Polyvagal theory

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The vagus nerve Recurrent laryngeal nerve.svg
The vagus nerve

Polyvagal theory (PVT) is a collection of proposed evolutionary, neuroscientific, and psychological constructs pertaining to the role of the vagus nerve in emotion regulation, social connection and fear response. The theory was introduced in 1994 by Stephen Porges. [1] There is consensus among experts that the assumptions of the polyvagal theory are untenable. [2] PVT is popular among some clinical practitioners and patients, [3] but it is not endorsed by current social neuroscience. [4] [5] [6] [7] [8] [9]

Contents

Polyvagal theory takes its name from the vagus, a cranial nerve that forms the primary component of the parasympathetic nervous system. [10] [11] [12] The traditional view of the autonomic nervous system presents a two-part system: the sympathetic nervous system, which is more activating ("fight or flight"), and the parasympathetic nervous system, which supports health, growth, and restoration ("rest and digest"). [13] Polyvagal theory views the parasympathetic nervous system as being split into two distinct branches: a "ventral vagal system" which supports social engagement, and a "dorsal vagal system" which supports immobilisation behaviours, both "rest and digest" and defensive immobilisation or "shutdown". [14] This "social engagement system" is a hybrid state of activation and calming that plays a role in our ability to socially engage. [14]

Theory

The vagus, or tenth cranial nerve, is a primary component of the autonomic nervous system, which operates the internal organs. It transmits parasympathetic signals to and from the heart, lungs, and digestive tract. [15] The vagal system is claimed to be inhibitory of primal instincts by being part of the parasympathetic nervous system, in opposition to the sympathetic-adrenal system, involved in mobilization behaviors. [14]

Polyvagal theory was developed in 1994 by Porges, who at the time was director of the Brain-Body Center at the University of Illinois at Chicago. [16] It focuses on the structure and function of the two efferent branches of the vagus cranial nerve, which originate from the medulla. [17] Each branch is claimed to be associated with a different adaptive behavioral strategy; the ventral branches more restful in nature and the dorsal ones more active in nature. [18]

According to the theory, three organizational principles can be distinguished:[ vague ]

Explanatory diagram Polyvagal theory Ventral Vagal.png
Explanatory diagram
  1. Hierarchy: The autonomic nervous system reacts in three reaction patterns, which are activated in a specific order.
  2. Neuroception: In contrast to perception, it is here a cognition without awareness, triggered by a stimulus such as danger. [14] [19]
  3. Co-regulation: The need to feel safe enough to allow oneself to be in relationships, which is difficult for traumatized people. [20]

Porges describes the three neural circuits as regulators for reactive behavior. His findings were taken into account by some theorists of childhood trauma, with related techniques used by trauma therapists such as Bessel van der Kolk, [21] Peter A. Levine and Marianne Bentzen.

Anatomical hypothesis

Polyvagal theory combines ideas from evolutionary biology and neurology, to claim that autonomic reactions have adapted to the phylogenetic development of neural circuits. [14] It claims that the sympathetic nervous system, and two distinct branches of the parasympathetic nervous system, are phylogenetically ordered and activated for responses. [17] The branches of the vagal nerve are claimed to serve different evolutionary stress responses in mammals: the more primitive branch is said to elicit immobilization behaviors (e.g., feigning death), whereas the more evolved branch is said to be linked to social communication and self-soothing behaviors. [22] These functions are claimed to follow a phylogenetic hierarchy, where the most primitive systems are activated only when the more evolved functions fail. [14]

According to the theory, these neural pathways regulate autonomic states and the expression of emotional and social behaviour. It claims that in mammals, facial expressions are connected to internal physical reactions, such as cardiac and digestive changes, [22] and in general physiological state dictates the range of behaviour and psychological experience. [14]

Claims about the nature of stress, emotion, and social behaviour, are traditionally studied via peripheral indices of arousal such as heart rate, cortisol level and skin conductance. [1] Polyvagal theory champions the measurement of vagal tone as a new index of stress vulnerability and reactivity, including in populations with affective disorders. [23]

Proposed dorsal vagal complex (DVC)

The dorsal branch of the vagus nerve originates in the dorsal motor nucleus and is postulated by polyvagal theory to be the phylogenetically older branch. [1] This branch is unmyelinated and exists in most vertebrates. Polyvagal theory calls this the "vegetative vagus" because it sees it as being associated with primal survival strategies of primitive vertebrates, reptiles, and amphibians. [24] Under certain conditions, these animals "freeze" when threatened, conserving their metabolic resources. This draws on the simplifying claims of the triune brain theory which are no longer considered accurate due to the many exceptions to this rule (see Triune brain § Status of the model). [1]

The DVC provides primary control of subdiaphragmatic visceral organs, such as the digestive tract. Under normal conditions, the DVC maintains regulation of these digestive processes. However, prolonged disinhibition can be lethal for mammals, as it results in apnea and bradycardia. [17] [ dubious – discuss ]

Proposed ventral vagal complex (VVC)

With increased neural complexity as seen in mammals (due to phylogenetic development) there is said to have evolved a more sophisticated system to enrich behavioral and affective responses to an increasingly complex environment. [17] [ dubious – discuss ] The ventral branch of the vagus originates in the nucleus ambiguus and is myelinated to provide more speed in responding. [17] Polyvagal theory calls this the "smart vagus" because it associates it with the regulation of sympathetic "fight or flight" behaviors by way of social affiliative behaviors. [24] These behaviors are said to include social communication and self-soothing and calming. [17] In other words, this branch of the vagus is said to inhibit or disinhibit defensive limbic circuits, depending on the situation. Note: Attributing defensive behaviours purely to the limbic system is an oversimplification, as these are triggered by perceived threats, thus requiring an interplay of brain areas performing sensory integration, memory, and semantic knowledge with the limbic system to be elicited. Similarly, the regulation of emotions requires a complex interplay of higher cognitive areas with limbic ones. The vagus nerve mediates the control of supradiaphragmatic visceral organs, such as the esophagus, bronchi, pharynx, and larynx. It also exerts an important influence on the heart. When vagal tone to the heart’s pacemaker is high, a baseline or resting heart rate is produced. In other words, the vagus acts as a restraint, or brake, limiting heart rate. However, when vagal tone is removed, there is little inhibition to the pacemaker, and according to polyvagal theory, rapid mobilization ("fight/flight") can be activated in times of stress, but without having to engage the sympathetic-adrenal system, as activation comes at a severe biological cost. [17] Note: While the vagus nerve's role in downregulating the heart rate is well-established, the notion that a Fight-or-flight response can be triggered without engaging the sympathetic nervous system is not substantiated by any evidence.

Vagal tone as a marker of stress

In order to maintain homeostasis, the central nervous system responds constantly, via neural feedback, to environmental cues. [13] Stressful events disrupt the rhythmic structure of autonomic states, and subsequently, behaviors. [13] Since the vagus plays such an integral role in the peripheral nervous system via regulation of heart rate, Porges suggests that the amplitude of respiratory sinus arrhythmia (RSA) is a good index of parasympathetic nervous system activity via the cardiac vagus. [25] That is, RSA is proposed as a measurable, noninvasive way to see how the vagus modulates heart rate activity in response to stress. If true, this method could be useful to measure individual differences in stress reactivity. [26]

RSA is the widely used measure of the amplitude of heart rate rhythm associated with the rate of spontaneous breathing. [25] Research has shown that amplitude of RSA is an accurate indicator of the efferent influence of the vagus on the heart. [25] Since inhibitory effects of the VVC branch of the vagus allow for a wide range of adaptive, prosocial behaviors, it has been theorized that individuals with greater vagal tone are able to exhibit a greater range of such behaviors. On the other hand, decreased vagal tone is associated with illnesses and medical complications that compromise the CNS. [25] These complications may reduce one's capacity to respond to stress appropriately.

Clinical applications in the human fetus

Healthy human fetuses have high variability in heart rate, which is mediated by the vagus. [27] On the other hand, heart rate decelerations, which are also mediated by the vagus, are a sign of fetal distress. More specifically, prolonged withdrawal of vagal influence on the heart creates a physiological vulnerability to the influence of the Dorsal Vagal Complex, which in turn produces bradycardia (very low heart rate). However, the onset of this deceleration is commonly preceded by transitory tachycardia, which is reflective of the immediate effects of Ventral Vagal Complex withdrawal. [28]

Reception

In a 2023 review of the literature, Paul Grossman lists five premises of polyvagal theory and states that "there is broad consensus among experts [...] that each basic physiological assumption of the polyvagal theory is untenable. Much of the existing evidence, upon which these consensuses are grounded, strongly indicates that the underlying polyvagal hypotheses have been falsified." [2]

Although proponents like Bessel van der Kolk praise the theory's explanatory power, [21] Grossman considers the theory an unnecessary and unsubstantiated conflict imposed on the public dialogue. [29]

Neuroscientific claims

Neuhuber and Berthoud (2022) state that polyvagal theory's "basic phylogenetic and functional-anatomical tenets do not withstand closer scrutiny". [30] They argue that polyvagal theory incorrectly portrays the role of the different vagal nuclei in mediating the freeze response. According to their analysis, the evidence "does not support a role of the 'dorsal vagal complex' in freezing as proposed by the PVT" and the dorsal vagal complex "should not be linked to passive defensive behavior". Regarding the proposed "ventral vagal complex", they state that "the PVT, by construeing a 'new ventral vagal complex' encompassing the entire branchiomotor column ascribed to the vagus much more than it actually can serve." They see it as "misleading to propose that brainstem branchiomotor ('source') nuclei 'communicate directly with the visceromotor portion of the nucleus ambiguus'", and conclude that the relevant networks "should not be termed 'ventral vagal complex'. This terminology may insinuate that the vagus is a "prime mover". This not the case [...]".

Taylor, Wang & Leite (2022) similarly regard it as "invalid to refer to this as a 'vagal system' or to postulate the existence of a 'smart vagus'." [31]

Evolutionary claims

Grossman and Taylor (2007) argue that there is no evidence that the dorsal motor nucleus (DMN) is an evolutionarily more primitive center of the brainstem parasympathetic system than the nucleus ambiguus (NA), and review evidence to the contrary. [29]

A more recent paper by Monteiro et al. (2018) finding myelinated vagus nerve fibers of lungfish leading from the nucleus ambiguus to the heart also indicates that polyvagal theory’s hypothesis that the nucleus ambiguus is unique to mammals is incorrect. [32] They state that "the mechanisms [Porges] identifies as solely mammalian are undeniably present in the lungfish that sits at the evolutionary base of the air-breathing vertebrates."

Grossman (2023) concurs, stating that "the polyvagal notion that the ventral vagal area is unique to mammals is opposed by years of evidence" and that the "findings, as a whole, firmly and consistently contradict the polyvagal hypotheses that propose the [dorsal vagal motor nucleus] as the “source nucleus” of unmyelinated pathways and the [nucleus ambiguus] as the “source nucleus” of myelinated pathways in mammals". [2]

Results reviewed by Taylor, Leite and Skovgaard (2010) also "refute the proposition that centrally controlled cardiorespiratory coupling is restricted to mammals, as propounded by the polyvagal theory of Porges". [33] In Taylor, Wang & Leite's 2022 review, the evidence for the presence of cardio-respiratory interactions similar to respiratory sinus arrhythmia (RSA) and their potential purpose in blood oxygenation in many vertebrate species (both air- and water-breathing) leads them to conclude that RSA may be a relic of older cardio-respiratory systems, contrary to polyvagal assumptions. [31]

The dichotomy between asocial reptiles and social mammals subscribed to by polyvagal theory has been contested. Doody, Burghardt & Dinets [34] consider several ways of assessing and classifying animal sociality and state that "Porges’ dichotomy is incorrect. While many mammals (particularly humans) may show more complex social behavior than reptiles, there is considerable overlap in social tendencies between the two groups. The labels ‘social’ and ‘asocial’ are too crude to have utility in a comparative framework of social behavior and should not be used to describe taxa". Listing examples of social behavior in reptiles and other non-mammal vertebrates, they observe that "PT appears to rest upon 20th century folk interpretation of vertebrate evolutionary biology rather than on current scientific understanding of it."

Claims regarding cardiac functioning

Polyvagal theory proposes a relationship between RSA responses and forms of psychopathology, but a meta-analysis finds the empirical evidence to be inconclusive. [35]

According to Grossman and Taylor, [29] the existing research indicates that respiratory sinus arrhythmia is not a reliable marker of vagal tone, since it is subject to both respiratory variables and sympathetic (beta-adrenergic) influences in addition to vagal influences. In addition, they argue that the results of Porges' 2003 study on two species of lizard was flawed due to incorrect measurements of heart rate variability.

Reviewing more recent evidence, Paul Grossman again finds RSA not "a direct measure of cardiac vagal tone" due to confounding factors. In addition, he concludes that contrary to polyvagal claims "there is no credible evidence that the [dorsal vagal motor nucleus] plays any role in massive bradycardia", and that it "appears to have almost no effect upon vagal heart rate responses". [2]

Scientific standards

In a 2021 publication, Porges stated that "the theory was not proposed to be either proven or falsified". [36] Falsifiability is a central tenet of the scientific method.

See also

Related Research Articles

<span class="mw-page-title-main">Vagus nerve</span> Main nerve of the parasympathetic nervous system

The vagus nerve, also known as the tenth cranial nerve, cranial nerve X, or simply CN X, is a cranial nerve that carries sensory fibers that create a pathway that interfaces with the parasympathetic control of the heart, lungs, and digestive tract. It comprises two nerves—the left and right vagus nerves—but they are typically referred to collectively as a single subsystem.

<span class="mw-page-title-main">Autonomic nervous system</span> Division of the nervous system supplying internal organs, smooth muscle and glands

The autonomic nervous system (ANS), formerly referred to as the vegetative nervous system, is a division of the nervous system that operates internal organs, smooth muscle and glands. The autonomic nervous system is a control system that acts largely unconsciously and regulates bodily functions, such as the heart rate, its force of contraction, digestion, respiratory rate, pupillary response, urination, and sexual arousal. This system is the primary mechanism in control of the fight-or-flight response.

<span class="mw-page-title-main">Parasympathetic nervous system</span> Division of the autonomic nervous system

The parasympathetic nervous system (PSNS) is one of the three divisions of the autonomic nervous system, the others being the sympathetic nervous system and the enteric nervous system. The enteric nervous system is sometimes considered part of the autonomic nervous system, and sometimes considered an independent system.

<span class="mw-page-title-main">Enteric nervous system</span> Vital system controlling the gastrointestinal tract

The enteric nervous system (ENS) or intrinsic nervous system is one of the three main divisions of the autonomic nervous system (ANS), the other being the sympathetic (SNS) and parasympathetic nervous system (PSNS), and consists of a mesh-like system of neurons that governs the function of the gastrointestinal tract. It is capable of acting independently of the SNS and PSNS, although it may be influenced by them. The ENS is nicknamed the "second brain". It is derived from neural crest cells.

<span class="mw-page-title-main">Medulla oblongata</span> Structure of the brain stem

The medulla oblongata or simply medulla is a long stem-like structure which makes up the lower part of the brainstem. It is anterior and partially inferior to the cerebellum. It is a cone-shaped neuronal mass responsible for autonomic (involuntary) functions, ranging from vomiting to sneezing. The medulla contains the cardiac, respiratory, vomiting and vasomotor centers, and therefore deals with the autonomic functions of breathing, heart rate and blood pressure as well as the sleep–wake cycle.

<span class="mw-page-title-main">Brainstem</span> Posterior part of the brain, adjoining and structurally continuous

The brainstem is the stalk-like part of the brain that interconnects the cerebrum and diencephalon with the spinal cord. In the human brain, the brainstem is composed of the midbrain, the pons, and the medulla oblongata. The midbrain is continuous with the thalamus of the diencephalon through the tentorial notch.

<span class="mw-page-title-main">Solitary nucleus</span> Sensory nuclei in medulla oblongata

The solitary nucleus is a series of sensory nuclei forming a vertical column of grey matter in the medulla oblongata of the brainstem. It receives general visceral and/or special visceral inputs from the facial nerve, glossopharyngeal nerve and vagus nerve ; it receives and relays stimuli related to taste and visceral sensation. It sends outputs to various parts of the brain, such as the hypothalamus, thalamus, and reticular formation. Neuron cell bodies of the SN are roughly somatotopically arranged along its length according to function.

<span class="mw-page-title-main">Nucleus ambiguus</span>

The nucleus ambiguus is a group of large motor neurons, situated deep in the medullary reticular formation named by Jacob Clarke. The nucleus ambiguus contains the cell bodies of neurons that innervate the muscles of the soft palate, pharynx, and larynx which are associated with speech and swallowing. As well as motor neurons, the nucleus ambiguus contains preganglionic parasympathetic neurons which innervate postganglionic parasympathetic neurons in the heart.

<span class="mw-page-title-main">Baroreflex</span> Homeostatic mechanism in the body

The baroreflex or baroreceptor reflex is one of the body's homeostatic mechanisms that helps to maintain blood pressure at nearly constant levels. The baroreflex provides a rapid negative feedback loop in which an elevated blood pressure causes the heart rate to decrease. Decreased blood pressure decreases baroreflex activation and causes heart rate to increase and to restore blood pressure levels. Their function is to sense pressure changes by responding to change in the tension of the arterial wall The baroreflex can begin to act in less than the duration of a cardiac cycle and thus baroreflex adjustments are key factors in dealing with postural hypotension, the tendency for blood pressure to decrease on standing due to gravity.

<span class="mw-page-title-main">Heart rate variability</span> Variation in the time intervals between heartbeats

Heart rate variability (HRV) is the physiological phenomenon of variation in the time interval between heartbeats. It is measured by the variation in the beat-to-beat interval.

<span class="mw-page-title-main">Area postrema</span> Medullary structure in the brain that controls vomiting

The area postrema, a paired structure in the medulla oblongata of the brainstem, is a circumventricular organ having permeable capillaries and sensory neurons that enable its dual role to detect circulating chemical messengers in the blood and transduce them into neural signals and networks. Its position adjacent to the bilateral nuclei of the solitary tract and role as a sensory transducer allow it to integrate blood-to-brain autonomic functions. Such roles of the area postrema include its detection of circulating hormones involved in vomiting, thirst, hunger, and blood pressure control.

<span class="mw-page-title-main">Vagovagal reflex</span> Reflex circuits in the gastrointestinal tract

Vagovagal reflex refers to gastrointestinal tract reflex circuits where afferent and efferent fibers of the vagus nerve coordinate responses to gut stimuli via the dorsal vagal complex in the brain. The vagovagal reflex controls contraction of the gastrointestinal muscle layers in response to distension of the tract by food. This reflex also allows for the accommodation of large amounts of food in the gastrointestinal tracts.

<span class="mw-page-title-main">Lateral hypothalamus</span>

The lateral hypothalamus (LH), also called the lateral hypothalamic area (LHA), contains the primary orexinergic nucleus within the hypothalamus that widely projects throughout the nervous system; this system of neurons mediates an array of cognitive and physical processes, such as promoting feeding behavior and arousal, reducing pain perception, and regulating body temperature, digestive functions, and blood pressure, among many others. Clinically significant disorders that involve dysfunctions of the orexinergic projection system include narcolepsy, motility disorders or functional gastrointestinal disorders involving visceral hypersensitivity, and eating disorders.

<span class="mw-page-title-main">Dorsal nucleus of vagus nerve</span>

The dorsal nucleus of vagus nerve is a cranial nerve nucleus of the vagus nerve situated in the medulla oblongata of the brainstem ventral to the floor of the fourth ventricle. It contains nerve cell bodies of parasympathetic neurons of CN X that provide parasympathetic innervation to the gastrointestinal tract and lungs as well as other thoracic and abdominal organs. These functions include, among others, bronchoconstriction and gland secretion.

<span class="mw-page-title-main">Esophageal plexus</span>

The esophageal plexus is formed by nerve fibers from two sources, branches of the vagus nerve, and visceral branches of the sympathetic trunk. The esophageal plexus and the cardiac plexus contain the same types of fibers and are both considered thoracic autonomic plexus.

The Hering–Breuer inflation reflex, named for Josef Breuer and Ewald Hering, is a reflex triggered to prevent the over-inflation of the lung. Pulmonary stretch receptors present on the wall of bronchi and bronchioles of the airways respond to excessive stretching of the lung during large inspirations.

Vagal tone is activity of the vagus nerve, the 10th cranial nerve and a fundamental component of the parasympathetic branch of the autonomic nervous system. This branch of the nervous system is not under conscious control and is largely responsible for the regulation of several body compartments at rest. Vagal activity results in various effects, including: heart rate reduction, vasodilation/constriction of vessels, glandular activity in the heart, lungs, and digestive tract, liver, immune system regulation as well as control of gastrointestinal sensitivity, motility and inflammation.

<span class="mw-page-title-main">Stephen Porges</span> Scientist and professor (born 1945)

Stephen W. Porges is an American psychologist and neuroscientist. He is the Professor of Psychiatry at the University of North Carolina at Chapel Hill. Porges is also currently Director of the Kinsey Institute Traumatic Stress Research Consortium at Indiana University Bloomington, which studies trauma.

A vagal maneuver is an action used to stimulate the parasympathetic nervous system by activating the vagus nerve. The vagus nerve is the longest nerve of the autonomic nervous system and helps regulate many critical aspects of human physiology, including heart rate, blood pressure, sweating, and digestion through the release of acetylcholine. Common maneuvers that activate the vagus nerve include the Valsalva maneuver and carotid sinus massage, which can serve diagnostic or therapeutic functions.

Neural top–down control of physiology concerns the direct regulation by the brain of physiological functions. Cellular functions include the immune system’s production of T-lymphocytes and antibodies, and nonimmune related homeostatic functions such as liver gluconeogenesis, sodium reabsorption, osmoregulation, and brown adipose tissue nonshivering thermogenesis. This regulation occurs through the sympathetic and parasympathetic system, and their direct innervation of body organs and tissues that starts in the brainstem. There is also a noninnervation hormonal control through the hypothalamus and pituitary (HPA). These lower brain areas are under control of cerebral cortex ones. Such cortical regulation differs between its left and right sides. Pavlovian conditioning shows that brain control over basic cell level physiological function can be learned.

References

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  32. ↑ Monteiro, Diana (2018). "Cardiorespiratory interactions previously identified as mammalian are present in the primitive lungfish". Science Advances. 4 (2): eaaq0800. Bibcode:2018SciA....4..800M. doi: 10.1126/sciadv.aaq0800 . PMC   5833999 . PMID   29507882.
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  34. ↑ Doody; Burghardt; Dinets (2023). "The Evolution of Sociality and the Polyvagal Theory". Biological Psychology. 180. arXiv: 2304.09238 . doi:10.1016/j.biopsycho.2023.108569. PMID   37094735. S2CID   258212987.
  35. ↑ Beauchaine, Theodore P.; Bell, Ziv; Knapton, Erin; McDonough-Caplan, Heather; Shader, Tiffany; Zisner, Aimee (2019). "Respiratory sinus arrhythmia reactivity across empirically based structural dimensions of psychopathology: A meta-analysis". Psychophysiology. 56 (5): e13329. doi:10.1111/psyp.13329. ISSN   1469-8986. PMC   6453712 . PMID   30672603.
  36. ↑ Stephen W. Porges (2021-08-01), "Polyvagal Theory: A biobehavioral journey to sociality", Comprehensive Psychoneuroendocrinology, vol. 7, p. 100069, doi:10.1016/j.cpnec.2021.100069, ISSN   2666-4976, PMC   9216697 , PMID   35757052

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