the nervous system provides the functional units for the bidirectional transduction of psychological and physiological processes
• Focus on neural regulation of the heart by the vagus and how it evolved to facilitate specific psychological processes

Polyvagal Systems:

• Mammals developed two vagal systems: a phylogenetic relic and an evolutionary modification unique to mammals
• The two vagal systems are programmed with different response strategies and may respond in a contradictory manner

Arousal Theory: Historical Legacy:

• Early psychophysiological research assumed peripheral autonomic measures, such as electrodermal activity and heart rate, provided sensitive indicators of arousal or activation
• This view was based on a rudimentary understanding of the autonomic nervous system and neglected important factors, such as parasympathetic influences, interactions between sympathetic and parasympathetic processes, peripheral autonomic afferents, central regulatory structures, the adaptive and dynamic nature of the autonomic nervous system, and phylogenetic and ontogenetic differences

Brain-Heart Communication: Historical Perspective:

• Autonomic nervous system is no longer functionally distinct from the central nervous system
• Peripheral organs are anchored to central structures by efferent pathways and continuously signaling central regulatory structures along their afferent pathways
• Darwin (1872) provided historical insight into the potential importance of the vagus in bidirectional communication between the brain and the heart

Neurogenic Basis of Heart Rate Responses in Orienting Reflex

Darwin and Claude Bernard's Contributions to Psychophysiology

Darwin:

• Acknowledged afferent feedback from heart to brain through vagus nerve (pneumogastric)
• Emphasized regulatory role of pneumogastric nerve in emotions
• Ideas contributed to modern psychophysiology, focusing on interaction between autonomic and sensory processes

Claude Bernard:

• Viewed heart as primary response system influenced by all sensory influences
• Central nervous system pathways have strongest effects on the heart
• Emphasized the potency of central nervous system pathways to the heart (Cournand, 1979)

Theoretical Basis for a Neuropsychophysiology of Autonomic Nervous System:

• Darwin and Claude Bernard's ideas laid foundation for understanding heart as both output system from brain and source of afferent stimulation to it
• Psychophysiologists investigated functional sensitivity of heart rate measures to sensory and affective stimuli (e.g., Darrow, 1929; Graham & Clifton, 1966; Lacey, 1967)
• Dynamic feedback between brain and heart in regulating psychological state and threshold for sensory stimuli (Lacey & Lacey, 1978)

Sokolov Model:

• Acknowledged afferents and efferents in both autonomic and somatic systems
• Autonomic feedback loop (autonomic tuning) to regulate sensory thresholds
• Interface between autonomic processes and psychological phenomena (orienting and defensive reflexes)
• Brain regulation of autonomic reactivity by habituation

Heart Rate Responses: A Neurogenic Emphasis

Orienting Reflex:

• Cardiac component characterized by heart rate deceleration influencing perceptual thresholds
• Neural mechanisms mediating cardiac orienting response are neurogenic in nature
• Rapid response onset and offset, similar to other neurogenic bradycardic reflexes (optovagal, vasovagal, baroreceptor-vagal, chemoreceptor-vagal)
• Cholinergic pathways along the vagus mediate short latency bradycardia associated with orienting reflex and classical conditioning (Obrist, 1981; Schneiderman, 1974).

The Vagal Paradox: Heart Rate and Respiratory Sinus Arrhythmia Discrepancy

Vagal Paradox in Psychophysiology:

• Inconsistency between data and theory regarding vagal regulation of heart rate and respiratory sinus arrhythmia (RSA)
• Arguments to explain discrepancy:
  • Different dimensions of vagal activity: tonic vs phasic (average heart rate vs RSA)
  • Respiratory parameters affecting RSA
  • Variation in quantification methods for RSA
  • Decrease in RSA with baroreflex stimulation
  • Complex interaction between sympathetic and vagal systems
• Neurophysiological interpretation of RSA debated due to:
  • Assumption of one central source of cardiac vagal tone
  • Differences attributed to response characteristics, not neural output or central mechanisms.

Evidence for Independent Vagal Control:

• RSA and heart rate often respond differently during various conditions (attention, inhalant anesthesia)
• Individual differences in resting heart rate and RSA contribute to measures of cardiac vagal tone
• Convergence observed during exercise or neural blockade with atropine
• Variability in relationship between RSA and heart rate depending on behavioral state.

Neurophysiological Research:

• Covariation between RSA and heart rate based on functional properties of vagal cardioinhibitory fibers to the heart (bradycardia, respiratory rhythm).

Dual Vagal Systems in Mammals: Neurogenic Bradycardia and RSA

Polyvagal Theory and Vagus Nerve

Vagal Paradox:

• Inconsistencies in interpreting vagal control of heart based on bradycardia and RSA (respiratory sinus arrhythmia)
  • Bradycardia during orienting reflexes
  • Contradictory indicators of health: positive with RSA, negative with bradycardia
  • Both can be affected by vagal blockade or severing the vagus nerve
• Proposed polyvagal theory to explain the paradox

Polyvagal Theory:

• Mammals have two anatomically distinct vagal response systems
• Different branches of the vagus regulate visceral function and originate in different brainstem nuclei
• Vagi may have opposing outputs to the same target organ (e.g., heart)
• Concept of autonomic space needs to account for potential vagovagal interactions

Vagus Nerve Anatomy:

• Not a single nerve but family of neural pathways originating in multiple brainstem areas
• Vagus is lateralized with left and right sides performing different tasks (chronotropic regulation)
• Asymmetrical, with left side more potent than right
• Dorsal motor nucleus of the vagus (DMNX) and nucleus ambiguus (NA) in medulla
  • NA located ventral to DMNX in reticular formation
  • Most cells originate from each nucleus project to specific regions: subdiaphragmatic vs. supradiaphagmatic structures
• Nucleus tractus solitarius (NTS) is terminus of afferent pathways through vagus

Evolution and Functions of Vagus Nerve in Mammals and Reptiles

The Polyvagal Theory

Premises of the Polyvagal Theory:

• The neural regulation of bradycardia and respiratory sinus arrhythmia (RSA) are mediated by different branches of the vagus, allowing them to respond independently
• Physiological evidence supports that the dorsal motor nucleus of the vagus (DMNX) contains vagal neurons capable of producing bradycardia with a response latency associated with the baroreceptor reflex

Evolutionary Development of the Polyvagal System:

• The neuroanatomical differentiation of the visceral efferent column of the vagus into a dorsal motor nucleus (DMNX) and a ventrolateral motor nucleus (NA) first occurred in reptiles
• In turtles, there was still a connection between the DMNX and NA, but in lizards and crocodiles, the separation between the two nuclei was as complete as it is in mammals
• Behavioral orienting in reptiles is characterized by a focusing of exteroceptors and freezing of gross motor activity, paralleling neurogenic bradycardia observed during this state

Evolutionary Origins and Behavioral Shifts in Vagus Nerve Function

Research Findings on Heart Rate and Arousal:

• Most researchers found bradycardia incompatible with emphasis on arousal and heart rate as an indicator (prevalent since sympathetic nervous system)
• RSA not observed in reptiles, despite phylogenetic development showing shifts in vagus neuroanatomy
  • Heart rate oscillations linked to ventilation not identified in spectral components of reptilian heart rate studies

Behavioral Shifts and Cardiac Systems:

• Mammals respond beyond reflexive orienting with sustained attention for detailed information processing or communication
• Phylogenetic development illustrates differences between reptilian and mammalian cardiac systems
  • Metaphor: Mammals have more powerful engines, while reptiles are underpowered
  • Reptiles rely on passive feeding strategies; mammals actively hunt and graze

Survival Strategies:

• Reptiles use vagal efferents from dorsal nucleus of the vagus to deal with specific challenges: orienting, freezing, conserving oxygen during apnea or quiescence
  • Vagal influences removed during periods of breathing and other activities in mammals
• Mammals use vagal efferents from nucleus ambiguus as a persistent brake on heart metabolism to inhibit high energy production
  • Highest vagal tone during unchallenged situations like sleep, withdrawn during external demands

Comparing Terrestrial and Aquatic Mammals:

• Terrestrial mammals could face cardiac ischemia and cortical anoxia if they adopted reptilian strategy of neurogenic bradycardia during stress states
  • Aquatic mammals manage oxygen resources and shift priorities for long periods underwater through complex mechanisms

Fetal Distress and Sudden Infant/Adult Death Syndrome:

• Massive neurogenic bradycardia observed during fetal distress, high-risk neonates with no observable RSA
  • Figure 2.2 illustrates low beat-to-beat variability during massive bradycardia in Figure 2.2a.

Distinction Between Myelinated Vagal Fibers in DMNX and NA: Potential Methodological or Species-related Differences

Polyvagal Theory: Vagal Influences and Heart Rate Variability (HRV)

Neonates with Low Amplitude RSA:

• At greatest risk for apnea and bradycardia
• Diminished vagal influences from nucleus ambiguus (NA) responsible for depressed RSA amplitude
• Associated with vulnerability to large neurogenic bradycardia

Complex Feedback System Between Hypoxia, Vagal Efficent Discharge, and Potentiation of Vagal Output:

• Maintains bradycardia despite massive decline in vagal firing associated with hypoxia
• Potentiates influence of vagal firing on sinoatrial node (SA)
• Bradycardia mediated through a branch of the vagus, but magnitude determined by peripheral mechanism, not centrally mediated vagal tone

Polyvagal Theory: Vagal Fibers from NA and DMNX:

• Distinguishable in structure and function
• Myelinated vagal efferent fibers from NA contain respiratory rhythm
• Unmyelinated vagal efferent fibers from DMNX do not express a respiratory rhythm

Inconsistencies in Proposed Distinction:

• Jordan et al. (1982) reported cardioinhibitory vagal neurons originating in DMNX with myelinated efferent axons and respiratory rhythm
• Schwaber's findings suggest that some neurons previously assumed to originate in DMNX are actually located in NA due to methodological limitations

Rabbit Data:

• Electrical stimulation of aortic depressor nerve results in both bradycardia and increased RSA (Figure 2.4)
• Electrical stimulation of DMNX results only in an attenuated bradycardia with no respiratory rhythm, different from NA fibers passing near the border of DMNX
• Suggests that vagal fibers discharging following DMNX stimation may not have a respiratory rhythm and are more likely to be located in NA

Future Research:

• Determine accuracy of proposed functional and structural distinctions between DMNX and NA efferents articulated in polyvagal theory.

Evolution of Vagal Systems in Mammals and Reptiles: Differences in Vagal Strategies and Origins

Neurophysiological Research on Mammalian Vagus Nerve:

• Most research conducted with rats, rabbits, cats, and dogs
• Human studies limited to pharmacological blockade and peripheral physiology measures
• Few neuroanatomical studies of human brainstem often from disease or trauma patients
• Existing data argue for polyvagal model: clinical bradycardia in human fetus, shifts in RSA independent of heart rate change during anesthesia, short latency responses from both systems.

Vagal Strategies in Mammals and Reptiles:

• Contradictory strategies: reptiles have low ambient vagal tone with transient increases in response to challenges; mammals have high ambient vagal tone and transient decreases in response to challenges.
• Adaptive for each species:
  • Reptiles: survival behaviors, freezing response, smaller metabolically active body organs, less oxygen-dependent than mammals.
  • Mammals: fight or flight responses, increased metabolic output, high energy demands, larger nervous system and body organs.

Phylogenetic Origins of Vagal Response Patterns:

• Neurogenic bradycardia controlled by DMNX observed in reptiles and mammals during orienting may have evolved from gustatory response systems of primitive vertebrates.
• Gustation is a primary method for identifying prey and predators, affecting heart, gustatory receptors, digestive systems.
• With phylogenetic development, the vagal system became more complex by incorporating pathways from other cranial nerves like trigeminal, facial, accessory, and glossopharyngeal.

Special Visceral Efferents:

• Motor component of the vagus shares origins with four cranial nerves (trigeminal, facial, accessory, and glossopharyngeal).
• Innervate somatic muscles involved in behaviors like mastication, facial expressions.
• The special visceral efferents from these five cranial nerves arise from branchial arches.
• NA controls complex coordination of pharynx, soft palate, larynx, and esophagus in mammals.

Mammalian Autonomic Functions Linked with Somatic Muscles.

Vagus Nerve: Role in Mammals' Autonomic Functions

Third Gill Arch and Carotid Body

• Part of third gill arch gives rise to carotid body (Warwick & Williams, 1975)
• Contains peripheral chemosensitive receptors sensitive to oxygen and CO2 levels
• Also houses accessory nerve fibers originating in cervical spinal cord

NA Control of Supradiaphragmatic Organs

• Coordinates complex sequence of sucking, swallowing, breathing (Warwick & Williams, 1975)
• Primary chronotropic control of heart rate
• Involved with movement, emotion, and communication behaviors

Two Branches of Vagus Nerve: Somatomotor vs. Visceromotor Functions

Anatomical Linkage Between Autonomic Function and Somatic Muscle Activity

1. Sympathetic Nervous System: regulates vasomotor tone, protects skin from tearing (Obrist, 1976)
   • Parallels evolution of voluntary motor activities
   • Effects profound on autonomic nervous system but doesn't mitigate importance of other relationships sensitive to psychological processes
2. NA and Cranial Nuclei: parasympathetic support for somatomotor projections (Haselton et al., 1992; Bieger & Hopkins, 1987)
   • Innervates larynx, pharynx, trachea, esophagus
   • Ventral part regulates bronchial resistance and heart rate (Brown, 1990)
   • Receives sensory input through trigeminal nerve and facial nucleus communication (Brown, 1974; Humphrey, 1970)

Ventral Vagal Complex in Mammals' Brainstem:

• NA and nuclei of trigeminal and facial nerves coordinate visceromotor regulation with somatomotor functions (Brown, 1974; Humphrey, 1970)
• Coexists with dorsal vagal complex consisting of DMNX and NTS that regulates vegetative processes observed in reptiles.

Evolution of Vagus Nerve: Vegetative vs Smart

Premises of Polyvagal Theory

Background:

• Neuroanatomical studies suggest that in mammals, visceromotor neurons may have migrated from the dorsal motor nucleus of vagus (DMNX) to the nucleus ambiguus (NA)
• These visceromotor neurons control facial expression, vocalization, swallowing, and sucking muscles
• They exert potent influences on heart and bronchi, slowing heart rate and increasing respiratory resistance

Special Visceral Efferents:

• Unique motor systems in mammals that arise from the source nuclei of five cranial nerves (trigeminal, facial, glossopharyngeal, vagus, accessory)
• Facial expressions reflect these muscles' control
• Synergistic relationship between somatic muscles and traditional general visceral efferents of vagus

Evolutionary Development:

• Central nervous system progression resulted in a large neocortex in mammals
• Vulnerable to shifts in oxygen, evolutionary pressures optimized autonomic strategies for oxygen availability
• Coexistence of ancestral reptilian strategies and mammalian adaptations (NA and DMNX)

Premises:

1. Neurogenic bradycardia associated with orienting is a phylogenetic vestigial relic of the reptilian brain and is mediated by the DMNX.
2. Regulation of vagal efferents by NA mechanisms contributes to mammalian ability to detect novelty, actively engage with environment, and socially communicate.
3. Withdrawal of cardiac vagal tone through NA mechanisms is a mammalian adaptation to select novelty in the environment while coping with metabolic output and continuous social communication.

Polyvagal Theory:

• Proposes that evolutionary shift led to distinct NA from DMNX and development of special visceral efferents changed role of vagus
• General visceral efferent pathways from DMNX vagus are passive reflexive motor system, vegetative vagus
• Special visceral efferent pathways from NA create active voluntary motor system, smart vagus.

Medullary Contributions to Cardiopulmonary Oscillation: Neural Networks and Regulation

Theory Focusing on Medullary Source Nuclei of Cranial Nerves

• Theory investigates shared medullary structures for special visceral efferents
• Emphasizes coordination and regulation of complex interactions among end organs, optimizing cardiopulmonary function

NA's Role in Mammals

• Coordinates cardiopulmonary functions with behaviors (ingestion, vocalizations, emotions, attention)
• Serves as cells of origin for smart vagus
• Potent link between NA and cardiopulmonary function not observed in reptiles

Medullary Contributions to a Common Cardiopulmonary Oscillator

• NA: continuum of interconnected subdivisions (compact, semicompact, loose, external)
  • Dorsal division: source of special visceral efferents innervating soft palate, pharynx, larynx, esophagus
  • Ventral division: source of general visceral efferents to thoracic viscera, primarily bronchi and sinoatrial node
• NA fibers terminating in bronchi and sinoatrial node have respiratory rhythm, suggesting RSA reflects common respiratory rhythm

Richter and Spyer's Model of Cardiopulmonary Oscillator

• Dependent on interaction between neurons in NTS and NA
• Respiratory rhythm is a manifestation of neural network comprised of interneurons regulating respiratory, laryngeal, cardiac functions
• NA is part of cardiorespiratory oscillator network

Other Brain Structures Contributing to Regulation of Cardiopulmonary Rhythm

• Respiratory rhythms observed in several nuclei (periaqueductal gray, central nucleus of amygdala, hippocampus, anterior cingulate)
• Stimulation of amygdala can influence respiratory cycle

Functional Influence on Oxygenation

• Covariation between bronchial tone and heart rate oscillations (RSA) may maximize oxygen diffusion
• Research needed to confirm relationship between oxygen saturation and RSA independent of average heart rate and respiration rate.

Polyvagal Theory: Monitoring Autonomic Nervous System Regulation via Respiratory Sinus Arrhythmia

Premises of Polyvagal Theory: The Role of Respiratory Sinus Arrhythmia (RSA)

Background:

• Interneuronal communication between dorsal and ventral nucleus ambiguus (NA) segments allows monitoring of vagal output through RSA amplitude
• NA fibers regulate heart and bronchi via special and general visceral efferents, affecting RSA

Premise 4: The ability of NA to regulate special and general visceral efferents can be monitored by the amplitude of RSA.

• Characteristic respiratory frequency in vagal fibers originating from NA produces RSA
• Accurate extraction of RSA parameters necessary for evaluating NA regulation of sinoatrial node

Role of RSA:

• Index of smart vagus (not global measure)
• Amplitude represents visceromotor tone, period reflects common cardiorespiratory drive frequency
• Functional consequence of output from vagal fibers originating in NA and terminating on sinoatrial node

Evaluation Considerations:

• Accurate determination of amplitude and period required for quantification of RSA
• Paced breathing may confound visceral-medullary feedback system, affecting RSA amplitude and period

Clinical Applications:

• Manipulations or conditions depressing special visceral efferents impact RSA
• Recovery of function parallels recovery of RSA in neurological diagnosis and neurosurgery
• Low levels of RSA observed in high-risk preterm neonates, potentially lethal for humans due to neurogenic bradycardia.

Vagal Competition and Emotional Regulation in Autonomic Nervous System

Polyvagal Theory: Vagal Competition Hypothesis

Sudden Death following Exercise:

• Surge in DMNX input, low RSA may result in sudden death
• Similar mechanism for asthma attacks

Vagal Competition Hypothesis:

• All organs with smooth and cardiac muscle have dual innervation from both the dorsal motor nucleus of the vagus (DMNX) and the nucleus ambiguus (NA)
• Two vagal inputs may innervate in a contradictory manner
• DMNX surge coupled with low RSA can lead to lethal outcomes like sudden death or asthma attacks

Asthma:

• NA efferent control of bronchi exhibits rhythmic waxing and waning with breathing
• Protects the bronchi from pathophysiological DMNX influences
• Without NA influences, bronchi become vulnerable to DMNX surges
• Asthma attack may be a product of primitive vagovagal reflex

Polyvagal Theory Testable Hypotheses:

• Nucleus ambiguus (vagal) protection hypothesis: Vagal projections originating in NA and terminating in visceral organs promote health, growth, and restoration
• Nucleus ambiguus (vagal) withdrawal hypothesis: Removal of the NA vagal brake promotes metabolic output to foster locomotion, but puts organ at risk for long periods

Emotion:

• Emotion defined by shifts in facial expressions and vocalizations change RSA and bronchomotor tone mediated by NA
• Parallel between cortical asymmetry and autonomic asymmetry
• Right brain function linked to primary emotions and right-biased autonomic regulation (NA, cardiac vagus)
• Facial expression research on lateralization is inconsistent.

Implications:

• Functional dominance of the right side of the brain in regulating homeostasis may contribute to motor and language development on the left side.

Autonomic Nervous System, Emotional Regulation, and Cardio-Respiratory Rhythm in Mammals

Polyvagal Theory Summary and Conclusion

Summary:

• Vagal System: Not a unitary dimension, includes vegetative (dorsal motor nucleus) and smart vagus (NA) systems
• Two Vagal Motor Systems: Vegetative vagus associated with passive reflexive regulation of visceral functions; smart vagus associated with active processes like attention, motion, emotion, communication
• Limited Value in Measuring Vagal Tone as a Single System
• NA Vagus Function: Monitored by respiratory sinus arrhythmia (RSA)
• Neurogenic Bradycardia: Mediated by the dorsal motor nucleus
• Common Cardiopulmonary Oscillator
• Relationship Between Autonomic Function and Primary Emotions

Polyvagal Theory Hypotheses:

• Evaluate relationship between RSA (NA vagal tone) and processes dependent on coordination of cardiopulmonary processes with special visceral efferents of cranial nerves, including vocalizations, feeding, breathing, facial expression.

Insights from Phylogenetic Approach:

• Explains vagal paradox in terms of medullary source nuclei of dorsal motor nucleus and NA
• Highlights importance of oxygen needs in evolving nervous system
• Constructs like orienting, attention, emotion, stress are byproducts of evolution to optimize oxygen resources.

Evolution of Mammalian Autonomic and Communication Systems

Polyvagal Theory and Evolution of Mammals

• Evolution of mammals required two autonomic behavioral shifts:
  • Obtaining large amounts of food
  • Protecting nervous systems from oxygen loss
• These objectives are linked
• In contrast to reptiles, mammals:
  • Orient in response to novelty or threat
  • Attend and then depart/approach (fight-or-flight)
• Increasing complexity of behavior parallels increase in autonomic nervous system organization and function

Defensive World for Mammals

• Survival systems of reptiles and other vertebrates can be organized into orienting and defensive dimensions
• Mammals had to circumvent potentially lethal reactions of other species
• Evolution of mammalian nervous system enables rapid escape from danger and complex information processing
• Communication systems developed for parenting, pair bonding, and social behavior

Author's Early Research on Attention and Heart Rate

• Observed heart rate changes during attention-demanding tasks:
  • Rapid directional change in response to stimuli
  • Reduced variability when subjects focused on task
• Developed vagal tone index (RSA) to study sustained attention response
• Two-component theory of attention: phasic orienting and tonic attention
• Polyvagal Theory evolution from psychophysiological model to neuroanatomically based theory

Components of Attention in the Polyvagal Theory

• Orienting component determined by vegetative vagus originating in dorsal motor nucleus
  • Reflexive response to stimuli
  • Neurogenic bradycardia
• Voluntary engagement component determined by smart vagus originating in nucleus ambiguus (NA)
  • Depression of RSA during complex tasks and focused attention.

3. The Polyvagal Theory: New Insights Into Adaptive Reactions of the Autonomic Nervous System

Chapter 3: The Polyvagal Theory: New Insights Into Adaptive Reactions of the Autonomic Nervous System

Historical Perspectives on the Autonomic Nervous System

• In 1872, Darwin acknowledged bidirectional communication between viscera and brain through the vagus nerve (p. 69)
• Subsequent research focused on peripheral motor nerves of autonomic nervous system, with emphasis on paired antagonism between sympathetic and parasympathetic pathways
• Early conceptualization of vagus focused on undifferentiated efferent pathway
• Brainstem areas regulating supradiaphragmatic (myelinated) and subdiaphragmatic (unmyelinated) vagal pathways not functionally distinguished
• Hess proposed autonomic nervous system was integrated system with central mechanisms, anticipating need for technologies to monitor peripheral and central neural circuits

The Vagal Paradox

• In 1992, Porges suggested RSA (respiratory sinus arrhythmia) as a more sensitive index of health status than beat-to-beat variability
• Distinction between tonic functional outflow from vagus to heart (cardiac vagal tone) and global measures of heart rate variability
• Data demonstrated healthy full-term infants had greater RSA amplitude than preterm infants
• Clinical risk: neurogenic bradycardia as an indicator of fetal distress or newborn apnea
• Fetal bradycardia occurs only when RSA is depressed, raising "vagal paradox" (inconsistency between mechanisms mediating both RSA and bradycardia)
• Physiological models assume vagal regulation of heart rate and RSA amplitude; however, data show inconsistencies in their covariance

Related Concepts:

• Vagus nerve: bidirectional communication between viscera and brain (Darwin, 1872)
• Autonomic nervous system: integrated system with both peripheral and central neurons (Hess, 1954)
• RSA: functional outflow from vagus to heart (Porges, 1992)
• Neurogenic bradycardia: indicator of fetal distress or newborn apnea.

The passage describes the Polyvagal Theory, which explains how different components of the autonomic nervous system function in mammals to regulate responses to social and dangerous situations.

Polyvagal Theory: Three Phylogenetic Response Systems

Vagal Paradox:

• Researchers continue to argue for a covariation between vagal tone and heart rate variability
• This inconsistency is what the author has labeled the "vagal paradox"

Polyvagal Theory:

• Investigates phylogeny of vertebrate autonomic nervous system
• Identifies two branches of the vagus:
  • Vagal output to the heart from one branch is manifested in respiratory sinus arrhythmia (RSA)
  • Output from the other branch is manifested in bradycardia and possibly slower rhythms in heart rate variability
• Slower rhythms have been assumed to have a sympathetic influence, but are blocked by atropine

Three Phylogenetic Stages:

• Polyvagal theory articulates three phylogenetically distinct autonomic subsystems:
  • Social communication system: Involves myelinated vagus that fosters calm behavior and inhibits sympathetic influence
  • Mobilization system: Dependent on the functioning of the sympathetic nervous system
  • Immobilization system: Dependent on unmyelinated vagus, shared with most vertebrates
• These systems are phylogenetically ordered and behaviorally linked to social communication, mobilization, and immobilization strategies

Polyvagal Circuits:

• Mammals have a myelinated vagus that originates in the nucleus ambiguus and has pre- and postganglionic muscarinic receptors
• Unmyelinated vagus is shared with other vertebrates and originates in the dorsal motor nucleus of the vagus

Consistency with Jacksonian Dissolution:

• Three circuits are organized and respond to challenges in a phylogenetically determined hierarchy
• When higher circuits are rendered functionless, lower circuits rise in activity

Neuroception: Distinguishing Safe from Dangerous Environments Based on Sensory and Visceral Information

Phylogeny of Vertebrate Heart Regulation and Social Engagement System

Four Principles:

• Phylogenetic shift in regulation of heart from endocrine communication to unmyelinated nerves, then myelinated nerves
• Development of opposing neural mechanisms of excitation and inhibition for rapid metabolic output regulation
• Face–heart connection evolved as source nuclei of vagal pathways shifted ventrally from dorsal motor nucleus to nucleus ambiguus
• Increased cortical development allows greater control over brainstem via direct (corticobulbar) and indirect (corticoreticular) neural pathways

Neuroception: Contextual Cueing of Adaptive, Maladaptive Physiological States

Two Important Adaptive Tasks:

1. Assess risk in the environment
2. If safe, inhibit more primitive limbic structures controlling fight-or-flight behaviors

Neuroception vs. Perception:

• Neuroception: a neural process that enables distinguishing safe from dangerous/life-threatening contexts
• Distinct from perception as it does not require conscious awareness and may involve subcortical limbic structures

Autonomic State Regulation:

• In safe environments, autonomic state is adaptively regulated to dampen sympathetic activation and protect oxygen-dependent CNS (especially cortex)

Evaluating Risk:

• Neural evaluation of risk does not require conscious awareness and may involve subcortical limbic structures
• Neuroception: a plausible mechanism mediating expression/disruption of positive social behavior, emotion regulation, and visceral homeostasis

Features of Risk in Environment:

• Not solely driven by environmental features
• Afferent feedback from the viscera provides a major mediator of accessibility of prosocial circuits associated with social engagement behaviors
• Polyvagal theory predicts that states of mobilization (fight, flight, freeze) would compromise ability to detect positive social cues

Neurophysiological Basis for Social Interaction and Emotion Regulation

Functionally Colored Perception:

• Visceral states impact perception of objects and others
• Same person engaging another may result in different outcomes based on physiological state of target individual
• Social engagement system more accessible when in a certain state leads to reciprocal prosocial interactions
• Mobilization state may result in withdrawal or aggression in response to engagement
• Difficulty dampening mobilization circuit and enabling social engagement system in this state.

Role of Insula:

• Involved in mediating neuroception, conveying feedback from viscera into cognitive awareness
• Proposed brain structure for experiencing pain and various emotions (anger, fear, disgust, happiness, sadness)
• Represents internal body states and contributes to subjective feelings
• Activity in insula correlates with interoceptive accuracy.

Summary of Polyvagal Theory:

• Provides explanation for covariation between atypical autonomic regulation and psychiatric/behavioral disorders involving difficulties regulating social, emotional, and communication behaviors
• Emphasizes physiological states support different classes of behavior (vagal withdrawal vs increased vagal influence on heart)
• Social engagement system formed through functional and structural links between neural control of facial muscles and smooth muscle of viscera
• Proposes neuroception mechanism to trigger or inhibit defense strategies.

PART II: BIOBEHAVIORAL REGULATION DURING EARLY DEVELOPMENT

4. Vagal Tone: A Physiological Marker of Stress Vulnerability

Stress Response and Vulnerability Assessment

• Chapter 4: Vagal Tone as a Physiological Marker of Stress Vulnerability
• Individual differences in stress response to medical procedures
• Current definitions focus on treatment or response, not neurophysiological state before treatment
• Proposed method assesses both stress response and vulnerability using vagal tone

Autonomic Nervous System (ANS)

• Regulates homeostatic function
• Composed of parasympathetic (PNS) and sympathetic nervous systems (SNS)
• PNS promotes growth, restoration, and conservation of energy; deals with anabolic activities
• SNS prepares individual for intense muscular action in response to external challenges; mobilizes existing reserves

Parasympathetic Nervous System (PNS)

• Regulates various organs: eyes, lacrimal glands, salivary glands, sweat glands, blood vessels, heart, larynx, trachea, bronchi, lungs, stomach, adrenal, kidney, pancreas, intestine, bladder, and external genitalia
• Effects antagonistic to SNS when innervating the same organ
• PNS deals with bodily conservation and vital organ rest

Sympathetic Nervous System (SNS)

• Prepares individual for intense muscular action in response to external challenges
• Mobilizes existing reserves of body's energy during stress response.

Autonomic Nervous System: Stress and Homeostasis in Physiology and Pathology

Autonomic Nervous System (ANS)

Characteristics of ANS:

• Peristalsis and alimentary secretion inhibited
• Sphincter contractions block urinary and rectal outlets
• PNS and SNS are reciprocally innervated, coordinating internal state to meet demands
• PNS is modulated by internal changes in viscera
• SNS is activated by external stimuli via somatic afferent fibers

Functions of ANS:

• Facilitates digestion and conserves energy
• Optimizes organism's relationship with environment
• Responds to both internal and external stimuli
• Afferent feedback from visceral organs regulates PNS tone, impacts SNS less

Integration of ANS:

• Peripheral efferent and afferent fibers, central neural structures
• Measuring peripheral activity provides insight into brain regulation

ANS Response to Stress:

• Responds to both internal and external stimuli
• Afferents crucial in maintaining homeostasis
• Unique responses to certain stimuli (dual activation or inhibition)

Homeostasis and New Definitions of Stress:

• Many definitions limited in clinical use
• Current definitions circular, confounded by individual differences
• Lack of operational definition for stress and stressor

Physiological Stress Measurement through Cardiac Vagal Tone Monitoring

Physiological Stress: Defining Stress through Autonomic Nervous System (ANS)

Background:

• Stress not only about response to stressor but also about physiological state of the patient
• ANS deals with internal viscera and responds to external challenges
• Homeostasis: regulation of internal environment, stress: subjugation of internal needs for external ones

ANS Definition of Stress:

1. Rationale: ANS deals with servicing internal needs and responding to external challenges
2. Homeostasis vs Stress: interdependent concepts; homeostasis maintains internal states, stress responds to external challenges
3. PNS tone: indexing variable for defining stress and stress vulnerability
4. Impact on SNS state: transitory withdrawal of PNS tone may be paralleled by increased expression of SNS tone in healthy individuals
5. Chronically compromised children: low PNS tone, clinically assessed as chronically stressed or exhibiting physiologic instability

Assessing Stress: Vagal Tone Monitoring

1. Rationale: identify and quantify an index of PNS activity
2. Measurement of PNS activity: respiratory sinus arrhythmia (RSA) amplitude provides validated and easily obtainable index of cardiac vagal tone
3. Online monitoring technology: available to estimate shifts in general vagal tone
4. Organized rhythmic physiologic variability: greater amplitude indicates healthier individual and greater response potential or behavior flexibility.
5. Impact on physiological processes: efficient neural control is manifested as rhythmic physiologic variability, attenuated variability may indicate lack of physiological and behavioral flexibility in response to environmental demands.

Heart Rate Variability and Cardiac Vagal Tone in Neonates: Stress and Behavior Flexibility

Cardiac Vagal Tone and Stress Reactions

Observations in Infants:

• Lack of self-regulatory capacity to adjust rapidly to stressful stimuli

Research on Cardiac Vagal Tone:

• Reflects general PNS deficits, as demonstrated by:
  • Cardiology
  • Gerontology
  • Physical therapy
  • Diabetology
• Increased vagal tone with PNS afferent stimulation results in increased cardiac vagal tone
• RSA (respiratory sinus arrhythmia) indexes vagal influence on heart rate activity
• Amplitude of RSA provides insight into central control of autonomic processes and behavior

Relationship between Cardiac Vagal Tone and Stress:

• Greater vagal tone correlates with greater range of competent behaviors
• Conditions that compromise the CNS result in attenuation of vagal tone
• Attenuated heart rate variability indicates reduced vagal influences on the heart
• Reduced behavioral flexibility parallels reduced vagal influences

Stress Vulnerability in Neonates: An Example of Vagal Tone Monitoring

• Figure 4.1 illustrates 2 minutes of heart rate pattern and RSA for a high-risk preterm neonate (top panel) and a healthy term neonate (bottom panel)
• The healthy term neonate has much greater beat-to-beat variability than the high-risk preterm neonate
• Rapid oscillations in heart rate are associated with respiration and reflect cardiac vagal tone, indexed by RSA

Vagal Tone in Neonates: Stress & Autonomic Reactivity

Research on Respiratory Sinus Arrhythmia (RSA) in Neonates:

• Top panel: High-risk preterm neonate versus healthy full-term neonate
  • Data from a high-risk preterm neonate monitored at approximately term (top line - beat-to-beat heart rate, bottom line - RSA)
  • Data from a healthy normal full-term neonate monitored within 36 hours of delivery (same layout as above)
• Bottom panel: Distribution of respiratory sinus arrhythmia (RSA) for normal full-term neonates and neonates in the NICU
  • RSA values are in natural logarithm units per millisecond squared
• Figure 4.2 illustrates the frequency distributions of amplitude of RSA for both high-risk and normal full-term neonates:
  • Sample sizes: 125 full-term neonates and 112 NICU neonates
  • Full-term neonates were tested during second day following delivery, NICU neonates during sleep between 35 and 37 weeks corrected gestational age
• Significant difference in vagal tone between high-risk neonates and full-term neonates (F[1, 235] = 226.3, p < .0001)
  • Respiration was faster for NICU neonates but even after removing this influence, there was still a highly significant difference between the two groups (F[1, 107] = 82.2, p < .0001)
• Group classification accounted for 53.1% and 43.7% of variance in statistical model after removing respiration's influence.

Vagal Tone Shifts During Stress: The Cost of Doing Business

• Autonomic Nervous System (ANS) has many physiologic responsibilities, including regulating blood pressure and monitoring blood gases while controlling digestion and metabolism
• Vagus nerve is critical to regulation of both ergotropic and trophotropic processes: increasing vagal tone results in increases in metabolic output and modulates digestive polypeptides and gastric motility
• Vagus has direct inhibitory influences on sympathetic excitation of the myocardium, which can facilitate trophotropic states or allow withdrawal of vagal tone for immediate organism mobilization
• Cardiac vagal tone increases during development, paralleling increases in self-regulatory and exploratory behaviors
• High cardiac vagal tone is associated with better visual recognition memory in infants.

Cardiac Vagal Tone and Behavioral Reactivity to Gavage Feeding:

• DiPietro and Porges (1991) studied the relationship between cardiac vagal tone and behavioral reactivity to gavage feeding in preterm neonates
• Individual differences in cardiac vagal tone were significantly correlated with behavioral reactivity to gavage method of feeding.

Cardiac Vagal Tone and Sustained Attention:

• Huffman et al. (1998) observed that 3-month-old infants with high cardiac vagal tone habituated more rapidly to novel visual stimuli and exhibited more sustained attention than infants with low cardiac vagal tone.

Effects of Drugs on Vagal Tone:

• Atropine sulfate: dose-dependent depression of vagal tone and performance decrements (Dellinger, Taylor, & Porges, 1987)
• Inhalant anesthesia: depressed cardiac vagal tone during anesthesia, parallel increase in cardiac vagal tone as patients regained consciousness (Donchin, Feld, & Porges, 1985).

Quantifying RSA to Assess Vagal Mechanisms:

• Monitors cardiac vagal tone more accurately and relationship between vagal tone and autonomic reactivity.

Cardiac Vagal Tone as an Index of Stress and Stress Vulnerability in Newborns.

Vagal Tone and Stress:

• Vagal tone index may indicate stress and stress vulnerability (Porter et al., 1988; Porges & Porter, 1988)
• Newborns exhibit massive withdrawal of cardiac vagal tone during circumcision
• Individual differences in cardiac vagal tone correlate with heart rate reactivity to procedures

PNS as Stress Modulator:

• Proposed as the modulator of stress vulnerability and reactivity
• Physiologic basis for defining stress and homeostasis interdependent
• PNS activity can be assessed through cardiac vagal tone measurement

Quantification of Cardiac Vagal Tone:

• Measured by quantifying amplitude of respiratory sinus arrhythmia (RSA)
• Standard instrument with statistical parameters for comparison between patients and throughout life span
• Noninvasive method practical for use even with neonates

Value of Cardiac Vagal Tone Assessment:

• Allows assessment of stress impact on young infants during clinical treatments
• Identification of individuals vulnerable to stress

Conclusion:

• Usefulness of traditional stress definitions limited due to circularity and focus on SNS contribution alone
• Cardiac vagal tone proposed as a novel index for assessing stress vulnerability and reactivity with applications in various branches of medicine, particularly pediatrics.

5. The Infant’s Sixth Sense: Awareness and Regulation of Bodily Processes

Chapter 5: The Infant's Sixth Sense

Sensory Experience and Adaptation:

• Life is a sensory experience
• Sensory experiences drive behavior, contribute to organization of thoughts and emotions
• Newborn infants are bombarded with new sensory stimuli and must adapt quickly

Sensory Systems:

• Traditional model: 5 primary sense modalities (smell, vision, hearing, taste, touch)
• Vestibular system (inner ear) and proprioceptive system (body position) also contribute to sensory input
• Internal senses are often overlooked in current models

Interoception: The Sixth Sense:

• Interoception refers to conscious and unconscious monitoring of internal bodily processes
• Components of interoception:
  • Sensors located in various internal organs
  • Sensory pathways conveying information to the brain
  • Brain structures to interpret and respond to sensory information
  • Motor pathways communicating from brain to organs to change state
• Interoception is crucial for infant survival, as it provides awareness of bodily processes

Conscious vs. Unconscious Dimensions:

• Conscious: digestive processes provide conscious sensations of hunger or pain
• Unconscious: interoception influences mood and emotions without conscious awareness

Importance of Interoception in Development and Clinical Practice:

• Understanding interoception can help explain infant behavior, thoughts, and emotions
• Differences in interoceptive ability may contribute to individual differences and developmental conditions

Interoception as Foundation for Physiological Homeostasis and Social Development

Sensory Processing and Interoception

Cardiovascular and Respiratory Systems:

• Provide conscious feedback through shifts in blood pressure and blood gas concentrations of carbon dioxide and oxygen
• Unconscious awareness fosters stability (homeostasis) by adjusting motor behaviors and psychological processes

Infant's Capacity to Sense External Stimuli:

• Clinical assessment tools focus on external stimuli processing
• Current childrearing and intervention strategies do not help children sense internal states
• Infants' reactions to digestive issues demonstrate the influence of sensory systems

Interoceptive Competence:

• No methods to quantify perception of bodily processes or test unconscious interoceptive feedback
• Developmental landmarks not identified
• Interoceptive competence strongly influences infant behavior and caregiver interaction

Interoception: The Infrastructure of Higher Order Behavior

Model of Sensory Processing Levels:

1. Level I - Homeostatic Physiological Systems: Monitoring and regulating internal organs via sensory and motor pathways
2. Level II - Conscious, Motivated Brainstem Regulation: Influences homeostasis
3. Level III - Observable Behaviors: Quantity, quality, appropriateness of motor behavior
4. Level IV - Social Interaction Coordination: Successfully negotiating social interactions

Importance of Interoception:

• Interoceptive processes contribute to individual differences in information processing, emotional expressiveness, and social behavior
• Dependency on successful bodily processing for complex behaviors, including social interactions

Autonomic Nervous System Regulation of Homeostasis and Behavior

Homeostasis and Autonomic Nervous System

Level I: Maintenance of Homeostasis

• Interoceptors from internal organs transmit information to brainstem structures
• Brainstem interprets sensory data and regulates physiological organs Direct control: heart rate, blood vessel constriction/dilation, peristaltic activity Indirect control: hormone or peptide release
• Homeostasis can be down-regulated under extreme conditions or challenges

Level II: Cost of Doing Business

• Autonomic nervous system serves internal needs and responds to external challenges
• Adaptive behavioral strategies involve trade-off between internal and external demands
• Parasympathetic promotes growth and restoration, sympathetic increases energy output for challenges

Central Nervous System Role

• Regulates distribution of resources based on demands
• Perceptions or assumed threats may promote withdrawal of parasympathetic tone, excitation of sympathetic tone

Level II: Integration of Senses and Psychological Processes

• Reflexive integration in Level I is replaced by higher brain processes
• Appropriate adjustment of homeostatic processes during attention, information processing, social behavior

Sensory Stimulation and Autonomic Responses

• After baby detects sensory input, brain structures regulate autonomic organs to facilitate processing or movement towards/away from stimulus

Interoception's Role in Homeostasis

• Accurate interoception necessary for maintaining physiological balance and survival
• Defects in interoception may lead to regulatory disorders (difficulties with eating, sleeping, sensory processing, state regulation)

Physiological and Behavioral Homeostasis Parallels

• Consistent concepts: physiological homeostasis and behavioral homeostasis observed by Greenspan (1991) during infant development from birth to 3 months.

Measuring Interoception for Infant Regulation and Behavioral Assessment

Greenspan's Model and Homeostasis:

• Homeostasis in children requires regulation of sleep, behavioral states, and sensory stimulation
• Greenspan focuses on external modalities (hearing, sight, touch)
• Proposed that physiological homeostasis (Level I) and its regulation for environmental stimuli processing (Level II) are necessary substrates for behavioral homeostasis
• Empirical research supports this hypothesis with findings related to interoceptive competence in infants

Assessment of Level I and Level II Processes:

• Homeostatic processes regulated by parasympathetic nervous system via vagus nerve
• Vagus nerve accounts for approximately 80% of the parasympathetic nervous system, with sensory pathways serving interoceptors within body cavity
• Measuring vagal activity can provide information on interoception and homeostasis (Level I & II processes)
• Level I: Evaluate vagal control during rest or sleep to measure infants' capacity to maintain homeostatic control
• Level II: Assess change in vagal control during environmental challenges to determine infant's capacity to downregulate the vagal system

Research and Development:

• Research program aims to profile infant capacity to regulate internal physiological systems during sensory processing demands
• Long-term goal is to create a clinical instrument to evaluate interoception, complementing neurological, neuropsychological, and other evaluations
• Instrument will measure vagal influences on the heart through quantifying rhythmic changes in beat-to-beat heart rate pattern (respiratory sinus arrhythmia as a measure of cardiac vagal tone)
• Evaluate two dimensions of interoception: capacity to monitor and maintain homeostasis in absence of challenges (Level I processes) and ability to alter homeostasis to support behaviors required by environmental challenges (Level II processes)
• New window to observe infant's internal feelings during illness, mental processing, and social behavior.

6. Physiological Regulation in High-Risk Infants: A Model for Assessment and Potential Intervention

High-Risk Infants and Physiological Regulation

• Birth marks transition from maternal physiology to newborn self-regulation
• High-risk infants face challenges in expressing competence due to less mature or damaged nervous system
• Research on high-risk neonates can evaluate relation between specific vulnerabilities and developmental problems

Model for Assessment and Intervention

• Two research questions: assess relative risk and help newborn negotiate transition from dependency to self-regulation
• Adaptation requires complex neurophysiological systems, some of which can be monitored through observation

Clinical Management in Neonatal Intensive Care Units (NICUs)

• Compensation for immature or compromised nervous system
• Attentiveness to observable physiological systems by staff
• Use of specialized equipment for monitoring self-regulation

Importance of Nervous System Function

• Implicit assumption that assessment reflects quality of nervous system function
• Self-regulation characterizes physiological systems, maintained through bidirectional communication between central regulator and peripheral organ.

Homeostatic Self-Regulation and Neural Feedback Mechanisms in Psychopathological Development

Physiological Systems and Self-Regulation

• Individual differences in development linked to socioeconomic status, family function, nutrition, stress factors
• Psychopathology studied for internal environment impact (brain, neural regulation)
  • Focus on organismic variation, mechanisms of feedback from visceral organs contributing to emotional, cognitive, behavioral processes

Self-Regulation: Negative Feedback System

• Physiological systems regulating visceral state are self-regulatory Adjust output based on changing input through feedback
• Negative feedback opposes system state, promotes stability and homeostasis
  • Room thermostat metaphor: maintains temperature within predetermined range by detecting deviations and triggering corrective measures

Blood Pressure Regulation as a Feedback System

• Physiological feedback system with objective to maintain levels within healthy limits
• Baroreceptors in blood vessels send information about changes in pressure to brainstem, which responds by adjusting heart rate Heart rate increases when blood pressure drops and decreases when it returns to normal
• Negative feedback allows for efficient adjustment to physiological demands

Positive Feedback Systems: Destructive Prolonged Feedback

• Rage, severe anger or panic as consequences of positive feedback promoting increased metabolic output
• Prolonged periods of positive feedback can compromise health

Physiological Feedback Characteristics

• Can change based on physiological, emotional, cognitive, behavioral demands
  • Vigilant and efficient during periods requiring massive metabolic output
  • Dissociation during less motorically demanding conditions
• Therapeutic drugs, such as clonidine, can alter neural feedback system by dampening impact of afferent feedback from visceral organs

Homeostasis: Signs and Signals of Competent Neural Self-Regulation

• Maintaining physiological homeostasis crucial for newborn survival
• Not a passive process, active process in which systems vary within functional ranges
• Healthy physiological systems exhibit characteristic rhythms providing clinical information on feedback quality and system status.

Vagal System: Regulating Survival Processes in High-Risk Infants

Autonomic Response Systems: Regulation of Heart Rate Oscillations (Respiratory Sinus Arrhythmia)

• Modulated by higher brain structures and limited by neurochemical processes
• Characterized by oscillations with period determined by feedback loop duration, amplitude controlled by central regulatory control

Measures of Heart Rate Oscillations: Respiratory Sinus Arrhythmia (RSA)

• Reflect bidiirectional communication between peripheral cardiovascular system and brain
• Changes in characteristics under demand situations (e.g., stress, attention, social engagement) serve as markers of physiological self-regulation

Compromised Nervous System: Apnea, Bradycardia, and Difficulties in Thermoregulation

• Occurrence signals dysfunction in neural regulation of cardiopulmonary processes
• Interventions (e.g., physical movement, technology) help reengage neural regulation

Diabetic Individuals: External Manipulation of Deficient Internal Feedback System

• Compensate for defective endogenous feedback system regulating blood sugar through insulin release and monitoring

Human Nervous System as a Collection of Interacting Self-Regulatory Negative Feedback Systems

• Sensors/receptors assess environmental and internal conditions
• Motor systems control body movements and visceral organs
• Feedback from internal sensors interpreted by brainstem structures contributing to autonomic state regulation (e.g., nucleus tractus solitarius, dorsal motor nucleus of vagus, nucleus ambiguus)

Survival Agenda: Self-Regulation of Physiological Systems in High-Risk Infants

• Effectiveness of assessment dependent on measuring nervous system status
• Success of intervention relies on functional enhancement of the nervous system
• Focus on vagal system, a critical physiological system for high-risk infant survival (breathing, sucking, swallowing, heart rate, vocalization)
• Dysfunction in these processes places infants at risk and produces clinical indicators (apnea, bradycardia, difficulties in swallowing)

The Vagal System: An Indicator of Survival-Related Self-Regulation

• Regulates and coordinates survival processes including breathing, sucking, swallowing, heart rate, vocalization
• Neuroanatomical and neurophysiological substrate shared among these functions.

Overview of Vagal Nerve's Role and Evolution in Autonomic Regulation

The Vagus Nerve and Autonomic Self-Regulation

Nucleus Ambiguus:

• Motor fibers originate here, travel through vagus nerve (cranial nerve X) to heart and lungs
• Myelinated motor fibers provide primary control of cardiopulmonary processes

Vagus Nerve Sensory Fibers:

• Compose 80% of vagal fibers
• Provide feedback to brainstem area (nucleus tractus solitarius) on visceral organ status

Dorsal Motor Nucleus of the Vagus:

• Unmyelinated motor fibers regulate digestive system processes
• Projects to bronchi, heart in addition to nucleus ambiguus

Nucleus Tractus Solitarius:

• Integrates sensory information from visceral organs
• Communicates with primary vagus nerve source nuclei (nucleus ambiguus and dorsal motor nucleus)
• Feedback system regulates digestive and cardiopulmonary processes

Respiration:

• Determined by brainstem system
• Outputs respiratory rhythm to heart and bronchi
• Dependent on interneuronal communication between nucleus ambiguus and nucleus tractus solitarius

Polyvagal Theory:

• Emphasizes functional difference between vagal fibers from nucleus ambiguus and dorsal motor nucleus
• Provides theoretical basis for clinical assessments and interventions in neonatal intensive care unit (NICU)
• Explains how oral-esophageal stimulation can elicit bradycardia, a life-threatening vagal reflex.

The Vagal Brake and Self-Regulation in Infants - Neomammalian vs Reptilian Responses

The Role of the Vagal Brake in Stress Response:

Stress and Infant Regulation:

• Faster heart rate and higher pitch vocalizations (e.g., cries) indicate stress
• Difficulties with coordinating sucking, swallowing, and breathing are commonly observed in physiologically stressed or compromised infants

The Removal of the Vagal Brake:

• Removing the vagal brake occurs as an adaptive response to increase metabolic output and react to survival demands
• Examples: Exercise, pain, attention during eating
• Successful postpartum adaptation is related to infant's skill in regulating the vagal brake

Neomammalian Vagal Response vs. Reptilian Vagal Reactions:

• Neomammalian vagus provides protection for heart and bronchi, ensuring oxygenated blood transport
• Removal of neomammalian vagus places nervous system at risk for reptilian vagal reactions (bradycardia, apnea)

Clinical Evaluation of Vagal Function:

• RSA (respiratory sinus arrhythmia) is a measure of vagal tone from the nucleus ambiguus
• Depressed RSA during fetal distress is associated with dorsal motor nucleus vagal surge and meconium production

Hierarchical Model of Self-Regulation:

• Four levels: Homeostatic processes, sensory processing, cognitive processing, and social processing
• Higher order behavior systems depend on more primary physiological systems for functioning.

Hierarchy of Self-Regulation in Infants: Physiological & Behavioral Development

Hierarchical Model of Self-Regulation: Levels I, II, III, and IV

Level I: Neurophysiological processes characterized by bidirectional communication between the brainstem and peripheral organs to maintain physiological homeostasis.

• Represents successful regulation of internal bodily processes via neural negative feedback systems
• Interoceptors monitor internal state, transmit information via neural pathways to brainstem structures
• Brainstem structures interpret sensory information and regulate visceral state by triggering motor pathways or releasing hormones/peptides

Level II: Physiological processes reflecting input of higher nervous system influences on the brainstem regulation of homeostasis.

• Metabolic output and energy resources are modulated to support adaptive responses to environmental demands
• Homeostatic processes are compromised when facing external challenges
• Central nervous system mediates distribution of resources for internal and external demands

Level III: Measurable motor processes including body movements and facial expressions.

• Can be evaluated in terms of quantity, quality, and appropriateness

Level IV: Coordination of motor behavior, emotional tone, and bodily state to successfully negotiate social interactions.

• Contingent with prioritized cues and feedback from the external environment

Importance of Levels I and II in High-Risk Newborns:

• Achievement of these levels is crucial for survival in Neonatal Intensive Care Unit (NICU)
• Competence in regulating these processes enables maintenance and regulation of homeostatic functions like temperature, breathing, feeding, blood pressure, and sleeping
• Brainstem control systems (nucleus ambiguus, nucleus tractus solitarius, dorsal motor nucleus of the vagus) are an infrastructure for emotional regulation, social behavior, and cognitive development

Transition from NICU to Post-NICU:

• Competence in Level I and II processes is essential for successful adaptation post-NICU
• Survival after NICU depends on Level III and IV processes related to motor behavior, emotional expression, cognitive processes, and social interactions.

Neonatal Assessment and Intervention using Respiratory Sinus Arrhythmia (RSA)

Neurophysiological Assessment Strategy

Importance of Primary Physiological Systems:

• Difficulties in primary neurophysiologically dependent systems contribute to problems in:
  • Impulse control
  • Attention, concentration, creative thinking
  • Affect integration
  • Social interactions

Level I and II Processes:

• Current detailed descriptions of Level I and II processes
• Dependence on the nucleus ambiguus
• Provide a neurophysiological model that complements clinical observations

Global Assessment Strategy:

• Use RSA to assess Level I and Level II processes:
  • Baseline or sleep measure of RSA for Level I process assessment
  • Feeding test to challenge Level II process
• Evaluate autonomic substrate (Level I and II) during baseline and tasks associated with higher order processes

Level I Assessments:

• Measured RSA during minimal environmental demand in neonatal nursery
  • Distinguished between high-risk and full-term newborns
  • Related to cognitive outcome at 3 years of age

Level II Assessments:

• Measured changes in RSA during periods of well-defined environmental demands (e.g., feeding)
• Responses to feeding challenge:
  • Heart rate increased, RSA decreased, and sucking frequency increased
  • RSA depressed, heart rate increased, then returned to baseline
• Relationship between RSA recovery following feeding and degree of prematurity

Intervention Strategy:

• Measurement of RSA can assess individual differences in neural regulation of homeostatic function
• Stimulating neomammalian vagus would be beneficial, while stimulating reptilian vagus would be detrimental
• Interventions that provide sucking opportunities, oral stimulation, and facial movement may be beneficial

Regulation of Vagal Tone and RSA in High-Risk Infants: Clinical Applications of Psychophysiological Assessment Model

Shifting Posture and High-Risk Infants:

• Shift in posture of an infant elicits baroreceptor responses, heart rate change via vagus to regulate blood pressure
• Low-risk infant: negative feedback system maintains cerebral blood pressure, contributes to behavioral state regulation
  • Motor control from dorsal motor nucleus and nucleus ambiguus
• High-risk infant: depressed nucleus ambiguus function
  • Posture shifts may result in massive bradycardia and loss of consciousness
  • Similar to vasovagal syncope in older adults with low vagal tone (RSA)

Caution:

• Emphasize that high-risk infants have compromised physiological state due to low nucleus ambiguus vagal tone
• Interventions like massage, posture shifts, or suction feeding may trigger dorsal motor nucleus reflexes and bradycardia, apnea, loss of consciousness.

Conclusion:

• Model can be generalized for studying older children and adults with behavioral and psychological problems
  • Difficulties in state regulation, such as hyperactivity or attention issues, related to physiological substrate self-regulation
• Research on RSA and Level I & II processes in clinical populations:
  • Level I assessments: investigate individual differences in vagal system tonicity (e.g., panic disorders, pharmacological treatments)
    • George et al. (1989): massive decrease in RSA during hyperventilation and sodium lactate infusion
    • McLeod et al. (1992): imipramine's effectiveness on general anxiety disorders related to its influence on RSA
  • High-risk neonates have lower amplitude RSA, related to clinical condition, predict cognitive outcome
  • Donchin et al. (1992): preneurosurgical levels of RSA predicted clinical course in adults.
  • Utility of Level I assessments: high-risk infants and adults with behavioral and psychological problems.

Regulating Autonomic Functions in Children through RSA Measurements and Feeding Challenges

Regulation of Autonomic State in Children:

• Independent of RSA resting levels, children who cannot regulate RSA during attention tasks are more likely to have behavioral regulation problems (DeGangi et al., 1991)
• Inability to regulate vagal tone at 9 months predicts behavioral problems at 3 years (chapter 7)
• Hierarchical model: RSA regulation measures are predictive when baseline RSA does not predict outcome
• Alcohol and narcotics impact ability to regulate vagal reflexes:
  • Children exposed to opiates in utero exhibit attentional problems and difficulties regulating vagal tone during sustained attention (Hickey et al., 1995)

Level II Processes Research:

• Parallel between autonomic state regulation and affective regulation investigated in infants
• Bazhenova et al. studied dynamic covariation of affect tone and RSA: optimum social behavior and state regulation in infants with systematic parallel (Bazhenova, Plonskaia, & Porges, 2001)
• Preliminary research on RSA regulation during feeding challenges: individual differences found using bottle feeding, sucking, or orogastric feeding (Portales et al., 1997; Porges & Lipsitt, 1993; DiPietro & Porges, 1991)
• Standardized Level II assessment for infants evaluating nucleus ambiguus vagal tone regulation during feeding

Summary:

• Methods for assessment and intervention focus on the nucleus ambiguus in newborn infants
• Nucleus ambiguus coordinates sucking, swallowing, vocalizing, breathing via vagal pathways and heart rate control
• RSA monitoring of nucleus ambiguus function provides insight into neural regulation competence
• Noninvasive monitoring of high-risk infants or clinical populations possible to assess relative risk and evaluate intervention effectiveness
• Need for intervention research and development of age-specific interventions to enhance neural feedback critical to vagal system function.

7. Infant Regulation of the Vagal “Brake” Predicts Child Behavior Problems: A Psychobiological Model of Social Behavior

Chapter 7: Infant Regulation of the Vagal "Brake" Predicts Child Behavior Problems: A Psychobiological Model of Social Behavior

Cardiac Vagal Tone:

• Describes functional relationship between brainstem and heart
• Related to clinical risk factors in infants, outcomes in neurosurgical patients, depth of anesthesia, individual differences in temperament

Steady-State vs. Dynamic Changes in Cardiac Vagal Tone:

• Steady-state: relatively stable under quiet conditions
• Dynamic changes: sensitive to environmental demands and stimulation
• Rapid changes often parallel shifts in cardiac output to match metabolic demands

Functional Roles of Vagal Tone:

1. During low demand states, vagal tone fosters physiological homeostasis to promote growth and restoration
2. During environmental challenges, vagus acts as a "brake" to regulate cardiac output and metabolic output

• "Vagal brake" functionally inhibits sympathetic influences on the heart's pacemaker, keeping heart rate slow

The Autonomic Nervous System: A Visceral Feedback System:

• Brainstem regulates homeostatic processes through the autonomic nervous system
• Includes central regulator (brainstem source nuclei), motor output (parasympathetic or sympathetic nerves), and sensory feedback from visceral organs (chemoreceptors, baroreceptors)

Exteroceptive vs. Interoceptive Feedback:

• Cardiac vagal tone is related to both exteroceptive (environmental challenges) and interoceptive (homeostasis) feedback
• Cardiac vagal output increases for homeostatic functions, decreases to increase cardiac output for motor behaviors in response to environmental challenge

Competing Demands on the Vagal System:

• Priorities shift from optimizing visceral state (homeostasis) to optimizing metabolic output (environmental challenges)
• Servicing internal viscera vs. responding to external challenges

Vagal Brake Regulation and Social Behavior Development: Infant Study

Polyvagal Theory

• Introduces and justifies studying vagal brake through comparative neuroanatomy, embryology
• Mammals have two vagal systems: neomammalian (controlled by nucleus ambiguus) and reptilian (controlled by dorsal motor nucleus)
  • Neomammalian system: myelinated, regulates heart rate via sinoatrial node, rapid adjustment of metabolic output
  • Reptilian system: unmyelinated, little impact on cardiac output in most conditions, hypothesized to foster resource conservation during low oxygen availability
• Nucleus ambiguus is an integral component of medullary system generating respiratory rhythm
• Output of vagal fibers terminating on heart are characterized by a respiratory rhythm leading to respiratory sinus arrhythmia (RSA)
  • Amplitude of RSA provides index of dynamically changing status of vagal brake

Vagal Brake and Social Behavior Development

• Study evaluates hypothesis that appropriate withdrawal of vagal brake during infancy is marker for developmental outcome
• Proposed ability to selectively engage/disengage with environment promotes social behavior development through vagal brake mechanism
• Current study: cardiac vagal tone regulation during Bayley Scales administration (9-month assessment) predicts social behavior problems at 3 years of age using Child Behavior Checklist for Ages 2–3.

Subjects and Procedures

• 24 subjects tested initially during infancy (12 male, 12 female) from metropolitan Washington, DC area
• Mothers ranged in age from 20 to 39 years with an average of 16 years of education
• At 9-month assessment: informed consent obtained, development evaluated using Bayley Scales, ECG recording during baseline and Bayley administration.

Infant RSA and Heart Rate Responses During Bayley Scales Correlate With Behavior Problems at Age 3

Study Design and Methodology

• Mothers completed questionnaires at 9 months and 3 years old to assess infant behavior and vagal tone
• Infant Characteristics Questionnaire (Bates, 1984) and Fussy Baby Questionnaire (Green­span et al., 1987) used for predictive variables and classifying infants as Regulatory Disordered or non–Regulatory Disordered
• Child Behavior Checklist for Ages 2–3 (CBCL/2–3; Achenbach, 1988) administered when child was 3 years old to assess behavioral/emotional problems
• Quantification of Behavior Problems Data: Scores derived from CBCL/2–3 for total problems and six narrow-band syndrome scales (social withdrawal, depressed, sleep problems, somatic problems, aggressive, destructive)
• Quantification of Heart Rate Data: ECG monitored to store data on Vagal Tone Monitor, analyze RSA amplitude offline using MXedit software
• Design: Individual differences in vagal brake disengagement during Bayley test assessed through difference scores between baseline and test conditions
• Correlational analyses conducted to evaluate relation between behavior problems at age 3 and RSA/heart period reactivity

Results

• No gender differences found in baseline levels or pattern of change for heart period and vagal tone
• Condition effect: Mean heart period increased (i.e., slowed) from baseline (445 ms) to Bayley test (463 ms), F(1,22) = 10.1, p < .01
• No significant condition effect for RSA levels, F(1,22) = 0.6, p > .1
• Most subjects increased heart period (n = 19), but RSA response was more heterogeneous with 13 subjects decreasing and 11 increasing levels during the test.
• Higher baseline RSA amplitude associated with larger decreases in RSA and heart period, r(22)= .42, < .05> and r(22) = .48, < .05> respectively.
• Longer baseline heart periods correlated with greater decreases in heart period during Bayley test, r(22)= .60, < .01>

Relation Between Infant Vagal Tone and Child Behavior Problems at 3 Years

Study Findings:

• Individual differences in RSA (respiratory sinus arrhythmia) and heart period changes during Bayley test correlated
• Greater decrease in RSA linked to fewer behavior problems at age 3, especially on social withdrawal, depressed, and aggressive scales
• Baseline RSA levels related to some outcome behaviors but not others
• Multiple regression models showed that only change in RSA was a significant predictor of total behavior problem score.

Methodology:

• Correlational analyses conducted between 9-month heart period, RSA values (baseline and change scores), and 3-year behavior problems on CBCL/2–3
• Results consistent across various outcome measures and genders

Significance:

• Decrease in infant's ability to regulate vagal brake during demanding tasks linked to fewer behavioral issues at age 3.

Vagal Tone and Two-Tiered Negative Feedback System in Infant Behavior

The Role of Vagal Tone in Regulating the Autonomic Nervous System: A Two-Tiered Negative Feedback System

First Tier: Vagus Nerve and Visceral Homeostasis

• Dual functions of vagal tone: Coincides with vagal contribution to visceral homeostasis
• Represents a basic negative feedback system with a central regulator (brainstem) monitoring organ status via sensory input
• Includes the vagus nerve providing bidirectional communication between brainstem and heart for regulation of cardiac output

Second Tier: Vagus Nerve and Metabolic Regulation

• Characterized by cortical inhibition of brainstem structures controlling vagal output to the heart
• Enables metabolic demands through increasing/decreasing heart rate and cardiac output based on environmental challenges
• Modeled as dynamic interaction between cortical and brainstem structures for monitoring and regulating visceral tone and metabolic output

Functional Interaction Between Tiers:

• Allows for either increasing cardiac output to support fight-or-flight behaviors or decreasing cardiac output to calm and self-soothe.

The Role of the Second Tier in Social Behavior:

• Maximizes goal-directed behaviors that minimize unpleasant experiences and follow the law of effect
• Choreographs quality and temporal dynamics of approach-withdrawal sequences in social interactions.

Vagal Tone and the Vagal Brake: Two-Tiered Model for Regulating Social Interactions

Two-Tiered Negative Feedback Model of Vagal Tone and the Vagal Brake

Schematic Representation of Two-Tiered Model:

• Schematic representation of a two-tiered negative feedback model
• Bidirectional communication between cortical and brainstem structures

Baseline Vagal Tone (Tier 1) vs. Vagal Reactivity:

• Baseline vagal tone represents "potential energy"
• Change in vagal tone from steady state to metabolically challenging state represents "kinetic energy"
• Infants with greater baseline vagal tone have greater decreases in cardiac vagal tone and heart period during tests (e.g., Bayley test)
• Relationship between individual differences in baseline cardiac vagal tone and magnitude of heart period and vagal tone reactivity

Behavior and Vagal Brake:

• Behavior is metabolically costly, requiring shift in energy resources from visceral homeostasis to observable behaviors
• Regulation of the vagal brake provides an index of this shift in resources
• Release of the vagal brake increases cardiac output to support metabolic demands

Constructs of Vagal Tone and the Vagal Brake:

• Vagal tone (Tier 1): Represents the magnitude of vagal efferent output on the heart, associated with optimal homeostatic function
• Vagal brake (Tier 2): Represents systematic decrease and increase in vagal efferent output to the heart, reflecting release of inhibition on heart rate
• Reliable reports of decreases in indices of cardiac vagal tone (e.g., heart rate variability) in response to environmental demands
• Social behavior requires releasing the vagal brake to promote social development and fewer subsequent behavioral problems

Summary:

• The nucleus ambiguus vagal system deals with internal visceral needs and external environmental challenges
• Competence in trading off homeostatic and environmental needs is required for successful development
• Two-tiered neural feedback model provides theoretical framework to explain the relation between vagal tone during steady states and vagal reactivity (i.e., the vagal brake) in response to environmental challenges

8. The Early Development of the Autonomic Nervous System Provides a Neural Platform for Social Behavior

Early Development of the Autonomic Nervous System Provides a Neural Platform for Social Behavior

Chapter 8: The Early Development of the Autonomic Nervous System and Its Role in Social Behavior

• Infant dependence on others during first year postpartum for survival
• Rapid changes in autonomic nervous system development ensure basic needs are met
• Parallels between decrease in dependence and maturation of neural regulation of the autonomic nervous system
• Proposed role of autonomic nervous system in social behavior and clinical outcome

Dependence on Others: Parallels with Maturational Changes in the Autonomic Nervous System

• Newborns are incapable of caring for themselves, dependent on caregivers to survive
• As infant develops, dependence decreases as they become more independent and socially skilled
• Higher brain circuits regulate brainstem nuclei controlling autonomic nervous system
• Infant's ability to calm after disruptive challenges and spend time alone improves

Social Separation and Isolation: Disruption of Physiological Regulation and Development

• Social separation and isolation for humans leads to disrupted physiological state regulation and compromises physical and mental health
• Studies on Romanian orphans reveal functional and structural changes in brain regions related to social engagement and emotional processing
• Early social deprivation can impact motor development, growth, cognition, parenting stress, and atypical social behaviors.

Human Autonomic Nervous System vs. Other Vertebrates

• Unlike reptiles, human maturation does not lead to total independence from others but an ability to function independently for short periods
• Humans seek appropriate others with whom they may form symbiotic regulation dyads
• Individuals who prefer interactions with objects instead of people to regulate physiological state often receive psychiatric diagnoses.

Evolution of Autonomic Nervous System and Social Behavior in Mammals: Polyvagal Theory and Vagal Brake Development

Polyvagal Theory: Development of Vagus Nerve in Mammals

Background:

• Described as polyvagal theory (Porges, 2001a, 2007a) based on two motor branches of the vagus nerve
• Emphasizes phylogenetic shifts in neuroanatomy and adaptive behaviors

Impact on Social Behavior:

• New structures added and older ones modified for greater control over physiological state and social behavior development
• Three identifiable circuits regulate adaptive behaviors and physiological reactions to challenges

Polyvagal Theory Components:

1. Social communication: newest circuit used first, associated with facial expression, vocalization, listening
2. Mobilization: survival-oriented circuit (fight-or-flight behaviors)
3. Immobilization: oldest circuit (feigning death or shutdown)

Development of Vagal Nerve:

• Mammals have three identifiable circuits in a phylogenetically ordered hierarchy
• Newest social communication circuit is used first, followed by older circuits if necessary
• Myelinated vagus functions as an active vagal brake to inhibit or calm physiological state

Vagal Brake:

• Inhibits heart rate through myelinated vagal pathways to the sinoatrial node (SA)
• Restrains heart rate and calms individual when tonic vagal influences to SA are high
• Measured by respiratory sinus arrhythmia (RSA) amplitude in beat-to-heart rate pattern

Infant Vagal Nerve Development:

• Not fully functional at birth but continues to develop during first few months postpartum
• Myelinated fibers increase from 24 weeks gestational age through adolescence, with greatest growth between 30–32 weeks and 6 months postpartum.
• Functional improvements in visceral regulation enable better behavioral regulation and support spontaneous social engagement behaviors.

Development of RSA and its Relation to Feeding in Preterm Infants

Preterm Infants and Autonomic Regulation

Lack of Functioning Mammalian Vagus:

• Preterm infants born before approximately 30 weeks gestational age are likely compromised due to lack of an appropriately functioning mammalian vagus, or vagal brake
• Without a functioning mammalian vagus, the preterm has a limited ability to regulate visceral state and is dependent solely on the sympathetic nervous system and on the phylogenetically older unmyelinated vagus to meet physiological needs
• This compromised profile of autonomic regulation obligates the preterm infant to rely on the sympathetic nervous system to increase heart rate in response to distress, in order to support tantrums and mobilization behaviors
• Preterm infants are more vulnerable to clinically dangerous hypotensive states and lowered oxygen saturation caused by episodes of bradycardia and apnea (i.e., massive slowing of the heart and cessation of breathing), which may be triggered by ingestive behaviors (e.g., sucking and swallowing) through activity in the more primitive unmyelinated vagus that has already developed

Respiratory Sinus Arrythmia (RSA):

• RSA in preterm infants follows a maturational trajectory that parallels the reported changes in both number and ratio of myelinated vagal fibers
• During the preterm period, there is a monotonic increase in RSA from 32 to 37 weeks gestational age
• Opportunities for skin-to-skin contact (i.e., kangaroo care) between mother and preterm enhance the development of RSA
• Enhanced development of RSA is even less than reports of RSA in typically delivered full-terms

Developmental Trends in Term Infants:

• In longitudinal studies evaluating heart rate and RSA in term infants during the first year postpartum, heart rate reliably slows with age
• RSA changes are less obvious, but effects of development on RSA appear to be maximized during the first 6 months postpartum and taper during the 6–12-month period
• Individual differences in RSA during the first year postpartum are even greater than developmental shifts

Inferences from Parallel Literatures:

• RSA during early infancy reflects the functional outflow of the myelinated vagus
• Efficient RSA reactivity and recovery are dependent on both the number of myelinated vagal fibers and the ratio of myelinated to unmyelinated vagal fibers
• Increases in RSA during the last trimester through the first few months postpartum support this assumption
• The second assumption has primarily been tested during feeding when ingestive-vagal reflexes are recruited, although additional research will need to examine reactivity during social challenges during the first few months postpartum

Face-Heart Connection:

• To ingest food properly and efficiently, newborns must have the neural resources to implement the complex sequence of sucking, swallowing, and breathing
• This sequence requires the coordination of striated muscles of the face, head, and neck with myelinated vagal regulation of the bronchi and the heart
• Autonomic support for these muscles is provided by the myelinated vagus, which can be dynamically monitored by quantifying RSA
• This "face-heart" connection provides the necessary elements for an integrated social engagement system

Ingestive Challenges:

• The face-heart connection can be evaluated by measuring RSA changes during ingestive behavior (e.g., sucking)
• In healthy neonates, there is a coordinated ingestive response in which the vagal brake is systematically removed to support increased metabolic demands
• Clinically stable low-birthweight preterm infants also decreased RSA and increased heart rate during feeding

Vagal Regulation and Social Engagement Development in Infants

Study Findings:

• RSA (heart rate variability) decreases during feeding for both groups
• Postfeeding RSA recovers only in later-born infants
• Term infants and stable older preterm infants modulate vagal brake during feeding
• Social engagement system develops with increased cortical development
  • Facial muscles regulated via myelinated vagus and corticobulbar pathways
  • Includes eyelids, facial expression, middle ear, mastication, laryngeal/pharyngeal, head turning/tilting
• Social engagement system crucial for social behavior and autonomic regulation
• Polyvagal theory: myelinated vagus links social behavior with autonomic regulation

Vagal Development:

• Myelination of vagal efferent fibers begins in last trimester
  • Continues postpartum, monitored by RSA amplitude
• Vagal brake provides mechanism for increasing metabolic output during feeding
  • Releases the brake: instantaneous increase in heart rate
  • Inhibitory vagal influence reinstated: decreased heart rate
• Prematurity, illness, or neglect may affect development trajectory of the vagal circuit.

Development and Function of Autonomic Nervous System in Fetus and Infancy: Cardioinhibitory Systems

Polyvagal Theory and Autonomic Nervous System Development:

• Delays or disruptions in neural maturation can result in lower RSA levels, less efficient vagal brake reactivity, behavioral state regulation difficulties, poor affective tone, and decreased reciprocal social engagement behaviors.

Myelinated Vagus:

• Myelinated vagus is not sole mediator of autonomic state or heart rate but influences heart rate through intrinsic cardiac mechanisms, thoracic anatomy, sympathetic nervous system, and unmyelinated vagal circuit from dorsal nucleus of the vagus.
• Development of sympathetic nervous system and unmyelinated vagal circuit not extensively studied in human fetuses but assumed functioning at start of last trimester based on phylogenetic perspective.

Unmyelinated Vagus (Dorsal Motor Nucleus of the Vagus):

• Immature undifferentiated dorsal motor nucleus appears by 9 weeks gestation, with clear demarcation and subnuclei visibility by 13 weeks.
• All magnocellular subnuclei considered essentially mature by 28 weeks but may have some postnatal changes with no significant functional consequence.

Myelinated Vagus (Nucleus Ambigus):

• Mature neurons appear in rostral nucleus around 9 weeks gestation and fill the nucleus by 12.5 weeks.
• Myelination begins at 23 weeks, increases linearly till 40 weeks, and continues actively during first year postpartum.

Sympathetic Nervous System:

• Development of sympathetic nervous system less well described in literature but assumed to develop between two parasympathetic systems based on phylogenetic progression.
• Fetal heart rate monitoring suggests functional development from 16 weeks gestation with increases in heart rate during locomotor activity, indicating sympathetic activity.

Ingestive-Vagal Reflexes:

• Measuring RSA can map myelinated vagus development and monitor vagal reactivity during feeding to evaluate ingestive-vagal reflexes efficiency in preterm and term infants.
• Efficiently working ingestive-vagal reflexes contribute to social engagement behaviors by coordinating facial muscles, vocal features, and corticobulbar pathways.

Regulating Autonomic State and Social Behavior in Infants

Problems in Regulating Survival-Related Processes:

• Difficulties in regulating survival-related processes may indicate sensitive prognostic index for social behavior issues and cognitive/language skill development
• Changes in Respiratory Sinus Arrhythmia (RSA) reflect dynamic adjustment of vagal brake on heart
  • Functionally, removal of vagal brake promotes vigilance and precautionary psychological process to monitor risk
  • Induction of different physiological states allows for social behaviors or defensive fight-or-flight strategies
• Rapid vagal regulatory mechanisms enable calming and self-soothing when not necessary for safety
• Infant data: Higher baseline RSA linked to fewer negative behaviors, less disrupted during procedures, longer attention spans, easier soothing (Huffman et al., 1998)
• Behavioral state regulation critical for expressing social behaviors
• Autonomic nervous system mechanisms tightly linked to behavioral state regulation
• Greater suppression of RSA related to better state regulation, greater self-soothing, more attentional control, and greater capacity for social engagement (Calkins et al., 2007; DeGangi et al., 1991; Huffman et al., 1998; Stifter & Corey, 2001)
• Regulation of behavioral state follows a developmental trajectory during early life
  • Availability and efficient functioning of neural circuits for state regulation enables opportunities for social engagement and strong social bonds
  • Developmental limitations in vagal system (low level of RSA, difficulty regulating RSA) may result in hyperreactivity, severe self-soothing difficulties, and limited ability to calm.
• Social behavior and capacity to manage challenges dependent on neural regulation of physiological state
• Neural circuits involved in state regulation develop during gestation and continue postnatally (if available and functioning efficiently, opportunities for learning and bonding can occur; if not, social skills are difficult to learn and social bonds become challenging)
• During most life span, vagal brake and other features of the social engagement system are readily available, enabling opportunities for social learning and social bonding. Without efficient vagal brake, prosocial behavior is limited, and opportunities for social learning and social bonding are minimized.

PART III: SOCIAL COMMUNICATION AND RELATIONSHIPS

9. Vagal Tone and the Physiological Regulation of Emotion

Chapter 9: Vagal Tone and the Physiological Regulation of Emotion

• Part III: Social Communication and Relationships
• Individual differences in nervous system state influence emotion expression and regulation
• Goal: Understand mechanisms behind individual differences in emotional regulation through vagal tone

Vagal Tone

• Measurable organismic variable related to emotion regulation
• Reflects vagal control of heart

Autonomic Nervous System (ANS)

• Regulates homeostatic function
• Composed of parasympathetic nervous system (PNS) and sympathetic nervous system (SNS)
  • PNS promotes growth and restorative processes
  • SNS prepares for intense muscular action in response to challenges

Vagus: Parasympathetic Nervous System

• Originates in brainstem, innervating various target organs (e.g., heart, lungs, stomach)
• Antagonistic effects with sympathetic nervous system on visceral organs
  • SNS: dilates pupils, accelerates heart rate, etc.
  • PNS: constricts pupils, slows heart rate, relaxes sphincters, etc.

Vagus and Emotion Regulation

• Darwin's insights on vagus role in emotion regulation
  • Anticipated the link between autonomic feedback and experience of emotion
  • Acknowledged afferent capacity of vagus to transmit sensory information from visceral organs independent of spinal cord and sympathetic nervous system
  • Recognized regulatory role of pneumogastric nerve (vagus) in the expression of emotions
• Modern models of emotion regulation overlooked importance of vagal afferents and efferents

Background and Definition of Vagal Tone

• Vagus is Xth cranial nerve, originating in brainstem and projecting to various organs (e.g., heart, digestive system)
• Complex bidirectional system with myelinated branches for direct communication between brain structures and target organs
• Promotes dynamic feedback between central regulation centers and target organs to regulate homeostasis.

Vagus Nerve: Dorsal and Ambiguous Branches, Functionality and Asymmetry.

Vagal Pathways and Nuclei

• Dorsal Motor Nucleus:
  • Two source nuclei: dorsal motor nucleus or nucleus ambiguus
  • Lateralized: left vs. right dorsal motor nucleus
    • Left: innervates cardiac and body portions of the stomach, promoting secretion of gastric fluids
    • Right: innervates lower portion of the stomach, controls pyloric sphincter regulating emptying into duodenum
• Nucleus Ambiguus:
  • Asymmetrical regulation of vagal pathways
  • Lateralized: right vs. left nucleus ambiguus
    • Right: provides primary vagal input to sinoatrial (SA) node, regulating atrial rate and heart rate
    • Left: provides primary vagal input to atrioventricular (AV) node, regulating ventricular rate
  • Involved in motion, emotion, and communication
    • Regulates vocal intonation, facial expressions, and other processes
• Vagus Originating from Dorsal Motor Nucleus: "vegetative vagus"
• Sympathetic Innervation of the Heart: also asymmetrical, ipsilateral control

Evaluating Vagal Control: Respiratory Sinus Arrhythmia (RSA)

• RSA: rhythmic increase and decrease in heart rate synchronized with breathing
• Changes in RSA amplitude reflect changes in vagal efferent regulation from right nucleus ambiguus
• Supports the expression of motion, emotion, and communication by regulating metabolic output and organs involved in vocalizations

Right Hemisphere's Role in Emotion Regulation and Autonomic Function

The Relationship Between Vagal Tone, Emotional Arousal, and Attention

Perceptions and Assumed Threats to Survival:

• Can promote massive withdrawal of parasympathetic tone
• Reciprocal excitation of sympathetic tone
• Promotes fight-or-flight behaviors

Less Intense Environmental Demands:

• Characterized by less withdrawal of parasympathetic tone
• Slight increases in sympathetic tone
• Trade-off between internal and external needs regulated by central nervous system

Vagal Tone Measured via Respiratory Sinus Arrhythmia (RSA):

• Related to affect, attention, and metabolic demands
• Right branch of vagus originating in nucleus ambiguus is primary determinant of RSA
• Laterality dependent on neurophysiology and neuroanatomy of mammalian nervous system

The Right Hemisphere: The Regulation of Emotion

• Right hemisphere function related to expression and interpretation of emotions
• Implicated in attention regulation
• Right hemisphere deficits associated with aprosody or lack of emotion expression in speech
• Attenuated autonomic reactivity in individuals with right hemisphere damage

EEG Research:

• Positive emotions linked to left hemisphere and negative emotions to the right
• Asymmetry of hemispheric control of negative and positive affect
• Right hemisphere dominance for recognizing emotional aspects of stimuli, prioritizing avoidance or defensive mechanisms

The Right Hemisphere: Autonomic Regulation and Reactivity:

• Right side plays a special role in emotion regulation
• Asymmetry in control of autonomic nervous system documented
• Peripheral organs are not symmetrical in shape or placement, leading to lateralized neural control
• Emphasis on asymmetrical neural control of autonomic processes is characteristic of mammals.

Vagal Circuit for Emotion Regulation: Approach-Withdrawal Model

The Unique Role of the Right Hemisphere in Regulating Autonomic Function

Encephalization and Brain Specialization:

• The process of encephalization differs among mammalian species, with humans possessing a uniquely large cerebral cortex
• The neural control of the vagus is ipsilateral (e.g., left vagus originates in left brainstem), so the right hemisphere promotes efficient regulation of autonomic function

Right Hemisphere Responsibilities:

• Regulates homeostasis and modulates physiological state in response to internal and external feedback
• Enabled the control of other functions to evolve on the left side of the brain
• With greater encephalization, lateralized specialization is more observable

Sharing of Central Control:

• Allows for complex voluntary communication and movement via the left side of the brain
• Intense emotion-homeostatic processes are dominant on the right side of the brain
• If these processes are lateralized, they may have autonomous regulation

Right Hemisphere Dominance in Regulating Autonomic Function:

• Right cortex activation results in larger and more reliable autonomic responses
• Right hemisphere damage or dysfunction is associated with severe deficit in facial, vocal, and autonomic components of emotion expression
• Right stellate ganglion has greater cardiovascular control than left

The Vagal Circuit of Emotion Regulation: A Model:

• Approach/Withdrawal Dimension:
  • Includes movement in psychological and physical space
  • Vagal regulation of the heart modulates metabolic output to approach or withdraw
  • Vagal modulation of vocal intonations provides clues about safety to approach
• Emotion Process Stages:
  1. Cortical areas stimulate the amygdala
  2. Central nucleus of the amygdala stimulates the nucleus ambiguus
  3. Right vagus regulates heart rate and vocal intonation by communicating with the SA node and right side of the larynx
• Emotion Regulation Pathways:
  1. Sensory information from visceral organs stimulates vagal afferents, which lateralize to NTS, and then stimulate cortex, amygdala, and nucleus ambiguus
  2. Emotion state may be initiated by the visceral afferent and trigger cortical, subcortical, brainstem, and autonomic responses

Interference with Transmission on the Vagal Circuit:

• Can result in affective disorders, including emotion regulation problems or severe mood states.

Vagal Tone and Emotional Reactivity in Infants: Impact on Regulation and Expression

Dysfunctional Vagal Circuit and Emotion Regulation:

• Brain damage, neural transmission problems due to drugs, or learned dysfunction can cause issues in the vagal circuit
• Based on classical conditioning and associative learning paradigms affecting autonomic function through cortical-autonomic and amygdaloid-autonomic pathways
• Autonomic afferents to/from nucleus ambiguus may be amplified, attenuated, or blocked via neuropathy, drugs, or associative learning for different affective states

Advances in Vagal Circuit:

• Introduces vagal system in emotion physiology and emphasizes bidirectional communication between brain and body via the vagus
• Dependent on right medullary control of autonomic function through nucleus ambiguus
• Measurable noninvasively via respiratory sinus arrhythmia (RSA) quantification
• Explains individual differences due to neurophysiology and associative learning
• Consistent with brain damage research
• Provides explanation for effectiveness of interventions like non-nutritive sucking, massage, eating, exercise, yoga, cognitive strategies in emotion regulation

Vagal Regulation and Emotion:

• Concept introduced by Eppinger and Hess (1910) to explain autonomic dysfunction without known anatomical basis
• Relevant for understanding the regulation of emotions through a stimulus-organism-response approach
• Individuals with low vagal tone may have difficulties regulating emotion, expressing appropriate emotions, attending to social cues, and communicating effectively

Vagal Tone Research:

• Early work on vagal tone as a regulatory mechanism in autonomic function by Eppinger and Hess (1910)
• Vagal system important for physiological responses, behavioral reactions, facial expressivity, emotion regulation, and approach-withdrawal behaviors
• Developmental shifts in vagal tone might contribute to affective expression changes over time.

Reactivity:

• Higher vagal tone related to more organized autonomic responses with shorter latency and greater magnitude reactions
• Research on the relationship between vagal tone, heart rate, and behavioral reactivity in infants.

Individual Differences in Heart Rate Variability and Emotional Regulation

Vagal Tone and Heart Rate Variability (HRV)

Observed Variations in HRV:

• Assumed dependent on physical stimulus parameters and subject's previous history with the stimulus
• Individual differences not attributable to these were treated as experimental error

Research on Spontaneous Base-Level HRV:

• Demonstrated relationship between individual differences in spontaneous base-level HRV and heart rate reactivity
• Stimulated interest in vagal mechanisms mediating HRV and developing methods to quantify vagal influences on the heart

Studies on Newborn Infant HRV:

• Higher baseline HRV associated with larger heart rate responses and shorter latency responses to stimuli
• Only infants with higher HRV exhibited conditioned heart rate response

Behavioral Reactivity and Irritability:

• Related to vagal tone as measured by RSA (respiratory sinus arrhythmia)
• Infants with higher RSA amplitude were more reactive, required more effort to test, and had lower fundamental cry frequencies in response to surgical procedures
• Premature infants with higher RSA tone were more reactive during medical procedures

Expression of Emotion:

• Few studies have investigated vagal tone as a mediating variable for facial expressivity
• Resting HRV measures may provide an index of neural organization necessary for facial expressions

Self-Regulation:

• Relationship between cardiac vagal tone (e.g., RSA) and attention performance
• Higher vagal tone and proper suppression during attention tasks are related to better performance
• Infants with higher vagal tone are more irritable, have greater difficulty self-soothing, but eventually enhance their capacity for self-soothing

Vagal Tone and Emotional Regulation in Infants: Asymmetry, Regulation, and Expression

Vagal Tone and Emotion Regulation

Observations about Vagal Tone:

• Peripheral autonomic nervous system is asymmetrical
• Medullary regulation of autonomic nervous system is also asymmetrical
• Right nucleus ambiguus is a source nucleus for right vagus and controls larynx, SA node of heart, vocal intonation, and cardiac vagal tone
• Right central nucleus of amygdala has direct influences on right nucleus ambiguus to promote laryngeal and cardiovascular responses associated with emotion
• Stimuli processed primarily by right hemisphere produce greater cardiovascular responses than those processed by left hemisphere
• Damage to right hemisphere blunts facial expression, vocal intonation, and autonomic reactivity

Model:

• Integrates information regarding lateral brain function with regulation of peripheral autonomic nervous system
• Based on observations 1 through 6

Testing the Proposed Model:

• Recent experiment tested model linking vagal tone to right hemispheric regulation of emotion using RSA (respiratory sinus arrhythmia) as a noninvasive measure

Relationship between Vagal Tone and Emotion Regulation:

1. Correlated with autonomic reactivity: individuals with higher amplitude RSA exhibit larger autonomic responses
2. Expressivity: relation with facial expressivity dependent on development; preliminary study showed higher amplitude RSA associated with greater facial expressivity in 5-month-old infants but not 10-month-old infants
3. Self-regulation: correlated with self-regulation independent of developmental stage
4. Subset of individuals have high vagal tone and do not suppress RSA or heart rate variability during information processing, displaying regulatory disorder
5. Vagal tone increases as infant matures, paralleling range and control of emotion states

Implications:

• Useful in integrating central, autonomic, and psychological components of emotion
• Index of individual differences in homeostatic capacity to foster rapid expression and attenuation of sympathetic reactions through the vagal circuit of emotion regulation
• Autonomic nervous system has capacity for appropriate reactivity, expressivity, self-regulation, and self-soothing.

10. Emotion: An Evolutionary By-Product of the Neural Regulation of the Autonomic Nervous System

Chapter 10: Emotion - An Evolutionary By-Product of the Neural Regulation of the Autonomic Nervous System

Polyvagal Theory of Emotion:

• New theory linking evolution of autonomic nervous system to affective experience, emotional expression, vocal communication, and social behavior
• Based on phylogenetic shift in neural regulation of the autonomic nervous system

Three Phylogenetic Stages:

1. Primitive unmyelinated vegetative vagal system: immobilization behaviors associated with threat or novelty
2. Spinal sympathetic nervous system: mobilization behaviors necessary for "fight or flight"
3. Myelinated mammalian vagus: fosters engagement and disengagement, controls facial expression, swallowing, breathing, vocalization (unique to mammals)

• Hypothesized to foster mother-infant interactions and complex social behaviors
• Inhibitory effect on sympathetic pathways promotes calm behavior and prosocial behavior

Polyvagal Theory of Emotion:

• Evolution of autonomic nervous system provides organizing principle for emotional experiences
• Brainstem regulatory centers of vagus and related cranial nerves provide substrates for social behavior in mammals
• Flexibility or variability of autonomic function dependent on structure, which evolves from primitive gill arches to facial muscles, cardiac output, vocal apparatus for affective communication

Cannon's Blunder:

• Cannon emphasized sympathetic nervous system as physiological substrate of emotion
• Limited emotional experiences to mobilization responses associated with sympathetic-adrenal activity
• Neglected contribution of parasympathetic nervous system and visceral feedback
• Incompatible with earlier statements acknowledging importance of bidirectional neural communication between heart and brain via vagus nerve.

Autonomic Nervous System and Emotional Expression: Evolutionary Perspective

Darwin's Statement on Autonomic Nervous System and Emotion (1872)

• Darwin emphasized afferent feedback from heart to brain, independent of spinal cord and sympathetic nervous system
• Neurophysiological mechanisms not known at the time: vagal fibers originate in multiple medullary nuclei; branches of vagus control periphery through different feedback systems; function of branches follows phylogenetic principle

Autonomic Nervous System and Emotion (1900s - Present)

• Distinguish three components: visceral afferents, sympathetic nervous system, parasympathetic nervous system
• Each related to different aspects of affective experiences:
  • Visceral afferents: major role in determining "feelings," convey sense of hunger or nausea during emotional distress
  • Sympathetic nervous system and adrenal activity: associated with mobilization, fight-or-flight behaviors, increase cardiac output and decrease metabolic demands of digestive tract
  • Parasympathetic nervous system, especially vagus: related to emotional state, fostering growth and restoration, important for social behavior development (chapter 7)

Problems in Understanding Autonomic Determinants of Emotion

• Difficulties organizing or categorizing intensive affective states with different etiologies or behavioral expressions
• Bias towards explanations based on overt behavior (facial expression following Darwin) or sympathetic activity (Cannon's focus)
• Dominated database of autonomic correlates of affect is dominated by measures related to sympathetic function

Evolution of Autonomic Nervous System: Emergent Structures for Expression of Emotions in Humans and Animals

• Acceptance that autonomic nervous system and face play role in emotional expression, but uncertainty regarding specific autonomic "signatures" of emotions.
• Researchers have focused on sympathetic nervous system as primary physiological covariate of emotion due to Cannon's theory and limited database of autonomic correlates of affect dominated by measures related to sympathetic function.

Evolution of Autonomic Nervous System and Cardiac Control in Vertebrates

Polyvagal Theory and Autonomic Nervous System

1. Overview of Polyvagal Theory:

• Based on evolution of autonomic nervous system
• Includes rules: phylogenetic development, functional derivatives, mammalian response hierarchy

2. Regulation of Heart:

• Sympathetic-catecholamine system (chromaffin tissue and spinal sympathetics)
• Parasympathetic nervous system (vagus nerve with branches in brainstem)
  • Dorsal motor nucleus of vagus
  • Nucleus ambiguus

3. Cardiac Control in Vertebrates:

• Phylogenetic pattern: endocrine communication, unmyelinated nerves, myelinated nerves

4. Regulatory Structures Influencing Heart (Table 10.1)

5. Phylogenetic Principles:

• Neural control of heart evolves from primitive methods to complex systems
• Development of opposing neural mechanisms for rapid regulation of metabolic output

6. Cyclostomes:

• Primitive neural control with chromaffin tissue as sole excitatory influences on the heart
  • Excitatory vagal innervation acting via nicotinic cholinoceptors
  • Location of chromaffin tissue within the heart storing epinephrine and norepinephrine

7. Elasmobranchs:

• First vertebrates to have a cardioinhibitory vagus
  • Inhibitory and muscarinic cholinoceptors on the heart
  • Cardiac vagal responses to hypoxia: reducing heart rate for adjusting metabolic output
  • Limited ability to self-soothe or calm due to reliance on circulating catecholamines from chromaffin tissue

8. Vertebrates with Sympathetic and Parasympathetic Neural Control:

• Vagal influences inhibit sympathetic response, promoting shifts in behavioral state
• Teleosts: first class of vertebrates with both sympathetic and parasympathetic neural control of the heart

Evolution of Autonomic Nervous System and its Impact on Emotional Response Systems

Autonomic Nervous System Phylogenetic Development: An Organizing Principle for Human Emotion

Phylogenetic Development of Autonomic Nervous System:

• Amphibians have dual innervation of the heart via spinal sympathetic chain (increases heart rate and contractility) and brainstem vagus (produces cardioinhibitory actions)
• True adrenal glands with a distinct medulla only present in birds, reptiles, and mammals
• Neural regulation by spinal sympathetics of the adrenal medulla provides controlled release of epinephrine and norepinephrine to stimulate cardiovascular function
• In teleosts, chromaffin tissue is related to the cardiovascular system, while in amphibians it's associated with the kidney

Mammalian Vagus:

• Contains two branches: one from dorsal motor nucleus of vagus (regulates subdiaphragmatic organs) and another from nucleus ambiguus (potent inhibition of sinoatrial node)
• Mammals can down-regulate cardioinhibitory vagal tone to heart, enabling rapid increases in cardiac output without activating sympathetic-adrenal system

Phylogenetic Development and Autonomic Response Systems:

1. Chemical excitatory system: Chromaffin tissue increases cardiac output for mobilization
2. Inhibitory vagal system: Dorsal motor nucleus of vagus reduces cardiac output during scarcity to support immobilization
3. Spinal sympathetic nervous system: Promotes rapid mobilization behaviors associated with fight or flight
4. Neurally regulated adrenal medulla system: Provides more direct control over catecholamine release for prolonged mobilization requirements
5. Mammalian vagal system: Specializes into a "tonic" inhibitory system allowing graded withdrawal of the vagal brake to promote transitory mobilization without requiring sympathetic or adrenal activation

Neuroanatomical Constructs and Affective Experience:

1. Dorsal vagal complex (DVC)
2. Sympathetic nervous system (SNS)
3. Ventral vagal complex (VVC)

• Linked to specific emotion subsystems in humans: immobilize, mobilize, signal

Autonomic Nervous System: Evolution & Emotions

Autonomic Nervous System: Vestibgial vs. Adaptive Systems

Dorsal Vagal Complex (DVC)

• Primarily associated with digestive, taste, and hypoxic responses in mammals
• Includes nucleus tractus solitarius (NTS) and dorsal motor nucleus of the vagus (DMX)
• Efferents originate from DMX, primary afferents terminate in NTS
• Provides neural control of subdiaphragmatic visceral organs
• Low tonic influences on heart and bronchi
• Vestige from reptilian vagal control
• Main stimulus: hypoxia or perceived loss of oxygen resources
• Triggers severe bradycardia and apnea, often with defecation
• Beneficial functions in humans: maintains tone to gut and promotes digestive processes
• Can contribute to pathophysiological conditions like ulcers and colitis

Sympathetic Nervous System (SNS)

• Primarily a system of mobilization
• Prepares body for emergency by increasing cardiac output, stimulating sweat glands, inhibiting metabolically costly gastrointestinal tract
• Evolution follows segmentation of spinal cord
• Long been associated with emotion and contrasts to parasympathetic nervous system

Ventral Vagal Complex (VVC)

• Primary efferent fibers originate in nucleus ambiguus
• Primary afferent fibers terminate in facial and trigeminal nerves' source nuclei
• Controls supradiaphragmatic visceral organs: larynx, pharynx, bronchi, esophagus, heart
• Myelinated fibers provide tight control and speed in responding
• Involved in the control and coordination of sucking, swallowing, vocalizing with breathing.

Evolution and Dissolution: Hierarchical Response Strategy

• Polyvagal theory proposes a hierarchical response strategy to challenges
• Most recent modifications employed first; most primitive last.

Evolution of Social Behavior and Emotional Expression through Facial Expressions

Phylogenetic Strategy for Social Behavior:

• Communication via facial expressions and vocalizations is a phylogenetically based strategy
• Low metabolic demand, contingent social interactions via verbal–facial mechanisms
• Hand gestures and head movements contribute to mammalian repertoire of communication-related behavior
• Prosocial behaviors have low metabolic demand and rapid switching between engagement and disengagement strategies (speaking then listening)

Polyvagal Theory of Emotion:

• Response strategy consistent with Jackson's concept of dissolution to explain nervous system response to challenges to survival
• VVC inhibits SNS through heart, withdrawal results in "disinhibition" and strong mobilization responses
• Withdrawal of sympathetic tone leads to "disinhibition" of DVC control over gastrointestinal tract, bronchi, and heart, resulting in clinical consequences like defecation, apnea, bradycardia

Darwin's Contributions:

• Careful observations on facial expressions and emotional adaptiveness within evolutionary model
• Limited understanding of underlying physiological mechanisms and linkage between facial muscles and emotions
• Repeatedly referenced Sir Charles Bell's "Anatomy and Philosophy of Expression" for physiological explanations
• Incorporated work of Duchenne on facial muscle stimulation in emotional expressions

Subsequent Research:

• Contemporary research on emotion owes much to Darwin but lacked emphasis on neural regulation of the face or evolution of autonomic function
• Observational approach focused on organizing facial expression into affective categories, with limited investigations of specific neural regulatory processes
• Tomkins (1962, 1963) emphasized face as structure of communication and self-feedback
• Ekman (1978) and Izard (1979) developed detailed coding systems for facial affect, studying individual differences, developmental shifts, and cross-cultural consistency.

Neural Regulation and Emotional Expressions: Linking Darwin's Theory with Cranial Nerves

Polyvagal Theory and Emotions

Neural Regulation of Facial Expressions:

• Facial expressions controlled by cranial nerves
• Motor pathways from trigeminal (V) and facial (VII) nerves control facial muscles
• Nucleus ambiguus serves as source for vagal motor pathways (IX, X, XI) to pharynx, larynx, head, neck muscles

Cannon's Voodoo Death Phenomenon:

• Cannon believed extreme emotional stress could be explained by sympathetic-adrenal excitation
• Cannon described "voodoo death" as a state of shock from continuous epinephrine outpouring
• Contradictory findings: rapid heartbeat and pulse vs. slow heart rate and engagement at death

Richter's Experiment on Voodoo Death:

• Tested on rats, wild rats died quickly while domestic rats lasted hours
• Richter found no evidence of sympathetic excitation before death, but vagal overstimulation was suggested
• No physiological explanation provided for the "hopelessness" effect

Prolonged Immobility and Feigned Death:

• Prolonged immobility with slow heart rate and shallow breathing seen in rodents
• Distinguished from feigned death with sudden onset and motor collapse during active struggling

Vagal Influence on Emotional States and Immobilization Response

Polyvagal Theory of Emotion

Hofer's Observations:

• Fear-induced slowing of heart rate interpreted as vagal phenomenon
• In species with prolonged immobility:
  • 71% had cardiac arrhythmias of vagal origin
  • Only 17% in non-immobile species exhibited such arrhythmias

Polyvagal Theory:

• Sequence of response strategies to fear:
  • Removal of VVC tone
  • Increase in sympathetic tone
  • Surge in DVC tone
• Domestic rats progressed from VVC removal, to increased sympathetic tone, and death from exhaustion
• Wild rats reverted to primitive system for metabolic conservation via DVC
  • Immunobilization response with reduced motor activity, apnea, and bradycardia
  • Lethal in mammals
• Hofer's "feigned death" illustrated transition from unsuccessful struggle to immobilized state associated with DVC

Vagus Contributes to Emotional States:

• Vagus contributes to severe emotional states, including "immobilization" like extreme terror
• Polyvagal approach dissects vagal processes into:
  • High VVC tone for communication
  • Low VVC tone unopposed by sympathetic system to support mobilization
  • High DVC tone with immobilization and potentially life-threatening bradycardia, apnea, and arrhythmias

Scientific Foundations:

• Darwin's evolution concept and phylogenetic variation
• Jackson's dissolution as a model for diseases of brain function
• MacLean's identification of human brain structures associated with primitive organisms

Polyvagal Theory:

• Focuses on neural and neurochemical regulation of emotion expression and experience
• Follows Jacksonian principle that higher nervous system structures inhibit lower ones, with dissolution when the higher are suddenly rendered functionless.

11. Love: An Emergent Property of the Mammalian Autonomic Nervous System

CHAPTER 11: Love as an Emergent Property of the Mammalian Autonomic Nervous System

Background:

• Love has various expressions, including individual relationships and behaviors associated with survival, culture transmission, pleasure, ecstasy (John 4:18)
• Neurobiological processes involved in love are shared with other mammals
• Phylogenetic origins of these processes reflect their adaptive function

Focus:

• Role of the autonomic nervous system in processes associated with feelings of love and behaviors linked to reproduction

Hypothetical Model:

• Two components: appetitive phase (courting, seductive behaviors) and consummatory phase (passionate sexual behaviors, pair-bonds)
• Phylogenetically newer structures (e.g., cortex via corticobulbar pathways) regulate facial expressions and vocalizations during courting
• Phylogenetically older structures (hypothalamus, medulla) involve neuropeptides like oxytocin and vasopressin in passionate feelings

Evolution and Dissolution:

• Autonomic nervous system evolution provides substrates for emotion subsystems
• Polyvagal theory emphasizes phylogenetic changes in the autonomic nervous system as an exaptation (shift in function) of structures to express emotions
• Hierarchical response strategy: most recent modifications employed first, primitive last (VVC > DVC > SNS)
• Transitional blends between emotion subsystems may occur due to feedback and higher brain structures.

Implications:

• Mating behavior is initiated by communication via facial expressions and vocalizations for low metabolic cost
• Proximity, reproductive behavior or social distance determined based on availability
• Limits vulnerability by allowing rapid switching between engagement and disengagement behaviors.

Vagal Complex Regulates Social Engagement in Mammals through Heart Rate and Facial Expression Control

The Ventral Vagal Complex (VVC)

• Initial response to environment via signaling and communication mechanisms
• Inhibits strong mobilization responses of the Sympathetic Nervous System (SNS) at heart level
• Withdrawal of VVC leads to disinhibition of sympathetic control over heart, gastrointestinal tract, and vulnerability of bronchi and heart
  • Defecation due to relaxation of sphincter muscles and increased digestive tract motility
  • Apnea from constriction of bronchi
  • Bradycardia due to stimulation of sinoatrial node
• When all else fails, nervous system chooses metabolically conservative course for primitive vertebrates, but may be lethal for mammals

The Social Engagement System: An Emergent Property of the Ventral Vagal Complex

• Composed of somatomotor and visceromotor components
  • Somatomotor: special visceral efferents, facial expression (VII), vocalizations (IX, X), head turning (XI), filtering low frequency sounds (VII), mastication (V)
  • Visceromotor: vagal control of heart and bronchi (X)
• Efferent pathways originate in medullary structures (cranial nerves V, VII, ambiguus)
• Corticobulbar pathways enable cortical regulation of these medullary source nuclei
• On medulla level, social communication system neuroanatomically communicates with structures regulating ingestion and cardiac output
• Modulation of vagal brake can promote calming or support mobilization

The Social Engagement System in Mammals

• Includes myelinated fibers that regulate heart rate
• Rapid inhibition and disinhibition of vagal tone changes cardiac output for engagement/disengagement with objects and individuals
• Autonomic components during social interactions may be mediated by changes in vagal tone, not sympathetic arousal
• Difficulties in regulating vagal brake can result in older systems being recruited to deal with environmental challenges

Respiratory Sinus Arrhythmia (RSA)

• Heart rate pattern characterized by rhythmic increase and decrease at the frequency of spontaneous breathing
• Brainstem nuclei regulating mammalian vagus are linked to brainstem source nuclei of special visceral efferents that control facial expression, head movements, and vocalizations
• Monitoring RSA and heart rate provides an efficient method of assessing social engagement system status

Love and Hypothalamic Regulation of the Dorsal Vagal Complex (DVC) in Mammals

Polyvagal Theory and Love:

Three Phases of Neurobehavioral Model of Love:

• First Phase: Social engagement system (signal and engage a prospective mate) with vagal brake modulation (metabolic resources) during perceived safety.
• Second Phase: Mobilization to defend and facilitate proximity for reproductive behaviors when separated, via sympathetic excitation.
• Third Phase: Immobilization without fear (behavioral inhibition of motor activity) in a state defined by safety and trust of the mate.

Polyvagal Theory and Immobilization:

• Behavioral immobilization during copulation is not necessarily a response to danger or fear, but a function of safety and trust.
• Dorsal motor nucleus of vagus (DVC) involved in other functions besides shutdown behaviors: anabolic activities related to energy restoration and conservation.

Paraventricular Nucleus and DVC:

• Paraventricular nucleus (PVN) is an important regulator of the DVC, involved in responses protective and defensive.
• Communication between PVN and DVC changes with experience, may exhibit a type of learning or memory.
• Phylogenetically older vertebrates used behavior to maintain homeostasis; paraventricular nucleus evolved into structures regulating internal functions in modern species.

Evolution of Hypothalamic Regulation:

• In phylogenetically older species, paraventricular nucleus governed homeostatic behaviors through the DVC.
• With neuroendocrine mechanisms emerging, behavior was directed towards environmental challenges while neural and neuroendocrine regulation controlled internal state.
• The role of PVN in modern vertebrates retains phylogenetically older functions but also results in vulnerabilities due to potential compromise of normal physiological function upon eliciting visceral and endocrine reactions during perceived challenges to survival.

Oxytocin and Vasopressin in Dorsal Vagus Nerve Communication and Visceromotor Functions.

Oxytocin and Vasopressin

Synthesis and Release:

• Oxytocin and vasopressin are synthesized in paraventricular and supraoptic nuclei of the hypothalamus
• Central release regulates vagal output, maintaining levels optimal for homeostasis
• Peripheral release related to milk ejection, uterine contractions, ejaculation

Central vs. Peripheral Effects:

• Central vasopressin modulates afferent feedback from viscera and shifts baroreceptor reflex set points
• Peripheral vasopressin may trigger massive vagal responses via dorsal motor nucleus of the vagus
• Systemic vasopressin can induce baroreceptor-mediated withdrawal of sympathetic tone

Interplay with Oxytocin:

• During perceived safety, small increases in peripheral vasopressin may trigger oxytocin and vasopressin release from paraventricular nucleus
• Central oxytocin promotes stress resistance, while central vasopressin potentiates mobilization responses
• Lesions of vagal afferents attenuate or abolish conditioned taste aversions

Dorsal Motor Nucleus of Vagus (DMN):

• Dorsal motor nucleus sensitive to oxytocin, insensitive to vasopressin
• Nucleus ambiguus provides system for voluntary engagement with environment, associated with prosocial behaviors

Neuropeptides and Classical Conditioning in Intimacy and Fear Responses

Conditioned Love and Physiological Mechanisms Involved in Intimacy

Classical Conditioning:

• Provides a neurophysiological process to associate gastrointestinal responses with specific sensory events
• Incorporates oxytocinergic and vasopressinergic pathways connecting the paraventricular nucleus with the dorsal motor vagal complex

Two Coping Systems:

• First system: Protects from predatory attack using instrumental mobilization behaviors
• Second system: Deals with protecting the gut from toxic foods and includes hedonic appraisal of visceral stimulation during eating and copulation
• Rapidly conditioned, difficult-to-extinguish gustatory–visceral associations

Oxytocin's Role in Conditioned Love:

• Oxytocin is associated with positive states like physical proximity, touching, prosocial behavior, and food ingestion
• Oxytocin facilitates pair-bonding through sexual interactions
• Oxytocin is involved in the cephalic phase of digestion, characterized by increased gastric secretion and reduced gastric motility

Vasopressin's Role:

• Intracerebroventricular injection of oxytocin attenuates passive avoidance
• Vasopressin enhances passive avoidance
• Central levels of both neuropeptides are involved in learning social cues and partner preferences

Oxytocin vs. Vasopressin:

• Oxytocin modulates vagal function to promote homeostasis and shift visceral organs to support progenitive behavior
• In the absence of oxytocin, increases in systemic vasopressin would facilitate fear-induced avoidance
• Central vasopressin would facilitate mobilization via sympathetic excitation
• Small increases in systemic vasopressin may trigger coexcitation of central oxytocin and vasopressin with vagal and sympathetic activity

Conditioning and Other Behaviors:

• Oxytocinergic communication between the paraventricular nucleus and dorsal motor nucleus of the vagus may provide a mechanism for:
  • Proximity with a mate to be linked with positive visceral feelings
  • Other classes of behavior like parent–child bonding, friendships, and reactions to loss of a loved one

Role of Amygdala in Fear and Positive Affect, Implications for Love and Mating Behavior

Amygdala's Role in Fear Associations

• Plays a major role in retaining fear or aversive associations (Davis, 1992; LaBar & LeDoux, 1996; LeDoux et al., 1988)
• Lesions of central nucleus attenuate conditioned bradycardia and heart rate orienting response (Gentile et al., 1986; Kapp et al., 1979)

Polyvagal Theory: Immunobilization Behaviors

• Two classes: fear-related and passion-related
• Perception of safety necessary for digestion, sleep, reproduction
• Paraventricular regulation of DVC determines which processes are fostered or inhibited
• Neuropeptide modulation of DVC contributes to determination of immobilization behavior and conditioned associations

Polyvagal Theory: Oxytocin and Vasopressin's Role in Immunobilization Behaviors

• Oxytocinergic pathways from paraventricular nucleus to dorsal motor nucleus of vagus foster reproduction, safety, pleasure, ecstasy, conditioned visceral associations with mate
• Vasopressinergic pathways from paraventricular nucleus to nucleus of solitary tract and area postrema inhibit processes associated with digestion, elimination, reproduction, facilitate fight-or-flight behaviors

Polyvagal Theory: Role in Love-Related Behaviors

• Mammalian neuropeptides modulate autonomic functions during love-related behaviors
• Phylogenetically more recent vagal pathways involve voluntary behaviors for social engagement (seduction)
• Phylogenetically older DVC associated with immobilization fear system, but oxytocin co-opts function to an immobilization passion or love system by protecting organism from massive vagal surges.

Autonomic Nervous System in Mating Behavior

• Supports seduction behaviors through mammalian or smart vagus and neural regulatory structures for facial expressions and vocalizations
• Inhibition of vagal system and excitation of SNS increase cardiac output to support withdrawal from unwelcomed engagements, fighting behavior, approach behaviors
• Phylogenetically older DVC contributes to behavioral immobilization in response to fear when no mobilization option exists
• Co-opting of DVC by neuropeptides promotes sexual arousal, immobilization without fear, copulatory behavior, positive visceral experiences, and conditioned associations with the mating partner.

Rape: Physiological Shutdown Response Profile

• Characterized by massive surge from dorsal motor nucleus of vagus leading to shutdown of physiological systems (immobilization without fear)
• May exhibit great resistance to extinction following unwelcomed sexual encounters

Understanding Neurobiology of Love and Fear for Mating Behavior

Immobilization Phase and Conditioned Responses:

• Immobilization phase may follow laws of conditioning through DVC (nausea, vomiting) for fear responses
• Fear response profile seen in individuals unable to escape or perceiving no way out
• Similar response patterns as post-traumatic stress disorder
• Seduction allows mate selection and changes immobilization from fear to passion
• Intimacy without trauma initiation of immobilized love system
• Physiological differences between immobilized fear and love systems
  • Immobilized fear: physiological shutdown, inhibition of social behavior, and sexual receptivity
  • Immobilized love: heightened sexual arousal, lubrication, maintained blood pressure, raised pain thresholds
• Co-option of paraventricular communication with DVC for immobilization love circuit fostering reproductive behaviors and enduring associations

Seduction and Vagal Brake:

• Social engagement system and vagal brake enable symbolic approach behaviors and metabolic support for mate engagement
• Mismatch between partners may result in mobilization response (fight or flight) if physical distance not increased
• Successful mating and bonding sequence: seduction, proximity reduction, mobilization restricted to copulation preparation, immobilization stimulated for ease of intromission and postcoitus recovery

Hypothalamic–DVC Regulation:

• Higher brain structures determine which hypothalamic–DVC communication circuit is recruited based on perceived safety or danger
• Amygdala may play a role in maintaining learned associations if Pavlovian conditioning applies to love response.

Integration of Neuropeptides with Autonomic Nervous System:

• Two options during fear: mobilize (fight or flight) or immobilize (behavioral shutdown, loss of consciousness)
• Immobilization results in a behavioral shutdown and death feigning if no other option is available.

Neurophysiological Effects of Vasopressin and Oxytocin on Autonomic Nervous System and Emotional Responses

Vasopressin and Oxytocin's Role in Autonomic Nervous System Regulation:

• Vasopressin from parvocellular neurons inhibits feedback from viscera, promotes sympathetic activation, and increases mobilization
• Systemically released vasopressin stimulates visceral afferents and leads to massive vagal surge associated with shutdown
• Oxytocin released centrally and systematically fosters immobilized love response pattern
• Central oxytocin limits DMX output, protects homeostasis, and stimulates visceral organs
• Small increases in systemic vasopressin might trigger central avp and oxt, promoting sexual arousal

Impact of Perceived Security:

• Changes fear response system into receptive and ecstatic reproductive system
• Enhances sensory feedback, acts as a reinforcer, and modulates pain perception
• Positive visceral feelings lead to experiences of pleasure, ecstasy, and love
• Organs of fear and vigilance become organs of pleasure, nurturance, and reproduction

Monogamy Switch:

• Love may have evolved for adaptive benefits in reproduction and safety
• Individuals need to negotiate risks: vulnerability to predation and nervous system forming enduring social bonds with inappropriate mates
• Monogamy is the focal point of seduction and sexual encounters, but not all experiences lead to monogamous relationships
• Conditioned love may require a prerequisite neurophysiological state (monogamy switch) for immobilization without fear
• Disabling the monogamy switch through mobilization strategies protects oneself from monogamy during sexual encounters.

Neurophysiological Basis of Love and Pair-Bonding

Mobilization Strategies and Conditioned Love

Conditioned Love:

• Mobilization strategies engage SNS mechanisms, inhibiting conditioning processes associated with DVC mechanisms
• Example: Promiscuous sexual activity need not lead to enduring bonds if it involves limited periods of immobilization

Gender-Specific Myths and Monogamy Switch:

• Female chastity and vulnerability to first love myths promote female immobilization without fear
• Male conquering female's fears allows for permanent bonding
• Gender bias may have evolved as copulatory behavior requires only female immobilization, while male mobilizes more during the act

Biological Prenuptial and Violations:

• Interactive negotiations between mating partners on exclusive copulatory rights and security needs
• Violation of biological prenuptial (male abuse or female infidelity) can be destructive to love bond

Conclusion:

• Evolution of neural and hormonal regulation of autonomic nervous system frames mammalian love as adaptive process for reproduction and safety promotion.

12. Social Engagement and Attachment: A Phylogenetic Perspective

Chapter 12: Social Engagement and Attachment: A Phylogenetic Perspective

Purpose:

• Expand scientific knowledge of neural processes in social behavior development
• Study nervous system function and structure in the intact living individual
• Integrate new methods with existing neuroendocrine and autonomic assessment strategies

Conceptual Divide:

• Two cohorts: animal models vs clinical research on social behavior

Animal Models:

• Focus on specific neural systems, neurotransmitters, neuropeptides, hormones, brain structures as regulators of social behavior
• Differs from clinical research focusing on aberrant psychological processes in clinical populations
• Differences in terminology and definitions of social behavior

Clinical Research:

• Focuses on studying aberrant psychological processes in clinical populations
• Correlates physiological correlates with disorders, without distinguishing causes or effects

Translating Neuroscience into Clinical Practice:

• Paradox: clinical observations of social behavior linked to mental illness in children differ from research parameters studied in both animal models and normal/atypical children
• Lack of shared agenda for translating research findings into practice (assessment and treatment)
• Limited information from clinical observations regarding specific features of behavior used to define pathology enters the research environment

Social Behavior and Attachment:

• Some researchers study social behavior development in children, focusing on attachment

The Social Engagement System: Behavioral and Autonomic Interactions in Mammals

Social Engagement System: The Preamble of a Social Bond

Research on Attachment:

• Research based on Ainsworth's paradigm assessing infant responses to separation
• Assumption that attachment classification system provides insights into psychological mechanisms of disorders like reactive attachment disorder (RAD)
• Traditional attachment theory focuses only on mother–infant relations and missing mechanisms mediating engagement between individuals bonding or forming attachments

Social Engagement System:

• Close proximity necessary for establishing social bonds
• Infants have limited abilities to move towards or away from caregiver
• Balance in behavioral repertoires of reproductive partners
• Proximity dependent on voluntary motor behaviors, which are immature at birth
• Neural regulation of striated muscles of face and head available for social cues and engagement
• Facial expressions, eye gaze, vocalizations, and head orientation influence social distance
• Muscles regulated by corticobulbar pathways through five cranial nerves (V, VII, IX, X, XI)

Neural Regulation of Striated Muscles:

• Special visceral efferent pathways mediate neural regulation
• Three nuclei in brainstem: trigeminal, facial, and ambiguus
• Five cranial nerves (trigeminal, facial, hypoglossal, vagus, accessory) regulate muscles

Phylogenetic Origins:

• Social engagement system evolved from ancient gill arches
• Muscles of face and head provide potent information regarding behavioral dimensions of attachment or stress to social bond
• Facial expressivity and prosody used as clinical indicators, quantifiable responses during separation distress.

Integrated Social Engagement System:

• Behavioral and visceral components intertwined in neural regulation
• Phylogenetic shift observed in transition from reptiles to mammals
• Myelinated vagus evolved with nucleus ambiguus for social engagement behaviors and calm state promotion.

Neural Basis for Social Engagement: Polyvagal Theory and Cranial Nerves

Polyvagal Theory: Three Neural Circuits Regulating Reactivity

Evolutionary Forces and Mammalian Physiology:

• Mammalian nervous system evolved specific neural and behavioral features to maintain visceral homeostasis
• Reactions change physiological state and limit sensory awareness, motor behaviors, cognitive activity
• Mammals need to determine friend from foe, evaluate environment safety, communicate with social unit

Polyvagal Theory:

• Proposes that evolution of mammalian autonomic nervous system provides neurophysiological substrates for emotional experiences and affective processes in social behavior
• Physiological state limits range of behavior and psychological experience
• Evolution determines emotional expression, quality of communication, ability to regulate bodily and behavioral state
• Links evolution of autonomic nervous system to affective experience, emotional expression, facial gestures, vocal communication, contingent social behavior

The Social Engagement System:

• Provides an explicit neurobiological model of how difficulties in spontaneous social behavior are linked to facial expressivity and regulation of visceral state
• Proposes a mechanism explaining how these difficulties might form a core domain of several psychiatric profiles
• Deficits associated with autistic spectrum disorders: poor gaze, low facial affect, lack of prosody, difficulties in mastication
• Interventions improving neural regulation of social engagement system enhance spontaneous social behavior, state and affect regulation, reduce stereotypical behaviors, improve language skills

Anatomical Structures Involved in the Social Engagement System:

• Components of cranial nerves form a neural substrate for the social engagement system
• Provides neural structures involved in social and emotional behaviors
• Includes control component in cortex to regulate brainstem nuclei controlling eyelid opening, facial muscles, middle ear muscles, muscles of mastication, laryngeal and pharyngeal muscles, head-turning muscles
• Source nuclei communicate directly with an inhibitory neural system that slows heart rate, lowers blood pressure, promotes calm states
• Direct corticobulbar pathways reflect influence of frontal areas of the cortex on regulation of this system
• Afferent feedback through vagus to medullary areas influences forebrain areas involved in psychiatric disorders
• Anatomical structures involved in social engagement system interact with hypothalamic-pituitary-adrenal (HPA) axis, neuropeptides of oxytocin and vasopressin, immune system

Neuroception: Neural Systems for Safety Evaluation and Behavioral Response in Mammals

Social Engagement System and Disorders:

• Special visceral efferent nerves regulate muscles involved in social behaviors like facial expression, head gestures, listening to voice, etc. (Truex & Carpenter, 1969)
• Difficulties in these areas are common features of individuals with autism and other disorders

Maladaptive vs Adaptive Behavioral Strategies:

• Social engagement system compromises result in "maladaptive" behaviors that hinder social relationships
• However, these asocial strategies may have "adaptive" features
• Phylogeny of autonomic nervous system (polyvagal theory) provides insight into adaptive features

Phylogenetic Stages:

1. Ancient gill arches: regulated by special visceral efferent pathways
2. Myelinated vagus: social engagement behaviors supported
3. Sympathetic nervous system and dorsal vagal complex: defensive behaviors fostered when myelinated vagus is compromised

Neuroception:

• Perception of safety determines social behavior (prosocial vs defensive)
• Importance in forming social bonds
• Polyvagal theory explains mechanisms enabling engagement by switching from defensive to social strategies
• Neuroception: neural evaluation of risk without conscious awareness.

Understanding Neural Structures for Social Engagement and Defense in Mammals

Evolving Neural Systems in Mammals:

• Cortical regulation of subcortical structures co-opted defense functions for reproductive behavior and pair bonding (chapter 11)
• Social engagement system inhibits defense in safe environments adaptive, but maladaptive in anxiety disorders or RAD
• Invalid neuroception of safety or danger contributes to maladaptive physiological reactivity and psychiatric disorders

Allostatic Load:

• Adaptive response to risk is metabolically costly in the short term, damaging if maintained (McEwen & Wingfield, 2003)
• Duration of response distinguishes adaptive from maladaptive reactions
• Oxygen dependence of central nervous system makes apnea lethal for mammals compared to reptiles
• Temporal cortex detects risk via facial features and vocalizations (Adolphs, 2002; Winston et al., 2002)
• Functional connections between temporal cortex and amygdala inhibit defensive strategies

Neuroception and Defensive Behaviors:

• Autonomic state adaptively regulated in safe environments to dampen sympathetic activation (McEwen & Wingfield, 2003)
• New technologies identify neural structures involved in detecting risk, such as temporal lobe and functional magnetic resonance imaging
• Functional connections between amygdala and periaqueductal gray (PAG) modulate defensive behaviors and autonomic states
• Inhibitory projections from FG and STS to the amygdala allow for social behavior when no threat is present.

Neuroception and Social Behavior: Evolution of Immobilization Defense Systems in Mammals

Neural Co-opting for Social Behaviors

Amygdala and PAG Activation:

• During situations with high risk appraisal, amygdala and various areas of PAG are activated
• These structures only share connections through the central nucleus

Detection of Safety Subdues Defensive Systems:

• Detection of safety subdues adaptive defensive systems dependent on limbic structures
• Provides a plausible model for how neural detection of environmental risk (neuroception) modulates behavior and physiological state to support adaptive behaviors in response to safe, dangerous, and life-threatening environments

Co-opting Immobilization Defense System:

• Immunilization defense system is phylogenetically old and associated with reduced metabolic demands and increased pain threshold
• In mammals, immobility coupled with autonomic state shifts can be lethal due to need for oxygen
• However, immobilization without fear is co-opted to serve social needs like reproduction, nursing, and pair-bonding

Role of vlPAG in Social Behaviors:

• Immobilization defense system co-opted to support social engagement behaviors and social bonding
• vlPAG coordinates freezing behavior and is part of neural circuit regulating lordosis (hormone-dependent female immobility for copulation) and kyphotic nursing posture for infant feeding
• Lesions in caudal vlPAG decrease kyphotic nursing, litter weight gains, and increase aggression

Preliminary Model of Social Engagement:

• There are neural circuits to support social engagement behaviors and defensive strategies (fight/flight or freeze)
• Without conscious awareness, the nervous system evaluates risk and regulates adaptive behavior based on neuroception of safe, dangerous, or life-threatening environments
• Social engagement behaviors require a neuroception of safety and physiological states associated with social support
• Immunilization without fear is mediated by co-opting neural circuits regulating defensive freezing behaviors through the involvement of oxytocin, a neuropeptide involved in social bonding

Neural Pathways and Social Engagement Behavior in Psychiatric Disorders

Neuroception of Safety, Danger, and Life Threat

Autonomic State:

• Sympathetic nervous system is activated during life threat
• Dominates autonomic state to support mobilization behaviors

Defense Strategies:

• Freezing behavior coordinated by PAG
• Immobilization response controlled by dorsal vagal complex

Polyvagal Theory:

• Autonomic reactions are hierarchically organized based on phylogeny and changes in vertebrate autonomic nervous system

Evaluating Safety and Trustworthiness:

• Difficult for individuals with psychiatric diagnoses
• FG and STS areas not activated in clinical populations
• Individuals with anxiety disorders, depression, autism, schizophrenia have compromised social engagement behaviors

Neuroception of Danger:

• Evaluation of risk in environment is important for appropriate attachment and social behavior

Attachment Disorders (RAD):

• Two subtypes: inhibited and uninhibited
• Inhibited subtype characterized by absence of attachment behaviors
• Uninhibited subtype characterized by indiscriminate attachment to strangers
• Recent research suggests children with multiple caregivers may be more likely to exhibit RAD symptoms

Social Development and Caregiver Familiarity:

• Familiarity of caregiver critical for normal social development
• Familiar features (face, voice, movements) trigger inhibitory pathways to disable limbic defense system
• Study of Romanian toddlers demonstrated monotonic relation between number of different caregivers and RAD indices

Conclusion:

• Understanding contextual and social features that inhibit defensive behavioral strategies can optimize developmental consequences of neural circuits promoting social engagement.

13. The Polyvagal Hypothesis: Common Mechanisms Mediating Autonomic Regulation, Vocalizations, and Listening

The Polyvagal Hypothesis: Common Mechanisms Mediating Autonomic Regulation, Vocalizations, and Listening

Chapter Overview:

• Chapter 13 of a book on the polyvagal theory (Porges, 2001a, 2007a)
• Links phylogenetic changes in autonomic nervous system regulation to mammalian behaviors
• Emphasizes vocalizations as an intricate component of mammalian biobehavioral repertoire
• Paucity of research on neurophysiological linkage between autonomic regulation and vocalizations or acoustic information processing

Polyvagal Theory:

• Links two distinct efferent pathways in the vagus nerve: unmyelinated (ancestors) and myelinated (mammals)
• Myelinated vagus serves to foster calm behavioral states by inhibiting sympathetic influences and HPA axis
• Phylogenetically ordered autonomic subsystems: social communication, mobilization, immobilization

Mammalian Distinctions:

• Detached middle ear bones, diaphragm, myelinated vagus system
• Social engagement system involves facial expression, head movements, vocalizations, listening, and visceral state regulation
• Fossil record identifies detached middle ear bones as defining feature of mammals

Autonomic Nervous System Development:

• Three phylogenetically ordered autonomic circuits: social communication (myelinated vagus), mobilization (sympathetic nervous system), immobilization (unmyelinated vagus)
• Mammalian nervous system evolved to promote social interactions and social bonds in safe environments
• Retains three neural circuits in a phylogenetically organized hierarchy: social communication, fight-or-flight, death-feigning behaviors

Investigating Phylogeny:

• Four principles extracted from vertebrate heart regulation research provide basis for speculation on emergent behaviors and social communication.

Evolution and Functions of Social Engagement System in Mammals

Phylogenetic Shift in Heart Regulation:

• From endocrine communication to unmyelinated nerves, and finally to myelinated nerves
• Development of opposing neural mechanisms for excitation and inhibition
• Face–heart connection evolved with shift of brainstem source nuclei of vagal pathways to nucleus ambiguus

Social Engagement System:

• Comparative anatomy, evolutionary biology, embryology suggest relationship between facial muscles regulation and emergent behaviors
• Five cranial nerves control muscles of face and head: special visceral efferent pathways
• Regulates structures derived from ancient gill arches (mastication, listening, emotional expression, prosody, gesture)
• Integrated social engagement system formed with myelinated vagus and facial muscles regulation
• Control component in cortex regulates brainstem nuclei to control various muscles for filtering social stimuli and determining engagement.

Middle Ear Evolution:

• Detachment of bones at end of mandible (ossicles) forming small bones of middle ear in mammals
• Sound transduced from eardrum to inner ear via ossicular chain, reducing effect of low-frequency sounds through bone conduction.

Middle Ear Muscles: Active Filters for Auditory Sensitivity

Impact of Middle Ear Structures on Hearing

Filtering and Attenuation:

• Filtering imposed by bone separation can be further reduced with:
  • Stapedius muscle contraction (stabilizing stapes, innervated via facial nerve)
  • Tensor tympani muscle contraction (innervated via trigeminal nerve)
• Tension in these muscles reduces ossicular chain compliance and dampens low-frequency acoustic stimulation
• Similar to tightening a drum's skin, this increases pitch and reduces eardrum movement, transmitting higher frequencies to inner ear and brain
• Attenuates low-frequency sounds, facilitating voice extraction in higher frequency bands

Evolutionary Shifts:

• Detachment of middle ear bones from mandible:
  • Allowed cranial expansion and cortical development
  • Enabled hearing high-frequency airborne sounds unheard by reptiles dependent on bone conduction
• Mammalian middle ear enabled communication in a frequency band undetectable to reptiles

Impact on Survival:

• Early mammals were small, and vocal communication outside reptile range crucial for survival
• Middle ear structures allowed hearing high frequencies above background low frequencies
• With larger mammals, resonant middle ear frequency became lower, fostering infrasound communication in large species

Perceptual Advantage:

• Human perception attenuates low-frequency sounds more than high frequencies
• Db(A) scale adjusts for perceived differences in loudness based on frequency
• Middle ear muscles and structures contribute to detecting conspecific vocalizations, especially at higher frequencies

Impact of Noise Exposure:

• Stapedius muscle active even without loud noise
• Contraction attenuates low-frequency noise for unmasking high-frequency signals

Middle Ear Muscles and Perceptual Advantage in Mammals

Middle Ear Muscles and Auditory Processing

Characteristics of Middle Ear Muscles:

• Composed primarily of small, fast-twitch fibers
• High anaerobic, glycolytic, and aerobic oxidative enzyme activity, resisting fatigue
• Numerous motor end plates and axon bundles suggest small motor units
• Able to perform finely graded contractions

Middle Ear Muscles in Auditory Processing:

• Attenuate low-frequency sound waves, improving frequency sensitivity and selectivity mediated by outer hair cells
• Relevant when considering impact of low-frequency background sounds on cochlear mechanisms

Physics of Middle Ear Structures:

• Ossicular chain stiffening functions as high-pass filter, dampening low-frequency influence on inner ear
• Ossicle inertia determines highest frequencies that can pass through middle ear

Frequency Band of Perceptual Advantage:

• Lowest thresholds are observed within frequency band defined by middle ear and inner ear mechanisms
• Smaller mammals have advantage to hear higher frequencies
• Relevant conspecific vocalizations occur within this frequency band
• Two methods to weight auditory information: index of articulation and speech intelligibility index
• Vocal music triggers neural regulation of middle ear muscles, calming behavioral and physiological state

Evolutionary Adaptations for Social Communication and Listening.

The Role of Compression in Auditory Perception

• Stapedius muscle contraction reduces sound transmission at low frequencies
• Placing stimulus compression at the auditory periphery is an evolutionary adaptation to operate within a more easily achievable range
• The remaining system can process higher frequency vocalizations

Frequency Modulation and Social Communication

• Vocalizations in social contexts are usually frequency modulated within the frequency band most easily detected by conspecifics
• Danger signals may have high pitch with diminished frequency modulation at the upper edge of this frequency band
• Aggressive signaling can push vocalizations to lower frequencies outside this band (e.g., lion's roar)
• Adaptive features of this preference, but also creates challenges in detecting low frequencies and long wavelength sounds over distance

Cross-Modal Binding and Speech Intelligibility

• Facial expressivity and behavioral gestures coordinate with prosody to reduce ambiguity of acoustic message
• Areas in temporal cortex sensitive to cross-modal binding of auditory–visual inputs during vocalizations
• Concurrent speech-related visual input activates multisensory neurons in superior temporal cortex, while reduced activation seen in schizophrenics with auditory hallucinations
• Observing facial and head movements improves speech intelligibility and extracts speech from background sounds

Infant Ultrasound Vocalizations and Caregiver Protection

• Infants cannot stray far from the protection of their mother due to predominance of ultrasound vocalizations
• Rat pups shift from infantile ultrasound to adult type communication as they mature and develop mobilization behaviors
• Parallels between neural regulation of larynx, pharynx, heart, and myelinated vagus

The Cost of Active Listening for Social Communication

• Engaging in active listening within the frequency band of perceptual advantage reduces ability to detect low-frequency predator sounds
• Potential cost of social communication is reduction of predator detection, limiting listening primarily to safe environments

Polyvagal Theory and the Social Engagement System

• Development of striated muscles involved in vocalization production and listening parallel maturation of myelinated vagus
• Integrated functional social engagement system includes several neural circuits

Mammalian Vocalizations and the Polyvagal Theory - Evolution of Autonomic and Muscular Regulation in Mammals for Social Interaction and Communication.

Polyvagal Theory and Mammalian Vocalizations

• The polyvagal theory emphasizes a phylogenetic parallel in the changing neural regulation of the autonomic nervous system and the neural regulation of the striated muscles of the face and head.
• This is relevant to the study of mammalian vocalizations, as the striated muscles of the face and head are involved in both detecting and producing vocalizations.
• The polyvagal hypothesis is based on convergent phylogenetic changes in the neural regulation of structures involved in producing and detecting mammalian vocalizations.
• Mammals have a diaphragm to coordinate vocalizations with respiratory effort and volume, and two branches of the vagus: one dealing with supradiaphragmatic organs and the other with subdiaphragmatic organs.
• The neural regulation of the subdiaphragmatic vagus is involved in abdominal breathing, while the neural regulation of supradiaphragmatic vagus is coordinated with the laryngeal and pharyngeal muscles that shape the acoustic features and provide facial expressions.
• Slow exhalation enhances the impact of the myelinated vagus on the heart, promoting calm states.
• The polyvagal hypothesis proposes that acoustic characteristics of vocalization not only communicate relevant features to conspecifics, but also reflect the physiological state of the producer.
• Mammals have a myelinated vagus, diaphragm, detached middle ears, and neural circuits linking the regulation of the myelinated vagus with the striated muscles of the face and head.
• This circuit conveys and expresses states of calmness and safety, associated with greater vagal influences to the heart and lungs, increased neural tone to the middle ear muscles for optimal listening, and increased neural tone to the laryngeal and pharyngeal muscles for prosody.
• Retraction of this circuit conveys and expresses states of danger and distress, associated with faster heart rate and breathing, and high-pitched vocalizations.
• Human infants' high-pitched cries with little frequency modulation are associated with reduced cardiac vagal tone during stress.

PART IV: THERAPEUTIC AND CLINICAL PERSPECTIVES

14. The Vagus: A Mediator of Behavioral and Physiological Features Associated With Autism

Part IV: Therapeutic and Clinical Perspectives

• Vagus nerve: A critical component of an integrated model of the nervous system to understand behavioral, psychological, and physiological features associated with autism diagnosis
• Chapter 14: The Vagus: A Mediator of Behavioral and Physiological Features Associated With Autism
• Darwin's observation: Importance of bidirectional neural communication between heart and brain via the vagus nerve (pneumogastric nerve)
• Current research: Vagal afferent stimulation regulates brain structures involved in epilepsy, depression, repetitive self-destructive behaviors linked to autism
• Polyvagal theory: Three neural circuits regulating reactivity and social behavior; links evolution of autonomic nervous system to emotional expression and communication behaviors
• Phylogenetic origins: Mammals have evolved a functional neural organization that regulates visceral state for social behavior, including facial expression, vocalization, listening
• Three adaptive behavioral strategies: Social communication (myelinated vagus), mobilization (sympathetic nervous system), immobilization (unmyelinated or "vegetative" vagus)
• Functional aspect of neural control: Emphasizes the role of common brainstem structures regulating striated muscles of face and smooth muscles of viscera without assuming structural damage to vagal systems.

Neural Development and Social Communication in Autism: Polyvagal Theory Perspective

Three Phylogenetic Stages of Neural Control of Heart (Polyvagal Theory)

• Development of opposing neural mechanisms of excitation and inhibition to regulate metabolic output
• Increased cortical development leads to greater control over brainstem via direct and indirect neural pathways originating in motor cortex, terminating in myelinated motor nerves
  • Controls visceromotor (e.g., heart, bronchi, thymus) and somatomotor structures (muscles of face and head)
• Phylogenetic principles provide basis for understanding autism behaviors and responses

Vagal Brake

• Tonic vagal influences on sinoatrial node inhibit pacemaker, lowering heart rate
• High vagal tone acts as a brake on beating rate, enabling engagement/disengagement with environment and self-soothing behaviors
• Low vagal tone allows no inhibition of pacemaker, increasing sympathetic activation for defense

Polyvagal Theory and Autism

• Deficits in social engagement system (facial expressivity, autonomic regulation) may contribute to autism symptoms
  • Compromises spontaneous social behavior, social awareness, affect expressivity, prosody, language development
• Interventions targeting neural regulation of social engagement system may enhance spontaneous social behavior and state regulation

Social Engagement System Components

• Control component in cortex (upper motor neurons) regulates brainstem nuclei (lower motor neurons) controlling facial muscles, head movements, listening, ingestion, vocalization, language, and orientation
  • Determines social experiences
• Source nuclei communicate with inhibitory neural system promoting calm states
• Direct corticobulbar pathways reflect frontal cortex influence on regulation of this system
• Afferent feedback through vagus to medullary areas influences forebrain areas involved in psychiatric disorders
• Interactions with hypothalamic-pituitary-adrenal (HPA) axis, neuropeptides, and immune system

Vagus Nerve's Role in Autism: Heart Rate Variability, Stimulation & Behavioral Impact

Neural Mechanisms of Eye Contact and Listening to Human Voice:

• Neural pathway raising eyelids also tenses stapedius muscle in middle ear, facilitating hearing human voice (Borg & Counter, 1989)
• Defective neural regulation of middle ear muscles linked to language delays, learning disabilities, and autistic spectrum disorders (Smith et al., 1988; Thomas et al., 1985)
• Middle ear infection (otitis media) can result in total inability to elicit stapedius muscle reflex (Yagi & Nakatani, 1987)
• Disorders affecting facial nerve function, such as Bell's palsy, influence stapedius reflex and speech discrimination abilities (Ardic et al., 1997; Wormald et al., 1995)

Predictions Based on Polyvagal Theory:

• Autistic individuals have difficulties recruiting neural circuit regulating social engagement system
• Behaviors suggest removal from direct social contact through defensive strategies (mobilization or immobilization)
• Limited facial expressions, head gestures, and ability to extract human voice from background sounds due to neural regulation of muscles

Vagal Regulation and Heart Rate:

• Myelinated vagus synapses on sinoatrial node produces respiratory sinus arrhythmia (RSA) rhythmic pattern in heart rate
• Greater cardioinhibitory influence through myelinated vagus results in greater RSA amplitude
• Autistic children show reduced or dampened transitory heart rate responses to stimuli (Hutt et al., 1975; Althaus et al., 1999; Zahn et al., 1987; Palkovitz & Wiesenfeld, 1980; Corona et al., 1998)

Vagal Nerve Stimulation:

• Effective treatment for epilepsy and depression
• Vagal afferent stimulation provides direct input to lower motor neurons in brainstem and upper motor neurons regulating social engagement system
• Recent reviews detail neurophysiological basis for intervention but lack acknowledgment of interaction between vagus and facial muscles (Porges, 2001a)
• Rocking behaviors in autistic individuals may reflect naturally occurring strategy to stimulate vagal system through baroreceptor feedback loop.

Vagal Nerve Stimulation Study on Autism:

• Vagal nerve stimulation reduced autistic-like behaviors in patients with hypothalamic hamartoma and medically refractory epilepsy (Murphy et al., 2000).

Vagal Regulation in Autism: Behavior, Gut, Immune System, and HPA Axis Dysfunctions

Vagal Nerve Stimulation and Autism Behaviors

• During vagal nerve stimulation, four out of six patients with autistic behaviors showed impressive improvements: poor communication, ritualisms, compulsions, no social skills, injury to self and others
• Impressive improvements were reversed when stimulation was discontinued without worsening seizure frequency

Vagal Regulation of the Gut in Autism

• High prevalence of gastrointestinal symptoms in individuals with autism
• Link between gut and brain as a determinant of autism has been studied due to parent reports of secretin reducing symptoms
• No evidence for efficacy of secretin in randomized, placebo-controlled trial
• Compromised vagal regulation of gastrointestinal processes in autistic individuals
• Vagus is a primary regulator of the gut with afferents providing information to brain structures

Role of Vagal Afferents in Modulating Sensory Experiences and Eating Disorders

• Involved in regulating satiety via vagovagal reflexes
• Regulate nociceptive sensations via solitary-spinal pathways
• Vagal afferent activation by binge eating and vomiting activates descending pain inhibitory pathway, resulting in elevated pain threshold
• Elevated pain thresholds found in anorexia nervosa subjects
• Ondansetron administered as intervention for bulimia nervosa due to its ability to prevent vagally mediated emesis

Vagal Regulation of the Immune System

• Subdiaphragmatic vagal afferents may provide a targeted signal to central structures regulating immune function
• Vagal efferent pathways linked to immune function through motor pathways to thymus and direct inhibition of sympathetic nervous system
• Neural mediation of myelinated vagus may trigger state promoting immune function
• Withdrawal of vagal tone through mobilization strategies increases sympathetic tone and HPA axis activation, suppressing immune function
• Afferent vagus mediates behavioral depression but not fever in response to peripheral immune signals following abdominal inflammation

Vagal Regulation of the HPA Axis

• Vagus is involved in regulating HPA axis and exhibits inhibitory influence on cortisol secretion
• Coordinated response promotes metabolic activity and mobilization behaviors by withdrawing vagal tone through myelinated vagus and increasing sympathetic activity and HPA axis activation

Autism and Dysfunctional Regulation of the HPA Axis

• Poorly developing autistic children more likely to have abnormal diurnal rhythm and response on dexamethasone suppression test than less severe cases
• Negative feedback mechanism of HPA axis may be disturbed in autistic children, especially poorly developing individuals
• Most autistic patients failed to suppress cortisol with dexamethasone test

Vagal System as an Organizing Principle

• Involved in expressing several disparate symptoms associated with autism: neural regulation of striated muscles via special visceral efferent pathways, dysfunctional target organ regulation, and influence on pain thresholds, HPA axis, immune system, and nucleus of the solitary tract

15. Borderline Personality Disorder and Emotion Regulation

Chapter 15: Borderline Personality Disorder and Emotion Regulation

Background:

• Diagnosis dates back to early 1800s, originally used for patients with neurotic and psychotic symptoms
• First listed as an Axis II diagnosis in DSM-III (1980)
• Cluster of symptoms: affective instability, intense relationships, difficulty controlling anger, impulsivity, suicidal tendencies, and self-mutilation
• Impact on approximately 2% of the population, more prevalent in women
• Associated with poor outcomes including job problems, relationship difficulties, social maladjustment, and reduced academic achievement

Causes:

• High correlation with past sexual abuse and family dysfunction
• Developmental hypothesis: trauma early in life can lead to BPD development
• Comorbid with mood and anxiety disorders

Neurobiological Mechanisms:

• Impairments in prefrontal cortex and limbic structures involved in emotion regulation
  • Smaller frontal lobes (Lyoo et al., 1998)
  • Poorer performance on go/no-go tasks (Völlm et al., 2004)
• Anomalies in neurotransmitter systems, such as serotonin and HPA system dysfunction

Autonomic Nervous System:

• Hypothesis: hyperarousal of sympathetic nervous system and depression of parasympathetic nervous system.
• Previous research contrasted physiological responses regulated by autonomic nervous system in individuals with BPD and controls. (Herpertz et al., 1999; Schmahl et al., 2004)

Investigating Vagal Brake Regulation in Borderline Personality Disorder Using Respiratory Sinus Arrhythmia

Autonomic Nervous System and Borderline Personality Disorder (BPD)

Studies on Autonomic Reactivity in BPD:

• Herpertz et al. (1999): No evidence of sympathetic hyperarousal associated with a diagnosis of BPD; did not monitor parasympathetic component or dynamic emotional stimuli
• Schmahl et al. (2004): No sympathetic hyperarousal but no measurement of parasympathetic nervous system or dynamic emotional stimuli

Polyvagal Theory as a Framework:

• Phylogenetic model of the autonomic nervous system provides an innovative framework to study parasympathetic involvement in BPD
• Emphasizes integrated social engagement system and myelinated vagus for calming visceral state and dampening sympathetic activity
• Autonomic reactions follow a phylogenetically ordered hierarchy with three distinct adaptive strategies: social engagement, dorsal vagal, and sympathetic nervous systems
• Neuroception is the unconscious process of evaluating risk and safety through subcortical systems

Myelinated Vagus in Mammals:

• Parallel shift from unmyelinated to myelinated vagus in facial expression muscles
• Myelinated vagus inhibits defensive limbic circuits and establishes social bonds

Function of the Myelinated Vagus (Vagal Brake):

• Inhibits sympathetic nervous system's influence on the heart
• Dampens HPA axis activity
• Actively maintains calm states in social contexts
• Amplitude of respiratory sinus arrhythmia (RSA) indexes the state of the vagal brake

Hypothesis for BPD:

• Difficulties in regulating vagal brake in social settings
• Contrast RSA regulation between BPD patients and controls during emotional film clips presentation and social interactions.

BPD Study: Emotional Response and Autonomic Function Analysis in Film Clip Experiment with Controlled Groups

Study Participants:

• BPD group: referred by clinicians at St. Elizabeth's Hospital (Washington, DC)
• Control group: volunteers recruited by National Institutes of Health
• Similar education level and age
• No drug or alcohol abuse
• No current prescription or illicit drugs
• BPD diagnosis confirmed using DSM-IV criteria and validated interviews
• Tested at St. Elizabeth's Hospital, control group tested offsite

Procedure:

1. Participants seated in a quiet room facing TV screen with ECG electrodes
2. Three film clips (conflict scenes and neutral) shown during experiment
3. Heart period and respiratory sinus arrhythmia (RSA) data collected for analysis
4. Experiment lasted approximately 1 hour, participants instructed to minimize movements
5. Experimenter remained in room for equipment monitoring and questions about film clips

Film Clips:

• Two conflict scenes: one from "Frances" and another from "The Great Santini" rated highly emotional (7.25 and 9.15) compared to neutral scene (1.75) on a Likert scale
• Participants' ratings confirmed assumed emotional content of each film sequence
• No significant differences in ratings between groups

Data Quantification:

1. Vagal Tone Monitor detected peak R-wave and stored heart period data for offline analyses
2. Sequential R–R intervals edited using MXedit software to remove outliers due to movement or digitizing errors
3. RSA calculated by converting time-based heart period data to frequency domain, filtering, and log transforming the variance in the 0.12–0.40 Hz band associated with spontaneous breathing
4. Sensitive marker of myelinated vagal influence on heart rate as shown in previous studies (Denver et al., 2007)

Analyses:

• Group (Borderline, Control) by Condition (Baseline, Film 1, Film 2, Film 3) analyses of variance (ANOVA) used for RSA and heart period data analysis.

Vagal Regulation and Heart Period Changes in Borderline Personality Disorder.

Experiment Design

• Heart period measured as time interval between successive R-waves of ECG
• Metric for analysis: average R–R interval in msec per condition
• Evaluate vagal contribution to heart period changes with correlations between changes from baseline in heart period and RSA

Results

• Significant group effect on RSA: F(1,77) = 7.16, p < .05 (higher in control group)
• Group × condition interaction for RSA: F(3,51) = 3.62, p < .05
  • Control participants exhibited increase in vagal influences to heart
  • BPD participants exhibited vagal withdrawal
• Significant group effect on heart period: F(1,77) = 14.2, p < .05 (shorter in BPD group)
• Group × condition interaction for heart period: F(3,51) = 6.49, p < .05
  • BPD participants exhibited shorter heart periods throughout experiment
  • Control participants exhibited longer heart periods throughout experiment

Vagal Contribution to Heart Period Changes

• Correlations between change from baseline in heart period and RSA within each group
  • Strong correlation only in control group (Figure 15.2)
  • BPD participants have poor vagal regulation, changes in heart period may be due to other influences

Discussion

• Previous studies focused on sympathetic nervous system in BPD with no differences found
• Current study focuses on parasympathetic limb of autonomic nervous system, first report of unique characteristics of autonomic regulation associated with BPD diagnosis.

Autonomic Nervous System Differences in BPD and Social Interactions

Polyvagal Theory Insights from Experiment

• Physiological state of BPD group characterized by vagal withdrawal, supporting fight or flight behaviors
• Control group's physiological state featured increased vagal influence on the heart, promoting spontaneous social engagement
• Social interactions with stranger (experimenter) might trigger defense strategies in BPD group, leading to physiological state change and defensive behaviors
• Film clips may contribute to need for mobilization in experiment
• Correlations between RSA and heart period support strong link between vagal regulation and control of heart period in individuals without psychiatric disturbances
• Limitations: small sample size, isolated experimental manipulation, no measures of test–retest reliability
• First documented evidence of autonomic nervous system differences between controls and BPD patients
• Study offers theoretical framework to explain emotional reactivity linked to BPD
• Potential for additional research into autonomic response profile in social challenges and measuring neuroception in BPD patients.

16. Abuse History Is Related to Autonomic Regulation

Abuse and Autonomic Regulation

Impact of Abuse

• Many individuals experience abuse in childhood or adulthood (Desai et al., 2002)
• Women are highly vulnerable to victimization, especially by those close to them (Bremner & Vermetten, 2001)
• Effects of abuse may include mood disorders like depression (Schuck & Widom, 2001; Arata et al., 2005) and maladaptive coping mechanisms (Rothschild, 2000) leading to substance abuse, eating disorders, and suicide (Doyle, 2001)
• Abuse may not result in severe debilitating symptoms of PTSD but can still impact daily experiences and social relationships

Autonomic Nervous System and Abuse

• Few studies on effects of abuse on autonomic nervous system, mainly focused on chronic PTSD (Buckley & Kaloupek, 2001)
• Inconsistent results regarding baseline heart rate differences (Prims et al., 1995)
• Heightened physiological reactivity to traumatic event stimuli in individuals with PTSD (Elsesser et al., 2004)
• Assessment of cardiovascular regulation variables during baseline and following a stressor may provide insight into impact on physiological response strategies

Vagal Regulation and Social Engagement

• Deficits in vagal regulation found in perpetrators of violent abuse (Umhau et al., 2002) and related to psychiatric disorders like PTSD, generalized anxiety disorder, depression (Sack et al., 2004; Sahar et al., 2001; McLeod et al., 2000; Rottenberg et al., 2005)
• Vagal regulation linked to emotional reactivity, social engagement, and reactions to stress (see chapter 7)

Vagal Brake and Exercise

• Rapid withdrawal of vagal inhibition on heart during challenges demands mobilization followed by recovery of vagal tone after exercise for calm states (vagal brake)
• Deficits in vagal regulation present in individuals with a history of abuse leading to difficulties in feeling safe with others and developing trusting social relationships

Yoga as an Alternative Strategy

• Individuals practicing yoga may be exercising their autonomic nervous system to normalize abuse-related damage to self-regulation abilities (Lee et al., 2004; Sovik, 2000)
• Yoga can help reduce symptoms of depression and anxiety, increase a sense of self-efficacy, and improve regulation of the autonomic nervous system.

Investigating Impact of Abuse History on Autonomic Regulation and Psychological Well-Being in Women without PTSD Diagnosis

Study Hypotheses:

• Participants with a history of abuse but no PTSD diagnosis will exhibit greater physiological coping difficulties characterized by lower RSA and less RSA recovery following mild exercise
• Abuse history will be related to greater use of dysfunctional coping strategies, increased mood disturbances, and lower self-concept

Participants:

• 49 female participants recruited from a local yoga studio
• Majority were in committed relationships (69.4%) and had children (46%)
• Most had college and graduate education
• Between 17 and 66 years old, no participant reported PTSD but diagnoses of depression (7) and anxiety disorders (4) were present

Heart Rate Data:

• Heart rate increased post exercise regardless of abuse history

Responses to Abuse History:

• RSA was related to abuse history
  • Participants with abuse history had lower levels of RSA
  • After exercise, their RSA did not recover to pre-exercise levels
• Dysfunctional coping strategies more prevalent in those with abuse history
• Lower self-concept reported by participants with abuse history

Impact of Abuse Type:

• Participants were grouped into no abuse, child abuse only, and adult abuse with/without child abuse groups
  • Those reporting adult abuse had the lowest pre-exercise RSA levels and least recovery post exercise

Cumulative Abuse Index:

• Higher self-reported index of abuse associated with greater decrease in RSA following exercise

Discussion:

• A higher percentage of reported abuse than expected based on normative data (e.g., Administration on Children Youth and Families Children's Bureau, 2006)

Impact of Abuse on Autonomic Nervous System & Vagal Tone in Women Practicing Yoga

Impact of Abuse History on Autonomic Nervous System and Psychological Functioning

Background:

• Some women with abuse history are experienced practitioners in yoga
• Hypothesized that their yoga training may help self-regulate and cope with physiological reactions
• Abuse history may "tune" the autonomic nervous system towards defensive mobilization strategies

Findings:

1. RSA (respiratory sinus arrhythmia):
   • Lower RSA prior to mild exercise in women with abuse history
   • Poor RSA recovery following exercise
2. Vagal Brake:
   • Abuse history may lower tonic influence of the vagal brake
   • Difficulties shifting from mobilized state to calmness
3. Self-Concept and Mood Disturbances:
   • Individuals with abuse history had lower self-concept
   • Graded relation between cumulative abuse experiences and both self-concept and mood disturbances
4. Polyvagal Theory:
   • Consistent with the polyvagal theory, focusing on adaptive functions of autonomic reactivity
   • Abuse experiences may "retune" the autonomic nervous system
5. Implications:
   • Compromised ability to express socially "trusting" behaviors
   • Hypervigilance for danger and facilitating fight-or-flight responses
6. PTSD:
   • Triggering unmyelinated vagus as a primitive defense system in inescapable contexts may lead to PTSD
   • Lower brainstem system regulates peripheral physiology, reducing oxygenated blood flow and leading to dissociation

Exploring the Impact of Trauma on Autonomic Nervous System Regulation and Social Engagement

Study Findings:

• Lower threshold to mobilize and hypervigilance for danger: may have survival consequences in protective sense
• Individuals with PTSD history: might react similarly to those with abuse history during exercise challenge
• Plausible explanation: mechanisms mediating fight-or-flight reactions clinically observed in individuals with histories of abuse
• Importance: demystifying personal experiences and understanding multidimensional impact on psychological and physiological domains
• Autonomic regulation retuning: a key feature in trauma and abuse assessments and interventions
• Treatment strategies: enabling clients to shift from fight-or-flight state to calmer physiological state for efficient access to psychological mechanisms.

Study Limitations:

• No evaluation of individuals with PTSD
• Only plausible explanation based on the study's findings.

17. Music Therapy, Trauma, and the Polyvagal Theory

Chapter 17: Music Therapy, Trauma, and Polyvagal Theory

• Music in Human Experience:
  • Used for education, rituals, expressions
  • Calming effect, building community
  • Intertwined with emotion & psychological processes
  • Transmits cultural values
• Music Therapy:
  • Involves dynamic interactions between therapist, client, and music
  • Enhances physical health and mental wellbeing
  • Facilitates regulation of bodily and behavioral states
• Polyvagal Theory:
  • Nervous system evaluates risk in environment
  • Identifies features of safety or danger
  • Low-frequency sounds: sense of danger, shift attention to potential dangers
    • Shared with other vertebrates
  • High-pitched screams: sense of urgency or empathy
• Music and Physiological State:
  • Elicits a variety of emotional experiences and physiological states
  • Paralleled with feelings of safety, danger, or life threat
  • Influences affect regulation, social engagement behaviors, communication
  • Changes emotive state and elicits changes in physiology.
• Musicophilia by Oliver Sacks (2007):
  • Music is part of human experience but not fully understood
  • No specific brain area or circuit identified for music processing.

Polyvagal Theory Links Music Processing and Social Engagement Behavior

Polyvagal Perspective

• From a polyvagal perspective, processing and expressing music is viewed as converging neural mechanisms required for music processing and social engagement behaviors
• This convergence is neurophysiologically determined and explained by the polyvagal theory

Polyvagal Theory

• Emerged from studying evolution of vertebrate autonomic nervous system (ANS)
• Based on functions regulating heart, lungs, and gut
• Brain dynamically regulates ANS through bidirectional communication
• Neural regulation of ANS linked to neural regulation of facial muscles signaling emotional state

Music Therapy and Polyvagal Theory

• Polyvagal theory explains how music therapy can recruit neural mechanisms for:
  • Social interactions between client and therapist
  • Listening and expressing music
• These features of music therapy promote restorative affective states and prosocial behavior

Biobehavioral Quest for Safety, Survival, and a Painless Death

• Polyvagal theory proposes that mammalian ANS provides neurophysiological substrates for emotional processes and stress responses
• Physiological state limits adaptive behaviors and psychological experiences
• Evolution of nervous system determines range of emotional expression, quality of communication, and ability to regulate body/behavioral state

Face–Heart System

• Integrated face–heart system enabled complex facial gestures and vocalizations associated with social communication
  • Smiling reflects calm state and triggers safety in observer
  • Angry face reflects mobilized state and triggers defensive state in observer
• Muscles regulated by the social engagement system act as filters of social stimuli and determinants of engagement with social environment

Middle Ear Muscles and Social Engagement System in Trauma Recovery

Neural Pathways Regulating Social Engagement System

Orbicularis Oculi Muscle:

• Sphincter muscle around the eye involved in expressive displays
• Also regulates stapedius muscle in middle ear via neural mechanisms

Difficulties in Social Engagement Behaviors:

• Common features of autism, PTSD, and other psychiatric disorders
• Includes avoidant gaze, nonresponsiveness to voice, reduced facial affect, diminished vocal prosody, and atypical head gestures

Social Engagement System Components:

• Somatomotor (e.g., poor gaze, low facial affect, lack of prosody, difficulties in mastication)
• Visceromotor (difficulties in autonomic regulation including cardiopulmonary and digestive problems)

Trauma and Social Engagement System:

• Compromises spontaneous social behavior, social awareness, affect expressivity, prosody, and language development
• Devastating consequences following life threat compromise subsequent social behavior and emotion regulation
• Attempts to socially engage traumatized individuals may result in defensive strategies of rage and anger
• Life threat triggers a neural circuit that severely limits social engagement behaviors and distorts neuroception, resulting in false detection of risk

Music and Prosodic Vocalizations:

• Provide an alternate portal to the social engagement system
• Can avoid initial face-to-face interactions that may be misinterpreted as threat by a traumatized individual

Middle Ear Evolution:

• Detached middle ear bones enabled mammals to communicate in a frequency band not detected by reptiles
• This critical neural regulation of middle ear muscles is defective in individuals with language delays, learning disabilities, and autistic spectrum disorders
• Middle ear infection can result in total inability to elicit the stapedius reflex
• Disorders affecting facial nerve function (e.g., Bell's palsy) not only influence the stapedius reflex but also affect speech discrimination

Music Therapy and Polyvagal Theory: Social Engagement System Activation.

The Effect of Vocal Music on Social Engagement System

Polyvagal Theory:

• Vocal music duplicates vocal prosody's effect and triggers neural mechanisms regulating social engagement system
• Facial affect and autonomic state change, leading to improved mood

Social Engagement System and Melodies:

• Frequency band of melodies similar to index of articulation in human speech
• Effectively stimulates social engagement without requiring face-to-face interaction

Trauma and Social Engagement:

• Trauma can turn off the social engagement system
• Therapeutic strategies engaging direct eye contact may trigger defensive behaviors
• Music therapy provides a safe portal to reactivate the social engagement system

Polyvagal Theory Application in Music Therapy:

• Two integrated processes:
  1. Face-to-face interaction invites neuroception of safety
  2. Frequency band associated with melodies engages neural regulation of social engagement system
• Breathing patterns during music therapy enhance calming effects and health benefits

Deconstructing Music Therapy:

• Face-to-face interaction triggers neuroception of safety when effective
• Vocal music engages neural regulation of social engagement system with positive outcomes
• Polyvagal perspective: Calm physiological state, improved socioemotional behaviors, and enhanced growth and restoration.

PART V: SOCIAL BEHAVIOR AND HEALTH

18. Reciprocal Influences Between Body and Brain in the Perception and Expression of Affect

Part V: Social Behavior and Health

• Emotions, affect regulation, and interpersonal social behavior: Describe basic human experiences in response to events, challenges, and people
• Shape sense of self, form relationships, determine safety contexts and with specific people
• Complex interplay between psychological experience and physiological regulation
• Dependent on dynamic bidirectional communication between peripheral organs and central nervous system

Affect and Interpersonal Social Behavior as Biobehavioral Processes

• Neural circuits: Provide bidirectional communication between brain and heart, triggering protective or social behaviors
• Peripheral reactions can initiate brain detection of danger, alter perceptions
• Reciprocal influences between body state and brain determine quality of psychological processes

Neuroception and Environmental Features of Safety/Danger

• Neural surveillance mechanisms (neuroception): Brain identifies features of risk or safety
• Hardwired reactions reflect adaptive strategies from phylogenetic history
• Specific features recruit physiological states associated with feelings of safety, danger, life threat
• Each state characterized by specific capacities for affect regulation and social engagement/communication

Affective Neuroscience Research

• Current research: Brain structures and neural circuits related to motivational/emotional processes
• Overlooked neurobiological substrate: Reciprocal communication between body states and brainstem, impacting availability of affective circuits
• Bidirectional circuit: Enables mental/psychological processes to influence body state and vice versa
• Dependence on lower brain regulation of visceral state for accessibility of prosocial emotions/restorative states

Polyvagal Theory as an Organizing Principle

• Focuses on neural circuits between higher brain structures, brainstem, and visceral organs mediated through autonomic nervous system
• Emphasizes role of physiological state in accessibility of prosocial emotions/restorative affective states

Physiological State and Psychotherapeutic Treatments

• Conceptualizing social interaction as a biobehavioral process: Supports non-pharmacological treatments relying on social interactions and interpersonal behaviors
• Changing neural regulation of physiological state to support further benefits from interpersonal interactions

Neurophysiological Regulation and Mental Health: A Holistic Approach

Importance of Physiological Monitoring:

• Provides insight into reactions not observable in overt behavior
• Neural regulation of face and viscera (e.g., heart) linked to brain circuits
• Bidirectionality between peripheral and central structures, as explained by Gellhorn (1964) and Darwin (1872)

Neurophysiological Background:

• Hess awarded Nobel Prize in Physiology or Medicine for central regulation of visceral state (1949)
• Disconnect between subjective affective experience and visceral state regulation in contemporary research
• Imaging techniques and neurochemistry focus on brain structures involved in adaptive behaviors

Role of Neural Regulation of Visceral State:

• Potentiates or dampens motivational circuits (e.g., seeking, rage, fear, lust, care, panic, play) based on physiological state
• Vagal withdrawal and high sympathetic excitation: fast heartbeat, low threshold for aggression
• Engaged myelinated vagus: dampened reaction to stimuli, options for further social interactions

Limitations of Parallelism Perspective:

• Overlooking contributions of peripheral sensory inputs and motor outputs in central circuits
• Hess' awareness of complex systems functioning as a whole (1949 Nobel speech)

Mental Health Research:

• Prevalent strategies focus on clinical features without measurable physiological substrate
• Neurophysiological variables used as correlates for clinical diagnosis, not defining anxiety or depression

Anxiety as Dependent on Autonomic State:

• Potential new research strategies focusing on sympathetic tone and contexts less likely to trigger high excitation
• Lack of interest in mapping autonomic regulation as a vulnerability dimension within psychiatry and psychology.

Historical Overview of Autonomic Nervous System and Arousal Theories.

Autonomic Nervous System: A Historical Perspective

Background:

• Researchers have measured autonomic variables for over a century as indicators of emotional state and perceived stress
• Early arousal theories assumed peripheral physiological measures regulated by the sympathetic branch were accurate indicators of brain "arousal" or "activation"
• Arousal theories neglected the importance of prosocial affective states, defensive strategies like immobilization, and parasympathetic nervous system (PNS)

Limitations of Arousal Theories:

• Assumption of a unitary arousal system in research areas like sleep, deception, sexual behavior, anxiety
• Emphasis on fight-or-flight behaviors and sympathetic activation, neglecting inhibitory neural pathways
• Lack of understanding about brain structures regulating autonomic function, evolution of the ANS, interactions with immune system, hypothalamic-pituitary-adrenal axis, oxytocin and vasopressin
• Neglect of the role of the PNS and bidirectional communication between brain structures and visceral organs

Polyvagal Theory:

• Emerged from studying the evolution of the vertebrate autonomic nervous system
• Proposes that social behaviors and vulnerabilities to emotional disorders are "hard-wired" into our nervous system
• Offers an understanding of mental health and treatment techniques for communication and relation skills

Key Concept: Polyvagal theory combines "poly," meaning many, and "vagal," referring to the vagus nerve, a primary component of the autonomic nervous system. The theory proposes two branches of the vagus related to different behavioral strategies: one for social interactions in safe environments and another for adaptive responses to life threat.

Evolution of Autonomic Nervous System & Biobehavioral Safety Response

Autonomic Nervous System: Paired-Antagonism Model vs Polyvagal Theory

Paired-Antagonism Model:

• Characterized autonomic nervous system as a constant battle between sympathetic (fight or flight) and parasympathetic (growth, health, restoration) systems
• Balance theories attempted to link "tonic" imbalances to physical and mental health

Polyvagal Theory:

• Proposes the autonomic nervous system reacts to real-world challenges in a hierarchical manner
• Phylogenetic changes in autonomic nervous system determine how it reacts to challenges
• In humans and other mammals, hierarchy is composed of three neural circuits: myelinated vagus (newest), sympathetic, unmyelinated vagus (oldest)
• Older vagal circuit involved in immobilization and decrease in metabolic resources; newer vagal circuit regulates calm states that promote social engagement and health

Evolutionary Context:

• Mammals must determine friend from foe, navigate stress to form social behaviors and cognitive processes
• Physiological state limits the range of adaptive behaviors and psychological experiences
• Evolution of mammalian nervous system provides neurophysiological substrates for affective processes and stress responses

Homeostasis Domains:

• Typically focused on visceral systems: cardiovascular, digestive, reproductive, immune functions.

Phylogenetic Shifts and Autonomic Circuits for Adaptive Behavior

Phylogeny and Autonomic Regulation

Three Principles of Vertebrate Heart Regulation:

• Phylogenetic shift from endocrine communication to unmyelinated nerves, then myelinated nerves
• Development of opposing neural mechanisms for excitation and inhibition
• Increased cortical control over brainstem via direct (corticobulbar) and indirect (corticoreticular) pathways

Brain-Face-Heart Circuit:

• Emergence of a vagal system that "cues" others of safety and danger
• Integrated system responds rapidly, selectively regulates magnitude and specificity of reactions
• Paralleled increase in neural control of heart via myelinated mammalian vagal system

Polyvagal Theory:

• Distinction between two branches of the vagus nerve (Xth cranial)
• Proposed that each vagal branch is associated with a different adaptive behavioral and physiological response strategy to stressful events
• Three phylogenetically defined autonomic circuits: social engagement, mobilization, immobilization.

Polyvagal Circuits:

• Social Engagement System (prosocial behaviors)
  • Cues others of safety and allows replacement of precautionary strategy with social interactions
• Mobilization System (defensive fight-or-flight behaviors)
  • Allows rapid response to threats without severe metabolic cost or adrenal activation
• Immobilization System (freezing, death feigning)
  • May be associated with dissociative psychological states.

Evolution of Mammalian Autonomic System for Social Engagement

Polyvagal Theory Assumptions:

• Evolution modified the autonomic nervous system (ANS) of mammals
• Mammalian ANS retains vestiges of phylogenetically older systems
• Emotional regulation and social behavior derived from structural changes in the ANS due to evolutionary processes
• Three response strategies: cranial nerves for facial expression, sympathetic-adrenal system, inhibitory vagal system
• Phylogenetic hierarchy: oldest structures first, then fight or flight, mammals have complex facial gesture and vocalization system

Mammalian Vagus as a Vagal Brake:

• Myelinated efferent pathways function as an active vagal brake
• High vagal tone inhibits heart rate, acts as restraint
• Low vagal tone allows uninhibited pacemaker, leading to increased metabolic output for mobilization or self-soothing behaviors

Social Engagement System:

• Emerged in mammals to detect and express signals of safety and foster proximity
• Involves cranial nerves V, VII, IX, X, and XI regulating facial expressions, intonation vocalizations, and heart via myelinated vagus fibers
• Capable of dampening sympathetic nervous system activation and hypothalamic-pituitary-adrenal axis activity through calming viscera and regulating facial muscles.

Social Engagement System: Neural Basis and Disorders in Behavioral Regulation

Social Engagement System:

• Innervates striated muscles regulating structures derived from ancient gill arches (Truex & Carpenter, 1969)
• Control component in cortex regulates brainstem nuclei controlling facial expressions, eye gaze, etc.
• Phylogenic origin intertwined with autonomic nervous system
• Includes myelinated vagus regulated by nucleus ambiguus
• Muscles function as neural gatekeepers expressing safety features through prosody and facial expressions

Autonomic Nervous System:

• Special visceral efferent nerves innervate striated muscles
• Interneuronal connections between source nuclei and myelinated vagus provide inhibitory pathway to slow heart rate, lower blood pressure
• Influenced by higher brain structures and visceral afferents
• Direct corticobulbar paths reflect influence of frontal areas on medullary source nuclei
• Feedback through afferent vagus influences both source nuclei and forebrain areas involved in psychiatric disorders
• Anatomical structures interact with hypothalamic-pituitary-adrenal axis, social neuropeptides, immune system (Carter, 1998; Porges, 2001b)

Social Engagement System and Psychiatric Disorders:

• Deficits in both somatomotor (gaze, facial affect, prosody, difficulties with ingestion) and visceromotor components
• Compromises spontaneous social behavior, social awareness, affect expressivity, language development
• Interventions that improve neural regulation may enhance social engagement behaviors and communication skills.

Disorders of Social Engagement System:

• Autism: poor gaze, low facial affect, lack of prosody, difficulties with mastication (clinical features)
• Social anxiety: difficulties expressing social behavior and reading social cues
• Post-traumatic stress disorder: social engagement behaviors impeded due to autonomic arousal.

Neuroception: Distinguishing Safe vs Dangerous Environments

Polyvagal Perspective and Social Engagement System

Core Component Characteristics:

• Depressed social engagement system
• Consequences: poor affect regulation, recognition, physiological state regulation
• "Maladaptive" behavioral strategies have "adaptive features"

Phylogenetic Development of Autonomic Nervous System in Mammals

1. Myelinated vagus (ventral) - supports high levels of social engagement behavior
2. Unmyelinated vagus, sympathetic nervous system - foster mobilization (fight or flight), immobilization (death feigning, freezing, shutdown) behaviors
3. Neural regulation associated with social engagement system is integrated into myelinated vagus, compromised social engagement leads to:
   • Changes in autonomic state
   • Difficulties in behavioral state regulation
   • Loss of neural regulation to facial muscles (flat affective expression)
4. Potential risks: physical (cardiovascular disorders), mental (anxiety disorders, depression) if removal is prolonged

Neuroception: Contextual Cueing of Adaptive and Maladaptive Physiological States

1. Adaptive tasks for mammals: assess risk and inhibit primitive limbic structures that control fight/flight or freeze behaviors
2. Social interaction promotes a sense of safety through processing sensory information (temporal cortex, superior temporal sulcus)
3. Inhibition of defensive circuits enables social engagement and calm visceral states to emerge
4. Neuroception: neural process that evaluates risk and matches neurophysiological state with actual environmental risk
5. Mismatch between nervous system's evaluation of safety and individual's experience can result in physiological states supporting fight/flight or freeze behaviors instead of social engagement
6. New technologies (functional magnetic resonance imaging) have identified neural structures involved in detecting risk, especially temporal cortex and its connectivity to amygdala
7. Invalid neuroception of safety or danger may contribute to maladaptive physiological reactivity and express defensive behaviors associated with specific psychiatric disorders. However, for most individuals neuroception accurately reflects risk and there is consistency between cognitive awareness and visceral response to risk.

Co-opting Defense Systems for Social Behavior in Mammals

Relationship Between Visceral Feedback and Prosocial Behaviors

• Visceral feedback from the viscera plays a significant role in mediating accessibility of prosocial circuits associated with social engagement behaviors.
• The polyvagal theory predicts that states of mobilization compromise our ability to detect positive social cues.
• Visceral states color perception of objects and others; same features of a person engaging another may result in different outcomes depending on physiological state.
• If individual is in a state of mobilization, reciprocal prosocial interactions are unlikely to occur, as they might be responded with asocial features like withdrawal or aggression.

Role of Insula in Mediating Neuroception and Internal Body States

• The insula may be involved in mediating neuroception due to its proposed role in conveying feedback from the viscera into cognitive awareness.
• Functional imaging experiments demonstrate that the insula has an important role in pain experience, emotion (including anger, fear, disgust, happiness, and sadness), and interoceptive accuracy.

Co-opting Immobilization Defense System for Reproductive Behaviors, Nursing, and Formation of Social Bonds

• Immobilization as a defense system is phylogenetically old and associated with reduced metabolic demands and increased pain threshold.
• In mammals, inhibition of movement coupled with autonomic state shifts to support immobilization behavior (apnea and bradycardia) can be lethal due to oxygen requirements.
• However, immobilization without fear is required for certain mammalian social behaviors like reproduction, nursing, and pair-bonding.
• The periaqueductal gray area coordinating immobility as a primitive defense system has been modified in mammals to serve intimate social needs, with the ventral lateral portion rich in oxytocin receptors associated with parturition, nursing, and pair-bonding.

Co-opting Mobilization Defense System for Play

• Playful "rough and tumble" behaviors are characterized by mobilization, sharing neurophysiological substrate with defensive fight-or-flight behaviors through sympathetic excitation and withdrawal of myelinated vagal pathways.
• How play is distinguished from aggressive behavior, and how anger is contained to resume play, involves access to the social engagement system to signal benign intentionality.
• Autism is associated with noninteractive (parallel) play due to difficulties in accessing the social engagement system.
• Play requires reciprocal interactions and constant awareness of others' actions to restrain mobilizations, differentiating it from fight-or-flight behaviors.
• Jogging and other forms of exercise result in a physiological state similar to team sports or rough and tumble play but lack the social engagement component required for polyvagal definition of play.

The Neuroscience of Social Engagement and Play Regulation: Polyvagal Theory Explanation

Polyvagal Theory

Background:

• Attempt to reorganize conceptualization of autonomic nervous system
• Focuses on specific neural circuits and adaptive functions, including affect, emotions, goal-directed behaviors

Key Features:

1. Role of brain structures and neural circuits in regulating autonomic state
2. Distinguishing dynamic vagal output to target organs
3. Impact of visceral afferents and sensory feature detectors on switching neural circuits regulating autonomic state
4. Relation between regulation of visceral organs and social engagement behaviors

Implications:

• Affective, emotional states dependent on lower brain regulation of visceral state
• Specific bodily states foster different domains of behavior

Polyvagal States:

1. Social Engagement:
   • State promoting positive social interactions and sense of safety
   • Dependent on a well-defined social engagement system
2. Mobilization (Fight or Flight):
   • State supporting fight-or-flight behaviors
   • Requires increase in metabolic output
3. Play:
   • Blend of mobilization and social engagement states
4. Immobilization (Life Threat):
   • State associated with life threat and reduction of metabolic output
   • Shutdown behaviors may be lethal for mammals

Understanding Autonomic Regulation and Social Engagement for Health and Healing

Polyvagal Theory and Affective Neuroscience:

• Five physiological states: immobilization without fear, vigilance, danger, safety, and social engagement
• States color perception of others; same engaging response may result in different outcomes based on individual's state
• S-O-R model: stimulus-organism-response with neuroception as an intervening process

Polyvagal Perspective:

• Emphasis on phylogenetic shifts in visceral regulation
• Three types of fear response: mobilization (fight-or-flight), immobilization, and cognitive precautionary
• Bridge between nervous system function and clinical disorders and affective experiences

Previous Research:

• Previous researchers attempted to bridge the gap between visceral states and emotional experiences
• Need for methodologies evaluating dynamic changes in physiological variables in a changing context

Polyvagal Theory:

• Provides a perspective on demystifying features of clinical disorders related to social engagement system compromise
• Explanation from an adaptive perspective for interventions promoting social engagement behaviors and dampening defensive strategies disrupting social interactions.

W.H. Hess's Nobel Lecture (1949):

• Emphasized central structures in regulation of visceral state, especially the hypothalamus
• Anticipated need for methodologies to monitor neural circuits involving both defined brain structures and peripheral nerves in real-time.

19. Neurobiology and Evolution: Mechanisms, Mediators, and Adaptive Consequences of Caregiving

Caregiving Defining Features

• Providing food, protection, or resources
• Social support for needs of affiliation and perceived safety
• Altricial infants require caregiving due to immature motor and autonomic systems
• Symbiotic regulation: caregiver becomes part of complex feedback system
• Transition from dependence on caregiver to greater self-regulation
• Caregiving may be reciprocal or non-reciprocal
• Beneficial effects of caregiving linked to hormones of birth and lactation

Evolution of a Caregiving System: The Transition from "Self-Regulation" to "Other Regulation"

• Focus on ultimate causes in evolutionary theories limited by fossil record
• Phylogenetic perspective illustrates neurobiological features underlying sociality
• Defining feature: shift from self-regulation to other regulation during mammalian transition
• Neurobiology of sociality emerges as adaptive "other regulation" becomes crucial for survival consequences
• Newest circuit (social communication) used first, older circuits recruited sequentially when needed.

Mammalian Social Behavior and Vagus Nerve Evolution for Social Communication

The Polyvagal Theory and Mammalian Social Behavior

Autonomic Nervous System:

• Central nervous system cannot function without the support of visceral organs supplying oxygen and energy
• Autonomic nervous system regulates the viscera and conveys information upward to the hypothalamus, amygdala, and neocortex
• Sensory information from the viscera contributes to emotional states

Parasympathetic Component of the Autonomic Nervous System:

• Evolution of this system in mammals permitted the emergence of complex social interactions and social communication
• The vagus (Xth cranial) nerve transmits and integrates complex bidirectional communication between the brain and peripheral organs involved in cardiovascular, respiratory, digestive, and immune functions
• Critical to understanding mammalian sociality is knowledge of the origins of the neuranatomical pathways of the social engagement system

Two Distinct EFFERENT (Motor) Pathways:

• The vagus nerve has two distinct efferent (motor) pathways with separate brainstem source nuclei (Table 19.1)
• Approximately 80% of vagal fibers are afferent, transmitting sensory input from the viscera to the brainstem

Polyvagal System and Phylogenetic Distinctions:

• The evolution of the polyvagal system parallels the phylogenetic distinction between reptiles and mammals
• Changes in the vagus nerve, myelinated vagus, unmyelinated vagus, and branchial arches enabled social engagement and communication (sucking, swallowing, facial expressions, vocalizations)

Unmyelinated and Myelinated Vagus:

• The unmyelinated component of the vagus originates in the dorsal motor nucleus of the vagus and provides the efferent component of the dorsal vagal complex
• The more modern myelinated component originates in the nucleus ambiguus of the ventral vagal complex
• Myelinated vagus is cardioprotective and stabilizes cardiovascular function, responsible for respiratory sinus arrhythmia (RSA)

Resilience and Health:

• Information from the myelinated vagus (measured by RSA) is cardioprotective and directly implicated in cortical oxygenation
• RSA is an index of health and resilience in humans.

Evolution of Mammalian Social Communication through Myelinated Vagus and Special Visceral Efferents

Modern Processes Supporting Human Cognition

• Oxygen supply to primate cortex allowed emergence of higher cognitive functions
• Myelinated vagus associated with cranial nerves regulating larynx, pharynx, and facial muscles
  • Important for social communication through vocalizations and facial expressions

Mammalian Anatomy Enabling Social Communication

• Middle ear bones transmit higher frequency sounds than reptiles
  • Ossicular chain tightens in safe environments for processing mammalian acoustic communication
  • Brainstem areas regulating vagus and face/head muscles intertwined
    • Emergence of social engagement system with dynamic regulation of facial expressions, vocalizations, listening

Myelinated Vagus and Autonomic Nervous System

• Inhibits sympathetic nervous system and hypothalamic-pituitary-adrenal axis
  • Allows calm behavioral states for high levels of social interaction
• Phylogenetic transition from reptiles to mammals resulted in face–heart connection
  • Striated muscles of face/head regulated by myelinated vagus
    • Involved in social cueing through facial expressions, vocalizations, listening

Neuroception and Social Management of Threat

• Myelinated vagus permits expression of positive emotions and social communication
  • Neuroception assesses risk through fight-or-flight or passive coping strategies
    • Fight-or-flight: mobilization, active coping (sympathoadrenal systems)
    • Passive coping: immobility, shutdown (unmyelinated vagus slows heart rate)
      • Mammals cannot maintain alertness without oxygen and may experience unconsciousness or death

Social Engagement System

• Pathways from cranial nerves regulating facial/head muscles labeled as special visceral efferents
  • Control muscles of mastication, listening, emotional expression, vocal prosody, gesture
• Source nuclei of face/head and myelinated vagus interact to form social engagement system
  • Provides neural structures for expressing social behaviors and associated feelings.

Neuropeptides Regulate Social Behavior and Autonomic Nervous System

Social Communication and Visceral Systems

• Infant cries are indicators of health state and can elicit caregiving
• Coordinated regulation of social communication and visceral systems helps explain relationship between positive social experiences and health
• Shared neural pathways underlie social communication and visceral functions (e.g., cardiovascular, digestive, immune systems)
• Myelinated vagus regulates vocal communication (breath, larynx, pharynx muscles) and heart rate through RSA

Heart Rate Variability and Prosody

• Depressed social engagement system: low variability in both heart rate (low amplitude RSA) and vocal intonations (lack of prosody)
• Lack of prosody is a risk factor similar to low amplitude RSA
• High variability in both heart rate and vocal intonations indicates optimally functioning social engagement system

Neuropeptides and Social Nervous System

• Neuropeptides regulate sociality, emotion, and the autonomic nervous system
• Oxytocin and vasopressin are important for mammalian sociality
• Increasing evidence that oxytocin is central to positive social behaviors (sensitivity to social cues, trust, caregiving)

Oxytocin vs. Vasopressin

• Similar neurochemical structure, differing in 2 of 9 amino acids
• Oxytocin produced primarily in hypothalamic nuclei (supraoptic and paraventricular), vasopressin in supraoptic and paraventricular as well as other brain regions
• Vasopressin also abundant in amygdala, bed nucleus of stria terminalis, lateral septum for social/emotional regulation and self-defense (especially males)
• Oxytocin and vasopressin transported from hypothalamus to posterior pituitary as hormones, act as neuromodulators in brain
• Both oxytocin and vasopressin have receptors in various social behavior areas, can affect each other's receptors

Evolution of Oxytocin and Vasopressin

• Essential elements of sociality likely arose from water and mineral conservation needs

Neuropeptides' Role in Social Behavior and Stress Management

Oxytocin and Vasopressin: Adaptations for Terrestrial Life

Transition from Aquatic to Terrestrial Life:

• Includes adaptations like internal fertilization, pregnancy, and placental reproduction
• Capacity to maintain or reabsorb water was critical in the evolution of terrestrial mammals
• Shift provided a protective environment for offspring before and after birth

Molecular Structure and Evolution:

• Genes for oxytocin and vasopressin are ancient, estimated to be over 700 million years old
• Vasotocin, an ancestor of oxytocin and vasopressin, was found in mammalian fetuses
• Specific coding sequences for oxytocin and vasopressin likely evolved around the time of mammalian emergence

Functions in Maternal Nurturing and Social Communication:

• Oxytocin's functions in birth and lactation assist in maternal nurturing of immature infants
• Capacity to induce uterine contractions may have allowed for expansion of the human skull and cortex
• Contributes to elaboration of human vocalizations into speech and social communication

Neuropeptides and Autonomic Functions:

• Oxytocin and vasopressin influence autonomic functions through effects on the brainstem
• Paraventricular nucleus in the hypothalamus is a site of convergence for neural communication coordinating endocrine and cardiovascular responses
• Receptors for oxytocin and vasopressin are found in the amygdala, which integrates sensory, cognitive, and emotional information

Emotional Reactivity and Autonomic Nervous System:

• Oxytocin and vasopressin can influence emotions and behavior through their effects on the autonomic nervous system
• Interactions between oxytocin and vasopressin at the level of the central nucleus of the amygdala regulate vagal circuits
• Vasopressin plays a complex role in behavior through effects on blood pressure, heart rate, sympathetic-adrenal axis, and parasympathetic functions
• Receptors for both oxytocin and vasopressin are found in pathways regulating the myelinated vagus

Polyvagal Theory:

• Oxytocin receptors are particularly abundant in the dorsal vagal complex, which regulates the unmyelinated vagus
• Unmyelinated vagus can slow heart rate and trigger massive drops in blood pressure, while myelinated vagus restrains this system
• During stressful conditions, oxytocin may protect the autonomic nervous system from reverting to a more primitive vagal state

Oxytocin's Role in Stress Management, Immunity, and Sex Differences in Caregiving Behavior

Oxytocin:

• Inhibits central effects of vasopressin and other adaptive peptides like corticotropin-releasing factor
• Released by intense stressors, such as restraint or exposure to social intruder
• Facilitates social behavior and protects both the caregiver and recipient from stress
• Affects immune system, acting during development and reducing inflammatory processes
• May promote wound healing in humans

Sex Differences:

• Women give more direct nurture through roles as spouse or parent
• Men express nurturance through less direct caregiving behaviors like defense or protection
• Biological differences, including neuropeptides and their receptors, influence sexually dimorphic social behaviors
• Little research on oxytocin levels between the sexes; context-dependent effects of estrogen and oxytocin
• Sex differences in central vasopressin system important for reactions to negative and positive stimuli
• Social experiences regulate synthesis and receptors of neuropeptides, influencing behavior throughout life.

Social Interactions and Neuropeptides Impact Health and Healing

Human Social Behavior and Oxytocin's Role in Healing

• Humans are highly social creatures with a capacity for healing linked to relationships (Paragraph 1)
• Caregiving interactions play a critical role in survival, involving gestures, facial expressions, prosody, proximity, and touch (Paragraph 2)
• Social support from friends and relatives may reverse illness and maintain health (Paragraph 2)
• Oxytocin likely plays a role in positive consequences of social support through effects on the autonomic nervous system and immune system (Paragraph 2)
• Person-to-person interactions that promote calm physiological states contribute to health, healing, and growth processes (Paragraph 3)
• Threating interactions trigger defensive strategies associated with fight-or-flight or shutdown behaviors (Paragraph 4)
• Neuroception involves assessing environment as safe, dangerous, or life-threatening and triggers neural circuits for health support or defense (Paragraph 5)
• Oxytocin and vasopressin may modulate neuroception in the amygdala (Paragraph 5)
• Innate person-to-person interactions can trigger adaptive biobehavioral systems that promote health and healing (Paragraph 6)

Dependance on Caregivers and Neuropeptides

• Long periods of self-regulated behaviors are expressed between caregiving dependence (Infancy and old age) (Summary)
• Dependence on caregivers is paralleled by limitations in myelinated vagus regulation (Summary)
• Oxytocin and vasopressin may enable infants or elderly to be soothed by various caregivers during caregiver dependence periods (Question for future research)
• As neural control circuits develop, oxytocin and vasopressin play a more important role in modulating state to promote strong social bonds (Summary)

Neurobiology of Sociality

• Humans are highly social mammals dependent on others for survival and reproduction (Summary)
• Evolved neural, autonomic, and endocrine underpinnings of sociality are shared with other species (Summary)
• Knowledge of neurobiology of social engagement and bonding provides insights into human concepts like social support and caregiving (Summary)
• Integrated systems including brainstem, hormones, and immune system regulate social behavior, stress management, and healing (Summary)
• Context-dependent actions of these systems can promote health or have detrimental consequences depending on the context. (Summary)

Epilogue

Polyvagal Theory Expansion and Integration

• The polyvagal theory (Porges, 2007a, 2007b) is continuously evolving with increasing knowledge from neurosciences and feedback from clinicians
• Will expand into an integrated neurovisceral regulation theory, incorporating the role of specific brain structures in regulating immune, endocrine, and autonomic systems
• This integration will enable a more succinct understanding of the influence on mental processes and bodily functions on health and vice versa

Neuroanatomical Integration

• The integrated theory will emphasize the neuroanatomical connections between these previously independent response systems (immune, endocrine, autonomic)
• This integration is obvious and long overdue at a neuroanatomical level

Reinterpretation of Immune and Endocrine Responses

• Immune and endocrine responses will be interpreted within a phylogenetic hierarchy, similar to the three circuits outlined in the initial statement of the polyvagal theory
• Rather than interpreting these responses as stressful or injurious, their adaptive function will be emphasized

Clinical Applications

• The expanded theory will provide a better understanding of bidirectional mind–body and brain–body responses, explaining processes such as the body's ability to heal and the relationship between physical disease and mental health

Training for Clinicians

• Clinicians, especially traumatologists, find the polyvagal theory useful in understanding mental health symptoms and developing interventions and treatment models respecting client safety
• Therapists will be trained to attend to prosody of voice, facial expressivity, gaze, and auditory hypersensitivities as both diagnostic and prognostic indicators

Noncontact Technologies for Monitoring Integrated Systems

• Easily monitored measures like heart rate, facial muscle activity, and acoustic features of vocalization may provide variables reflecting endocrine, immune regulation, brain structures, and compromises due to white matter disease or other aspects of brain dysfunction
• In the future, noncontact technologies such as high-resolution infrared cameras may be used to monitor these variables
• Polyvagal monitor could indicate when a client shifts between defensive strategies (fear-induced mobilization or immobilization behaviors) and calm states associated with safety and social engagement

Neurophysiological State as Necessary but Not Sufficient Condition for Specific Behaviors to Occur

• Polyvagal theory challenges the scientist to think in terms of bidirectional and hierarchical neural feedback circuits involving communication between peripheral organs and various brain structures
• The clinician is challenged to interpret atypical behaviors and physiological reactions as adaptive