Table of contents
By Torsten Liem & Winfried Neuhuber
Comparative anatomical and functional studies argue against the postulated phylogenetic rootedness of polyvagal theory (PVT). Also, the term "polyvagal" in the neuroanatomical construct of PVT and in the functional construct of the system of social engagement is misleading, as the term implies that a "new" ventral vagal complex would exert coordinating function alongside an "old" dorsal one. The vagus nerve is certainly an important factor in the system of social engagement (in which the hypoglossal nerve should be included), but it is not the coordinator. Rather, the mesencephalic periaqueductal gray, along with the limbic system and neural brainstem networks, coordinates behavioral states such as fight and flight and freezing-with associated motor, autonomic, and endocrine effects. Ultimately, numerous other brain areas, if not the entire brain, act as systems of social engagement. Consequently, a reformulation, or at least a clarifying re-labeling, would be indicated.
1.1 The polyvagal theory
Since its first description by Stephen Porges in 1995 , polyvagal theory (PVT) has received much attention among mind-body therapists including osteopathy worldwide, especially with regard to the treatment of trauma patients. PVT is an attempt to explain the relationship between parasympathetic activity and behavior from an evolutionary perspective . It aims to provide an understanding of the links between brain and body processes .
The term "polyvagal" refers to 2 vagal circuits. One is the phylogenetically older unmyelinated system represented by the motor nucleus dorsalis n. vagi, which mainly innervates subdiaphragmatic organs (mainly the gastrointestinal tract), but also the heart, and is associated with immobilization and dissociation. Evolutionarily younger, according to Porges, a 2nd younger vagal pathway is thought to have evolved, observed only in mammals but not in reptiles, with the ability to downregulate immobilization and fight and flight behaviors. According to Porges, the anatomical structures of this component of the vagus interact in the brainstem with structures that innervate the striated muscles of the face and head to create an integrated system of social engagement . This younger system is represented in particular by the nucleus ambiguus. In PVT, it is associated with the other branchiomotor (specifically visceroefferent) nuclei of the Vth, VIIth, IXth, and XIth cranial nerves. Cranial nerves as the ventral vagal complex . This system regulates the heart and lungs via myelinated nerve fibers to allow resting states, and is thought to be associated with safety and social behavior .
The focus of PVT is on the phylogenetic shift between reptiles and mammals that resulted in specific changes in vagal pathways regulating the heart. Accordingly, primary vagal efferent pathways regulating the heart shifted from the dorsal nucleus of the vagus in reptiles to the nucleus ambiguus in mammals, establishing a face-heart connection with properties of a social engagement system that allows social interactions to influence visceral state and visceral dysfunction manifested in neural regulation of the heart .
1.2 Comparative anatomical and functional studies related to PVT
These studies argue against the proposed phylogenetic basis of PVT. It is undisputed that in mammals myelinated cardioinhibitory axons arise from the nucleus ambiguus. However, already in cartilaginous fish (elasmobranchs, e.g., sharks), which have existed for 400 million years, the cardioinhibitory vagus neurons are myelinated and conduct at speeds between 7 and 35 m/s (corresponding to mammalian B-fibers). Moreover, their cell bodies are located at 2 different sites in the brainstem (dorsal vagus nucleus and primordium of the nucleus ambiguus) . Thus, cartilaginous fish are already "polyvagal".
Lungfish, which are evolutionary precursors of air-breathing animals, also possess a myelinated cardiac vagus nerve that originates in dorsal and ventrolateral brainstem nuclei . These myelinated, fast-conducting axons enable beat-to-beat slowing of the heart rate, which is mandatory for the cardiorespiratory interactions observed in these ancient vertebrates, similar to mammalian respiratory sinus arrhythmia .
The unmyelinated vagal cardiac neurons of the nucleus dorsalis n. vagi most likely have no significant influence on heart rate and therefore cannot be held responsible for bradycardia observed in the freezing state. They seem to influence ventricular inotropy and might protect cardiomyocytes from ischemia .
1.3 Response patterns in PVT
PVT assigns reactions to perceived risks to 3 categories: feeling safe, being in danger, or perceiving a threat to life. These categories follow one another in phylogenesis. They are related to the adaptive behaviors of social communication (facial expressions, speech, listening), which are thought to be controlled by the nucleus ambiguus, and to defense in terms of mobilization (fight, flight) and immobilization response (vasovagal syncope, dissociation, immobilization or freezing state), which are controlled by the nucleus dorsalis n. vagi .
Again, the proposed association of these behavioral phenomena with the old unmyelinated or the new myelinated vagus nerve is misleading. The mammalian nucleus ambiguus contains, in addition to cardioinhibitory neurons, primarily branchiomotor (specifically visceroefferent) neurons for laryngeal, pharyngeal, and striated esophageal muscles , but does not control facial expression (mimic muscles are innervated by the n. facialis) nor hearing via the middle ear muscles (tensor tympani muscle, innervated by the motor branch of the trigeminal nerve, and stapedius muscle, innervated by the facial nerve) nor other head and neck muscles, as suggested by PVT. Also, conversely, the facial nucleus does not affect the ambiguous nucleus.
All these motor nuclei, including the hypoglossal nucleus, are coordinated by premotor networks in the lateral parvocellular and intermediate reticular formation . The intermediate reticular formation, located between the medial magnocellular and lateral parvocellular areas, also houses the neuronal networks for cardiovascular regulation (circulatory center) and the central generators for respiratory rhythm (pre-Bötzinger complex, respiratory center) and for swallowing and vomiting. Nucleus dorsalis n. vagi and nucleus ambiguus are anatomically and functionally embedded in these networks, but as output elements rather than coordinators. Vagal afferents are connected via the solitarius nucleus (nucleus tractus solitarii) not only to the motor vagus nuclei (nucleus dorsalis n. vagi and nucleus ambiguus), but also to the premotor networks of the formatio reticularis and the circulatory and respiratory centers . Equally important for the coordination of the entire head and neck motor system, however, are trigeminal and upper cervical spinal afferents, which are also fed to the premotor reticular networks.
1.4 Role of the mesencephalic periaqueductal gray (PAG)
A bilateral periventricular nucleus in the ventral mesencephalon, showing a similar location to the mammalian PAG, has already been described in the lamprey, which belongs to the oldest group of vertebrates living today . Behavioral states such as fight and flight, immobilization or freezing state, and risk assessment-with associated motor, autonomic, and endocrine effects-are coordinated by the mesencephalic periaqueductal gray (PAG) . The PAG is connected to the hypothalamus and limbic system (primarily the amygdala and prefrontal cortex)  as well as to various premotor and autonomic brainstem nuclei that coordinate respiration and the emotional motor system . The PAG receives afferents from almost all sensory systems - not least the nociceptive system - and modulates their processing .
Undoubtedly, the vagus nerve has a significant influence on emotions and various behavioral states due to its large afferent component. Vagal afferents, which constitute about 80% of its axons, are transmitted through the nucleus tractus solitarii to the PAG, hypothalamus, amygdala, as well as to the insular, cingulate, and prefrontal cortex, where they are integrated into emotional and cognitive processes . Recent studies suggest that subdiaphragmatic vagal afferents influence innate fear, learned fear, and other behaviors . Moreover, vagal afferents modulate spinal nociceptive processes in various experimental models .
It is true that Porges  mentions the representation of neuroanatomically already long known relations of the limbic system and PAG with the bidirectional connections to the vagus complex. However, since it is not the ventral vagus complex but the PAG in association with limbic and other brainstem networks that is responsible as a coordinator for these behavioral states and, moreover, numerous brain areas, if not the entire brain, function as a system of social engagement, the term "polyvagal" to characterize it seems a misleading misnomer.
As already shown by Grossman and Taylor , phylogenetic references are questionable as a basis for PVT. Facts of cranial nerve anatomy are also sometimes incorrectly represented in PVT. Instead of extending the notion of the ventral vagal complex to all branchiomotor nuclei, it would make more sense to leave them their autonomy and emphasize their coordination by a network of brainstem neurons.
The concept of the system of social engagement is plausible and seems relevant to practice. However, it is misleading and should be avoided to link it with the "old unmyelinated or new myelinated vagus" and the term "polyvagal". Moreover, the concept of the system of social engagement should also include the hypoglossal nerve, which, although not a branchiomotor nerve, innervates the socially important tongue muscles.
The mesencephalic trigeminal nucleus and other sensory trigeminal nuclei also play a major role in the coordination of orofacial motor function. The vagus nerve, efferent as well as afferent, is certainly an important factor in the system of social engagement. However, since the "new" vagus nerve in the form of the nucleus ambiguus does not exert a coordinating function on the other branchiomotor nuclei (V, VII, IX, XI), even though vagal afferents are fed into these coordination networks via the nucleus tractus solitarii, PVT turns the causal relationships on their head. Consequently, the term "polyvagal" is a misleading misnomer. The functional construct of the social engagement system should not be associated with the term "polyvagal". Perhaps a clarifying new designation would be indicated.
1. Porges SW. The polyvagal theory: phylogenetic substrates of a socialnervous system. Int J Psychophysiol 2001; 42 (2): 123–146
2. Porges SW. The polyvagal theory: phylogenetic contributions to socialbehavior. Physiol Behav 2003; 79 (3): 503–513
3. Porges SW. The polyvagal perspective. Biol Psychol 2007; 74 (2): 116–143
4. Porges SW, Dana D. Clinical Applications of the Polyvagal Theory: The Emergence of Polyvagal-Informed Therapies. New York: WW Norton; 2018
5. Porges SW. Social engagement and attachment: a phylogenetic perspective. Ann N Y Acad Sci 2003; 1008: 31–47
6. Porges SW. The Polyvagal Theory: Neurophysiological foundations of emotions, attachment, communication, and self-regulation. New York, NY: Norton; 2011
7. Porges SW, Kolacz J. Neurocardiology through the lens of the polyvagal theory. In: Gelpi RJ, Buchholz B. Neurocardiology: Pathophysiological Aspects and Clinical Implications. Elsevier; 2018
8. Barrett DJ, Taylor EW. The location of cardiac vagal preganglionicneurones in the brain stem of the dogfish Scyliorhinus canicula. J Exp Biol 1985; 117: 449–458
9. Barrett DJ, Taylor EW. The characteristics of cardiac vagal preganglionic motoneurones in the dogfish. J Exp Biol 1985; 117: 459–470
10. Monteiro DA, Taylor EW, Sartori MR et al. Cardiorespiratory interactions previously identified as mammalian are present in the primitive lungfish. Sci Adv 2018; 4 (2): eaaq0800
11. Grossman P, Taylor EW. Toward understanding respiratory sinusarrhythmia: relations to cardiac vagal tone, evolution and biobehavioral functions. Biol Psychol 2007; 74: 263–285
12. Porges SW. Love: an emergent property of the mammalian autonomic nervous system. Psychoneuroendocrinology 1998; 23: 837–861
13. Porges SW. The polyvagal perspective. Biol Psychol 2007; 74: 116–143
14. Porges SW. The polyvagal theory: new insights into adaptive reactions of the autonomic nervous system. Cleve Clin J Med 2009; 76 (suppl 2): S86–S90
15. Fritzsch B, Elliott KL, Glover JC. Gaskell revisited: new insights into spinal autonomics necessitate a revised motor neuron nomenclature. Cell Tissue Res 2017; 370: 195–209
16. Fay RA, Norgren R. Identification of rat brainstem multisynaptic connections to the oral motor nuclei using pseudorabies virus: I: Masticatory muscle motor systems. Brain Res Brain Res Rev 1997; 25 (3): 255–275
17. Fay RA, Norgren R. Identification of rat brainstem multisynaptic connections to the oral motor nuclei in the rat using pseudorabies virus: II: Facial muscle motor systems. Brain Res Brain Res Rev 1997; 25 (3): 276–290
18. Fay RA, Norgren R. Identification of rat brainstem multisynaptic connections to the oral motor nuclei using pseudorabies virus: III: Lingual muscle motor systems. Brain Res Brain Res Rev 1997; 25 (3): 291–311
19. Travers JB, Norgren R. Afferent projections to the oral motor nuclei in the rat. J Comp Neurol 1983; 220 (3): 280–298
20. Büttner-Ennever JA, Horn AKE. Solitary nucleus (SOL). In: Büttner-Ennever JA, Horn AKE. Olszewski and Baxter’s Cytoarchitecture of the Human Brainstem. 3. Aufl. Basel: Karger; 2014
21. Olson I, Suryanarayana SM, Robertson B, Grillner S. Griseum centrale, a homologue of the periaqueductal gray in the lamprey. IBRO Rep 2017; 2: 24–30
22. Deng H, Xiao X, Wang Z. Periaqueductal gray neuronal activities underlie different aspects of defensive behaviors. J Neurosci 2016; 36 (29): 7580–7588
23. Roelofs K. Freeze for action: neurobiological mechanisms in animaland human freezing. Philos Trans R Soc Lond B Biol Sci 2017; 372 (1718): 20160206
24. Jänig W. The integrative action of the autonomic nervous system. Cambridge: Cambridge University Press; 2006
25. Holstege G. The periaqueductal gray controls brainstem emotional motor systems including respiration. Prog Brain Res 2014; 209: 379–405
26. Craig AD. How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 2002; 3 (8): 655–666
27. Critchley HD, Mathias CJ, Dolan RJ. Neuroanatomical basis for first and second-order representations of bodily states. Nat Neurosci 2001; 4 (2): 207–212
28. Saper CB. The central autonomic nervous system: conscious visceral perception and autonomic pattern generation. Annu Rev Neurosci 2002; 25: 433–469
29. Berthoud HR, Neuhuber WL. Functional and chemical anatomy of the afferent vagal system. Auton Neurosci 2000; 85 (1–3): 1–17
30. Klarer M, Arnold M, Günther L et al. Gut vagal afferents differentially modulate innate anxiety and learned fear. J Neurosci 2014; 34 (21): 7067–7076
31. Klarer M, Krieger JP, Richetto J et al. Abdominal vagal afferents modulate the brain transcriptome and behaviors relevant to schizophrenia. J Neurosci 2018; 38: 1634–1647
32. Foreman RD, Qin C, Jou CJ. Spinothalamic system and viscerosomatic motor reflexes: functional organization of cardiac and somatic input. In: King HH, Jänig W, Patterson MM. The science and clinical application of manual therapy. Edinburgh: Churchill Livingstone; 2011: 11–127
33. Jänig W, Green P. Acute inflammation in the joint: its control by the sympathetic nervous system and neuroendocrine systems. Auton Neurosci 2014; 182: 42–54
34. Porges SW. Social engagement and attachment: a phylogenetic perspective. Ann N Y Acad Sci 2003; 1008: 31–47