Dr. Porges Responds to Polyvagal Theory Critiques
Abridged by Polyvagal Institute with permission, August 2023
CRITICISM:
In a 2023 review of the literature, Paul Grossman 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."
Grossman, Paul (2023). Fundamental challenges and likely refutations of the five basic premises of the polyvagal theory. Biological Psychology. doi:10.1016/j.biopsycho.2023.108589.
RESPONSE FROM DR. PORGES:
Statements like this as ‘criticism’ are not very constructive in resolving any disagreement. First, what data substantiates his statement of consensus? Who are the experts with sufficient knowledge of the theory to make these judgments? Second, which specific assumptions is he referring to? Without a clear statement of the theory and the assumptions associated with the theory the ‘tenability’ of any aspect of the theory cannot be judged.
If we define ‘consensus’ acceptance of the theory within peer reviewed publications, then PVT would be viewed as having broad consensus among peers involved in the research relevant to PVT. This broad acceptance is substantiated by the approximately 20,000 peer reviewed articles in academic science.
Statements like this, often supported by research conducted by Edwin Taylor, and repeated by Paul Grossman, have frequently been used to dispute PVT. However, as documented in Porges (2023), Taylor’s papers have repeatedly misrepresented PVT; they have argued that their misrepresentations, and not any specific aspect of the theory, are evidence that PVT is untenable. In dealing with any criticism of PVT, it is first necessary to have the critic articulate the point of disagreement, which requires the critic to document how the point of contention is actually represented in PVT and why it is wrong.
If there were truly ‘broad consensus’ documenting that the underlying polyvagal hypotheses had been falsified and the foundational science upon which PVT rests was truly unsubstantiated, it would represent a major consequence to our understanding of many biologically informed sciences. If this falsification was substantiated it would have effectively falsified evolution and how evolution is mirrored in embryology. It would have falsified the Jacksonian principle of dissolution (a guiding principle in neurology), it would have falsified Taylor’s documentation of ventral migration of cardioinhibitory neurons in the brainstem, and it would have falsified Grossman’s own research documenting that the suppression of RSA is a vagal phenomenon. Finally, this quote, by not inviting dialog or alternative perspectives, makes such sweeping and biased claims that it’s hard not to question what the critic actually knows about PVT.
See:
Sections 17 and 18 of the Vagal Paradox paper for more detail.
CRITICISM:
Neuhuber and Berthoud (2022) state that polyvagal theory's "basic phylogenetic and functional-anatomical tenets do not withstand closer scrutiny". 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 (Porges, 2001)" and the dorsal vagal complex "should not be linked to passive defensive behavior".
Neuhuber, Winfried; Berthoud, Hans-Rudolf (2022-10-01). Functional anatomy of the vagus system: How does the polyvagal theory comply?. Biological Psychology. 174: 108425. doi:10.1016/j.biopsycho.2022.108425. PMID 36100134. S2CID 252188181.
RESPONSE FROM DR. PORGES:
Scientists are entitled to their opinion, but an opinion does not falsify a theory. PVT emphasizes the role of the different vagal circuits in supporting a threat physiology. It uses supporting literature that proposes the species-specific responses of prey species who do freeze. See section 3, paragraph 8, as well as sections 11-13 of
the Vagal Paradox paper.
But, more specifically, in the updated paper (Porges, 2023) the role of the dorsal vagal complex is elaborated to include widely accepted threat reactions including reduction of blood pressure that potentially could trigger fainting and the frequently reported experienced effect of threat on the gut. In discussing dorsal vagal defense reactions, PVT acknowledges that the neural pathways are still being explored in research and that the most reliable vagal effect mediated via the dorsal vagus may not be heart rate slowing, but reduction of contractility leading to a drop in blood pressure as well as profound effects on digestion resulting in bowel evacuation and gut pain. Personally, as research progresses, I am curious to learn more about how the dorsal vagus can shift its role from supporting homeostatic function by protecting the myocardium and the gut to a pathway that would disrupt homeostatic function with potential damaging consequences.
CRITICISM:
Regarding the proposed "ventral vagal complex," Neuhuber and Berthoud state that "the PVT, by construing 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' (Porges, 2001)," 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 is not the case [...]."
RESPONSE FROM DR. PORGES:
This is a good example of incorrect paraphrasing. PVT goes to great lengths to focus not on the vagus but on the brainstem area from which the vagus emerges. The vagus is a conduit in PVT, which is far from a ‘prime mover.’ Neuhuber and Berthoud are entitled to their opinion, but that does not substantiate their incorrect inference.
It is important to note that the central vagal complex as proposed in PVT is the product of a ventral migration of cardioinhibitory neurons from the dorsal motor nucleus of the vagus to a brainstem area that regulates the striated muscles of the face and head. It is this ventral migration that provided the neuroanatomical substrate that enabled mammals to nurse and subsequently to engage in social behavior as a co-regulatory system. It is clear that this point is not understood in framing the above criticism, which does not appreciate the conceptualization of the social engagement system as the functional output of the interneuronal connections among the nuclei composing the ventral vagal complex. These points are elaborated in
Porges (2023) in Sections 6-9.
CRITICISM:
Taylor, Wang & Leite (2022) regard it as "invalid to refer to this as a 'vagal system' or to postulate the existence of a 'smart vagus.'"
Taylor, Edwin; Wang, Tobias; Leite, Cleo (2022-06-28). An overview of the phylogeny of cardiorespiratory control in vertebrates with some reflections on the 'Polyvagal Theory'. Biological Psychology. 172: 108382.
RESPONSE FROM DR. PORGES:
Again, this is an opinion and as long as the definitions are clear it should not be ‘invalid’ to use a term not in agreement with other opinions. Initially, as PVT emphasized the link between intentionality (overt behavior) and ventral vagal function, the ventral vagus was labeled the ‘smart’ vagus. This was later dropped (at least 20 years ago), since it implied an ‘executive’ function, which was not the intention. The term was meant to highlight the autonomic state that might optimize higher brain functions while the dorsal vagus was initially labeled the ‘vegetative’ vagus since it was involved in background homeostatic processes as well as being recruited in survival reactions. It would have been helpful to Taylor and his group in framing their criticisms, if they carefully read the primary papers describing the theory. In response to a changing scientific background, the theory has been refined and updated several times during the 30 years since its inception.
CRITICISM:
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.
Grossman, Paul; Taylor, Edwin W. (2007-02-01). Toward understanding respiratory sinus arrhythmia: Relations to cardiac vagal tone, evolution and biobehavioral functions. Biological Psychology. 74 (2): 263–285. doi:10.1016/j.biopsycho.2005.11.014.
RESPONSE FROM DR. PORGES:
This is an uninformed criticism of PVT. The following is taken from
section 18 of the recently published Vagal Paradox paper:
Taylor and colleagues have also questioned the assumption that the dorsal motor nucleus of the vagus is an evolutionarily older structure than the ventral vagus. It has been reliably documented that prior to mammals the prominent cardioinhibitory vagal neurons in vertebrates originated in the dorsal motor nucleus of the vagus. Thus, it is indisputable that estimating an evolutionary timeline through phylogeny, cardioinhibitory neurons originated first in the dorsal motor nucleus of the vagus and then, consistent with Taylor’s own work [36], migrated ventrally. In the earliest (now extinct) mammals this ventral migration was sufficiently complete to embed cardioinhibitory functions with activities of branchiomotor neurons (i.e., special visceral efferent pathways) that regulate the striated muscles of the face and head promoting ingestion (e.g., nursing) and social communication via facial expression and vocalizations.
CRITICISM:
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. 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."
Monteiro, Diana (2018). Cardiorespiratory interactions previously identified as mammalian are present in the primitive lungfish. Science Advances. 4 (2): eaaq0800. Bibcode:2018
RESPONSE FROM DR. PORGES:
The following is taken from
section 9 and
section 18 of the recently published Vagal Paradox paper:
Describing respiratory-heart rate patterns in other vertebrates does not mean that the neural mechanisms are identical to those observed in mammals. In fact, in vertebrate species other than mammals, except for the report of a myelinated cardioinhibitory pathway emerging from the dorsal motor nucleus of the vagus in the lungfish [49], all reports document that heart rate-respiratory interactions were mediated via unmyelinated vagal cardioinhibitory pathways originating in the dorsal motor nucleus of the vagus. The identification of the myelinated fibers in the lungfish have been misused to infer a ‘fatal flaw’ in PVT. However, the identification of myelinated vagal fibers in lungfish is unrelated to PVT and reflects a misunderstanding of PVT. The lungfish appears to be a phylogenetic outlier, having vertebrate ancestry that did not have myelinated cardioinhibitory dorsal vagal fibers nor has this feature been reliably transmitted to the groups of vertebrates that subsequently evolved (i.e., amphibia, reptiles, mammals).
CRITICISM:
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."
Grossman, Paul (2023). Fundamental challenges and likely refutations of the five basic premises of the polyvagal theory. Biological Psychology. doi:10.1016/j.biopsycho.2023.108589.
RESPONSE FROM DR. PORGES:
This is another uninformed statement. PVT emphasizes that the source nucleus of myelinated vagal pathways conveying a respiratory rhythm in mammals is the ventral vagus. This does NOT occur in reptiles. This point is consistent with the research literature for several decades.
See Section 18 of The Vagal Paradox for more detail.
CRITICISM:
Results reviewed by Taylor, Leite and Skovgaard (2010) "refute the proposition that centrally controlled cardiorespiratory coupling is restricted to mammals, as propounded by the polyvagal theory of Porges."
Taylor; Leite; Skovgaard (2010). Autonomic control of cardiorespiratory interactions in fish, amphibians and reptiles.
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.
Taylor, Edwin; Wang, Tobias; Leite, Cleo (2022-06-28). An overview of the phylogeny of cardiorespiratory control in vertebrates with some reflections on the 'Polyvagal Theory.' Biological Psychology. 172: 108382.
RESPONSE FROM DR. PORGES:
In this section Taylor and his research team repeatedly confuse mammalian RSA, which is dependent on myelinated vagal fibers originating in the ventral vagus (nucleus ambiguus) that have an inherent respiratory rhythm, with non-mammalian cardio-respiratory coupling that involves vagal fibers from the dorsal motor nucleus of the vagus. This criticism reflects a feature of Taylor's repeated strawman arguments. PVT does NOT make this proposition.
CRITICISM:
The dichotomy between asocial reptiles and social mammals subscribed to by polyvagal theory has been contested. Doody, Burghardt & Dinets (2023) 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."
Doody; Burghardt; Dinets (2023). The evolution of sociality and the polyvagal theory. Biological Psychology.
RESPONSE FROM DR. PORGES:
The following reply is excerpted from
Section 18 of the newly published Vagal Paradox paper:
These criticisms are irrelevant to PVT, which is mammal centric. Sociality through a polyvagal lens focuses on the transformative qualities of social behavior expressed in mammals and not observed in reptiles such as nursing during mother-infant interactions, vocal intonations, facial expressions, and other co-regulatory behaviors that have profound impact on calming autonomic state to optimize homeostatic functions. This criticism is not only applying the theory to questions in another discipline, but to a question (i.e., social behavior in reptiles) that has been explicitly stated to be outside the scope of the theory.
CRITICISM:
Polyvagal theory proposes a relationship between RSA responses and forms of psychopathology, but a meta-analysis finds the empirical evidence to be inconclusive.
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.
RESPONSE FROM DR. PORGES:
The PVT does not make that proposition, since it does not adhere to psychophysiological parallelism (see Porges, S. W., 2022, Polyvagal Theory: A Science of Safety. Frontiers in Integrative Neuroscience, 16, 27.) in which a physiological marker would be a defining feature of mental health diagnosis. However, research informed by PVT would test hypotheses that might investigate such a relationship. A PVT informed hypothesis would focus on compromised vagal regulation being more frequently observed in individuals with specific clinical disorders such as depression or anxiety. Thus, there might be bias within these clinical diagnostic groups to be in autonomic states of defense. In general this is the case, and I have published several papers in this general area. A simple Google Scholar search will identify hundreds of papers documenting association between indices of RSA and mental health features. This does not preclude that there may be a large overlap in the distributions between those without diagnoses and diagnosed participants. The relationship is far from causal and its relationship with PVT is linked to the autonomic characteristics mediating mental health symptoms and NOT mental health diagnoses being defined by autonomic features.
CRITICISM:
According to Grossman and Taylor, 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.
Grossman, Paul; Taylor, Edwin W. (2007-02-01). Toward understanding respiratory sinus arrhythmia: Relations to cardiac vagal tone, evolution and biobehavioral functions. Biological Psychology. 74 (2): 263–285. doi:10.1016/j.biopsycho.2005.
RESPONSE FROM DR. PORGES:
This conclusion is dependent on Grossman and Taylor using a poor metric to quantify RSA. The vulnerability of their metric has been substantiated in peer reviewed publications (see Lewis et al. 2011; Byrne & Porges, 1996). However, when an appropriate method is used, RSA maps into the cholinergic influence (see Lewis et al., 2011, Porges, 1986). Recent papers (e.g., Gourine et al., 2016) emphasize that the respiratory pattern in HR (RSA) is a reliable marker of ‘ventral vagal tone.’ Interestingly, this phenomenon was reported by Hering in 1910, although it took decades to refine the methodology to accurately monitor ventral vagal tone via RSA.
Lewis et al., 2011 and A.V. Gourine, A. Machhada, S. Trapp, K.M. Spyer, Cardiac vagal preganglionic neurones: an update. Auton. Neurosci. 199 (2016) 24–28. https://doi.org/10.1016/j.autneu.2016.06.003
CRITICISM:
Reviewing more recent evidence, Paul Grossman 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."
Grossman, Paul (2023). Fundamental challenges and likely refutations of the five basic premises of the polyvagal theory. Biological Psychology. doi:10.1016/j.biopsycho.2023.108589.
RESPONSE FROM DR. PORGES:
These are poorly informed comments. The methodology used to quantify RSA greatly influences its sensitivity to vagal influences (see Lewis et al. 2011; Bryan & Porges, 1996). Again, when appropriate methods are used, RSA maps into the cholinergic influence. See
section 7.4 of The Vagal Paradox:
'There are publications with rabbits and rats documenting fear-induced bradycardia. However, the strongest evidence comes from my laboratory in which preterm infants were tested. Preterm infants are at a phase of maturation that results in an autonomic nervous system without a functional ventral vagal circuit. This results in a propensity to react with clinically relevant massive bradycardia - as is prevalent in the perinatology literature (see Reed et al., 1999).’
CRITICISM:
In a 2021 publication, Porges states that "the theory was not proposed to be either proven or falsified." Falsifiability is a central tenet of the scientific method.
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
RESPONSE FROM DR. PORGES:
This is taken out of context and the author presumes to know my motivation in developing the theory. It would be helpful to read the complete paragraph, which puts the phrase in context:
The theory was not proposed to be either “proven” or “falsified,” but rather to be informed by research and modified. Claims of falsification would argue that the evolved changes in the autonomic nervous system would not support a social engagement system and that socially delivered cues of safety would not calm the autonomic nervous system and consequently socialize behavior.
The theory is dependent on evolution and development to structure a hierarchical model of autonomic function inclusive of the Jacksonian principle of dissolution. This model could explain how co-regulatory social interactions are not merely ‘social’ behaviors, but neuromodulators of autonomic state via an integrated social engagement system that is capable of either supporting or disrupting homeostatic functions. Thus, aspects of social behavior can functionally support or disrupt health.
The theory uses evolution to extract a phylogenetic sequence of autonomic regulation. This sequence identifies stages during vertebrate evolution when a spinal sympathetic nervous system and the two vagal pathways emerge and become functional via maturation in mammals. It would be difficult to argue that the sequence does not occur, although it would be possible to identify antecedent similarities in most vertebrates regardless of class or group. The question is not whether there are similarities in ancestral vertebrates, but rather how these circuits have been adapted to provide a unique mammalian autonomic nervous system that is intimately intertwined with co-regulatory social behavior.
