The polyvagal theory: New insights into adaptive reactions of the autonomic nervous system

Stephen W. Porges, PhD

Cleveland Clinic Journal of Medicine February 2009, 76 (4 suppl 2) S86-S90; DOI: https://doi.org/10.3949/ccjm.76.s2.17

Abstract

The polyvagal theory describes an autonomic nervous system that is influenced by the central nervous system, sensitive to afferent influences, characterized by an adaptive reactivity dependent on the phylogeny of the neural circuits, and interactive with source nuclei in the brainstem regulating the striated muscles of the face and head. The theory is dependent on accumulated knowledge describing the phylogenetic transitions in the vertebrate autonomic nervous system. Its specific focus is on the phylogenetic shift between reptiles and mammals that resulted in specific changes to the vagal pathways regulating the heart. As the source nuclei of the primary vagal efferent pathways regulating the heart shifted from the dorsal motor nucleus of the vagus in reptiles to the nucleus ambiguus in mammals, a face–heart connection evolved with emergent properties of a social engagement system that would enable social interactions to regulate visceral state.Go to:

HISTORICAL PERSPECTIVES ON THE AUTONOMIC NERVOUS SYSTEM

Central nervous system regulation of visceral organs is the focus of several historic publications that have shaped the texture of physiological inquiry. For example, in 1872 Darwin acknowledged the dynamic neural relationship between the heart and the brain:

. . .when the heart is affected it reacts on the brain; and the state of the brain again reacts through the pneumo-gastric [vagus] nerve on the heart; so that under any excitement there will be much mutual action and reaction between these, the two most important organs of the body.1

Although Darwin acknowledged the bidirectional communication between the viscera and the brain, subsequent formal description of the autonomic nervous system (eg, by Langley2) minimized the importance of central regulatory structures and afferents. Following Langley, medical and physiological research tended to focus on the peripheral motor nerves of the autonomic nervous sytem, with a conceptual emphasis on the paired antagonism between sympathetic and parasympathetic efferent pathways on the target visceral organs. This focus minimized interest in both afferent pathways and the brainstem areas that regulate specific efferent pathways.

The early conceptualization of the vagus focused on an undifferentiated efferent pathway that was assumed to modulate “tone” concurrently to several target organs. Thus, brainstem areas regulating the supradiaphragmatic (eg, myelinated vagal pathways originating in the nucleus ambiguus and terminating primarily above the diaphragm) were not functionally distinguished from those regulating the subdiaphragmatic (eg, unmyelinated vagal pathways originating in the dorsal motor nucleus of the vagus and terminating primarily below the diaphragm). Without this distinction, research and theory focused on the paired antagonism between the parasympathetic and sympathetic innervation to target organs. The consequence of an emphasis on paired antagonism was an acceptance in physiology and medicine of global constructs such as autonomic balance, sympathetic tone, and vagal tone.

More than 50 years ago, Hess proposed that the autonomic nervous system was not solely vegetative and automatic but was instead an integrated system with both peripheral and central neurons.3 By emphasizing the central mechanisms that mediate the dynamic regulation of peripheral organs, Hess anticipated the need for technologies to continuously monitor peripheral and central neural circuits involved in the regulation of visceral function.Go to:

THE VAGAL PARADOX

In 1992, I proposed that an estimate of vagal tone, derived from measuring respiratory sinus arrhythmia, could be used in clinical medicine as an index of stress vulnerability.4 Rather than using the descriptive measures of heart rate variability (ie, beat-to-beat variability) frequently used in obstetrics and pediatrics, the paper emphasized that respiratory sinus arrhythmia has a neural origin and represents the tonic functional outflow from the vagus to the heart (ie, cardiac vagal tone). Thus, it was proposed that respiratory sinus arrhythmia would provide a more sensitive index of health status than a more global measure of beat-to-beat heart rate variability reflecting undetermined neural and nonneural mechanisms. The paper presented a quantitative approach that applied time-series analyses to extract the amplitude of respiratory sinus arrhythmia as a more accurate index of vagal activity. The article provided data demonstrating that healthy full-term infants had respiratory sinus arrhythmia of significantly greater amplitude than did preterm infants. This idea of using heart rate patterns to index vagal activity was not new, having been reported as early as 1910 by Hering.5 Moreover, contemporary studies have reliably reported that vagal blockade via atropine depresses respiratory sinus arrhythmia in mammals.6,7

In response to this article,4 I received a letter from a neonatologist who wrote that, as a medical student, he learned that vagal tone could be lethal. He argued that perhaps too much of a good thing (ie, vagal tone) could be bad. He was referring, of course, to the clinical risk of neurogenic bradycardia. Bradycardia, when observed during delivery, may be an indicator of fetal distress. Similarly, bradycardia and apnea are important indicators of risk for the newborn.

My colleagues and I further investigated this perplexing observation by studying the human fetus during delivery. We observed that fetal bradycardia occurred only when respiratory sinus arrhythmia was depressed (ie, a respiratory rhythm in fetal heart rate is observable even in the absence of the large chest wall movements associated with breathing that occur postpartum).8 This raised the question of how vagal mechanisms could mediate both respiratory sinus arrhythmia and bradycardia, as one is protective and the other is potentially lethal. This inconsistency became the “vagal paradox” and served as the motivation behind the polyvagal theory.

With regard to the mechanisms mediating brady-cardia and heart rate variability, there is an obvious inconsistency between data and physiological assumptions. Physiological models assume vagal regulation of both chronotropic control of the heart (ie, heart rate) and the amplitude of respiratory sinus arrhythmia.9,10 For example, it has been reliably reported that vagal cardio-inhibitory fibers to the heart have consistent functional properties characterized by bradycardia to neural stimulation and a respiratory rhythm.9 However, although there are situations in which both measures covary (eg, during exercise and cholinergic blockade), there are other situations in which the measures appear to reflect independent sources of neural control (eg, bradycardic episodes associated with hypoxia, vasovagal syncope, and fetal distress). In contrast to these observable phenomena, researchers continue to argue for a covariation between these two parameters. This inconsistency, based on an assumption of a single central vagal source, is what I have labeled the vagal paradox.

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About S. R. Zelenz 117 Articles
S.R. Zelenz has worked in education for 20 years. Working with students from all walks of life, cultures, races, and social diversity, Zelenz’s research in Educational Leadership led to finding a better way to approach learning for students with trauma histories. Many were juvenile offenders, gang members, diagnosed with varying behavioral disorders, or had family histories of violence, murder, or narcissistic parenting. This research could not be effectively accomplished without further understanding: how epigenetic trauma inheritance may be impacting these students; how brain development from trauma may be impacting their behavioral and emotional development; as well as deep understanding of psychology and its varying classifications for behavioral and personality disorders. The goal is to find solutions for changing the conversation and making a real difference for these students. She has also worked with nonprofits of varying focus areas for the last 25 years. Her undergraduate degree in Arts Administration and Music prepared her for managing nonprofits of any size as well as procuring funding so that they can achieve their goals. Pairing her nonprofit background with her education background, she has been able to make a difference for over 200 nonprofits worldwide, written curriculum for schools across the globe, and assisted many arts organizations through performance and management.