Polyvagal theory

Polyvagal theory ("poly-" "many" + "vagal" "wandering") is a collection of evolutionary, neuroscientific and psychological claims pertaining to the role of the vagus nerve in emotion regulation, social connection and fear response. While not endorsed by state-of-the-art social neuroscience, it is nevertheless popular among some clinical practitioners and patients.
Hypothesized phylogenetic subsystems/stages.
The vagus nerve is a primary component of the autonomic nervous system. The polyvagal theory focuses on the structure and function of the two efferent branches of the vagus cranial nerve, both of which originate from the medulla. More specifically, each branch is claimed to be associated with a different adaptive behavioral strategy; the ventral branches are more restful in nature and the dorsal ones are more active in nature. The vagal system is claimed to be inhibitory of primal instincts by being part of the parasympathetic nervous system, and in opposition the sympathetic-adrenal system is involved in mobilization behaviors. According to polyvagal theory, these opposing systems are phylogenetically ordered and activated for responses.
Anatomical conjectures.
The vagus, or tenth cranial nerve transmits parasympathetic signals to and from the heart, lungs, and digestive tract, a fact established before the middle of the 20th century. "Polyvagal theory" was introduced in 1994 by Stephen Porges, director of the Brain-Body Center at the University of Illinois at Chicago. As has been established since the early days of neuroanatomy, the Autonomic nervous system encompasses nerve fibers transmitting information from the body toward the brain, called afferent influences. According to polyvagal theory, this effect has been observed and demonstrated by adaptive reactivity dependent on the neural circuits' phylogenetical development. Polyvagal theory claims that human facial expressions are associated with, or reflect, physical reactions, such as cardiac and digestive changes.
Porges argues this theory with observations from both evolutionary biology and neurology.
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. These functions are claimed to follow a phylogenetic hierarchy, where the most primitive systems are activated only when the more evolved functions fail. These neural pathways regulate autonomic state and the expression of emotional and social behaviour. Thus, according to this theory, physiological state dictates the range of behaviour and psychological experience. 
Polyvagal theory makes broad claims on the nature of stress, emotion, and social behaviour, for the study of which peripheral indices of arousal such as heart rate, cortisol level and skin conductance have traditionally been used. Polyvagal theory champions the measurement of vagal tone in humans as a novel index of stress vulnerability and reactivity in populations with affective disorders.
The 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. 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. 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 (please see Triune brain - Status of the model for more).
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.
The proposed ventral vagal complex (VVC).
With increased neural complexity 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. The ventral branch of the vagus originates in the nucleus ambiguus and is myelinated to provide more speed in responding. 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. These behaviors are said to include social communication and self-soothing and calming. 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 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. 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 physiological marker of stress.
In order to maintain homeostasis, the central nervous system responds constantly, via neural feedback, to environmental cues. Stressful events disrupt the rhythmic structure of autonomic states, and subsequently, behaviors. 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. 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.
RSA is the widely used measure of the amplitude of heart rate rhythm associated with rate of spontaneous breathing. Research has shown that amplitude of RSA is an accurate indicator of the efferent influence of the vagus on the heart. 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. These complications may reduce one's capacity to respond to stress appropriately.
Clinical applications in the human fetus.
Healthy human fetuses have a high variability in heart rate, which is mediated by the vagus. 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 Control, 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 Control withdrawal.
Results of Porges' theory.
As described by Bessel van der Kolk, professor of psychiatry at the Boston University School of Medicine: 
Criticism.
Polyvagal theory has not, to date, been shown to explain any phenomena or experimental data above and beyond what is explained more precisely by Attachment theory, research on Emotional self-regulation, Stress models, the Neurovisceral Integration Model and neuroimaging studies from the field of Social Neuroscience.
Its appeal to non-scientists may lie in the fact that it provides a very simple (if inaccurate) neural underpinning to well-established psychological and therapy-related knowledge.
Inconsistencies and lack of evidence.
Critics of the polyvagal theory point out that its premises are not supported by empirical, scientific research. Paul Grossman of University Hospital Basel argues that there is no evidence that the dorsal motor nucleus (DMN) is an evolutionarily more primitive center of brainstem parasympathetic system than the nucleus ambiguus (NA), and that no evidence supports the claim that sudden decrease in heartrate elicited by extreme emotional circumstances (like trauma-related dissociation) is due to DMN efferent activity to the heart. In fact, there seems to be no evidence that such decrease happens in trauma-related dissociation in the first place. 
Grossman also points out that even the results of Porges' own study on two species of lizard was flawed due to inappropriate measurement of heart rate variability.
While the criticism does not address the clinical speculations of the polyvagal theory directly, it contradicts its premises. In particular, it undermines the suggestion that there is a phylogenetic hierarchy, where one vagal system is more primitive than the other, and therefore is activated only when the more evolved one fails (as in dissociation, or acute trauma). It has been known for roughly a century that "a differentiation of the visceral efferent column of the vagus nerve into a dorsal motor nucleus and a ventrolateral nucleus (nucleus ambiguus) is first seen in reptiles (Ariens Kappers, '12; Ariens Kappers et al., '36; Addens, '33)". This contradicts the polyvagal claim of the nucleus ambiguus being unique to mammals.
More recent findings in lungfish of myelinated vagus nerve fibres leading from the nucleus ambiguus to the heart point in the same direction.
In polyvagal theory the term vagal tone is equated with respiratory sinus arrhythmia (RSA), which is suggested to be linked to dimensions of psychopathology. A number of research studies have evaluated RSA responses across a range of dimensions of psychopathology, but a comprehensive meta-analysis has shown that no clinically meaningful relation can be found between psychopathology and RSA reactivity. 
Grossman & Taylor (2005) reviewed findings indicating that RSA is not a reliable marker of vagal tone, being subject to both respiratory variables and sympathetic (beta-adrenergic) influences in addition to vagal influences.
Apart from this, a correlation between vagal tone and stress regulation would not necessarily indicate a causal role of the vagus nerve activity on different stress responses in mammals (see Correlation does not imply causation for more).
By overemphasizing the role of the vagus nerve in deciding between freezing and other fear responses, the theory disregards decades of neuroscientific findings on the origins of the freeze response and fear responses in general. While the vagus nerve undoubtedly plays a role in "transmitting" emotion-related signals between the brain and the rest of the body (a fact established long before the emergence of polyvagal speculations, see Vagusstoff), there is no evidence to suggest that it has any "control" over whether a freeze response is triggered or not.
From a methodological perspective, many claims do not meet the criteria of a scientific theory because they are formulated in a manner too vague for empirical testing. For example, the precise functioning of the two proposed distinct "vagal systems" or of the "social engagement system" is not explained, nor is that of the "face-heart connection" supposedly embodied in the ventral branch of the vagus nerve. 
Furthermore, the claims do not explain any findings beyond what was previously (and more precisely) explained by Thayer's Neurovisceral Integration Model.
While other brain areas known to be involved in fear responses (e. g. the amygdala and periaqueductal gray) are mentioned by Porges, he does not integrate them into the description of his own hypothesized systems. The proposed anatomical difference between the vagus nerve origins of mammals vs. other vertebrates, even if it were borne out by more recent studies, would be an insufficient basis for explaining complex social and emotional behaviour differences.
In addition, polyvagal theory introduces the term "neuroception" for "a neural process that enables humans and other mammals to engage in social behaviors by distinguishing safe from dangerous contexts". It thus attempts to encompass several categories of psychological phenomena, each one of which constitutes a broad field of research in its own right: fear, threat perception, social behaviour, and emotion regulation. The neural substrates for many of the included phenomena are known at least tentatively, and comprise a large number of brain structures including, but not limited to, the vagus nerve. Polyvagal theory does not explain the mechanism of any of these phenomena with any precision, resulting in an oversimplification rather than an expansion or refinement of existing knowledge.