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By Torsten Liem & Winfried Neuhuber Comparative anatomical and functional studies argue against the postulated phylogenetic grounding of the Polyvagal Theory (PVT). In addition, the term “polyvagal” is misleading in the neuroanatomical construct of the PVT and in the functional construct of the social engagement system, as the term implies that a “new” ventral vagal complex would perform a coordinating function alongside an “old” dorsal one. The vagus nerve is certainly an important factor in the social engagement system (which should include the hypoglossal nerve), but it is not the coordinator. Rather, the mesencephalic periaqueductal gray, together with the limbic system and neuronal brainstem networks, coordinates behavioral states such as fight and flight as well as freezing—along with their associated motor, autonomic, and endocrine effects. Ultimately, numerous other brain regions—if not the entire brain—function as a social engagement system. Consequently, a reformulation, or at least a clarifying renaming, would be indicated.
1.1 The Polyvagal Theory
Since its first description by Stephen Porges in 1995 [1][2], the Polyvagal Theory (PVT) has received considerable attention worldwide among mind-body therapists, including in osteopathy, particularly with regard to the treatment of trauma patients. The PVT is an attempt to explain the relationship between parasympathetic activity and behavior from an evolutionary perspective [3]. It aims to create an understanding of the connections between processes in the brain and the body [1][2]. The term “polyvagal” refers to two vagal circuits. One is the phylogenetically older unmyelinated system, represented by the dorsal motor nucleus of the vagus nerve, which primarily innervates subdiaphragmatic organs (especially the gastrointestinal tract) but also the heart, and is associated with immobilization and dissociation. According to Porges, evolutionarily a second, younger vagal pathway is said to have developed that is observed only in mammals, not in reptiles, and has the ability to downregulate immobilization as well as fight-and-flight behavior. According to Porges, the anatomical structures of this vagal component interact in the brainstem with structures that innervate the striated muscles of the face and head to create an integrated social engagement system [4]. This younger system is represented in particular by the nucleus ambiguus. In the PVT, together with the other branchiomotor (especially visceromotor efferent) nuclei of cranial nerves V, VII, IX, and XI, it is referred to as the ventral vagal complex [5]. Via myelinated nerve fibers, this system regulates the heart and lungs to enable resting states and is said to be associated with safety and social behavior [6]. The focus of the PVT is on the phylogenetic shift between reptiles and mammals, which resulted in specific changes in the vagal pathways that regulate the heart. Accordingly, primary vagal efferent pathways regulating the heart shifted from the dorsal vagal nucleus in reptiles to the nucleus ambiguus in mammals, allowing a face–heart connection with characteristics of a social engagement system to become established, enabling social interactions to influence the visceral state and visceral dysfunctions that manifest in the neuronal regulation of the heart [7].
1.2 Comparative anatomical and functional studies related to the PVT
These studies argue against the proposed phylogenetic basis of the PVT. It is undisputed that in mammals, myelinated cardioinhibitory axons originate from the nucleus ambiguus. However, even in cartilaginous fish (elasmobranchs, e.g., sharks), which have existed for 400 million years, the cardioinhibitory vagal neurons are myelinated and conduct at speeds between 7 and 35 m/s (corresponding to the B fibers of mammals). In addition, their cell bodies are located in two different sites in the brainstem (dorsal vagal nucleus and primordium of the nucleus ambiguus) [8][9]. Thus, cartilaginous fish are already “polyvagal.” Lungfish, which are considered evolutionary precursors of air-breathing animals, also have a myelinated cardiac vagus nerve that originates in dorsal and ventrolateral brainstem nuclei [10]. These myelinated, fast-conducting axons enable beat-to-beat slowing of the heart rate, which is essential for the cardiorespiratory interactions observed in these ancient vertebrates, similar to the respiratory sinus arrhythmia of mammals [10][11]. The unmyelinated vagal cardiac neurons of the dorsal motor nucleus of the vagus nerve most likely have no significant influence on heart rate and therefore cannot be held responsible for bradycardia as observed in the freezing state. They appear to influence ventricular inotropy and could protect cardiomyocytes from ischemia [12].
1.3 Response patterns in the PVT
The PVT assigns responses to perceived risks to three categories: feeling safe, being in danger, or perceiving a threat to life. These categories follow one another in phylogeny. They are associated with adaptive behaviors of social communication (facial expression, speaking, listening), which are said to be controlled by the nucleus ambiguus, as well as with defense in the sense of mobilization (fight, flight) and the immobilization response (vasovagal syncope, dissociation, immobilization or freezing state), which are controlled by the dorsal motor nucleus of the vagus nerve [1][6][12][13][14]. Here, too, the proposed link between these behavioral phenomena and the old unmyelinated versus the new myelinated vagus nerve is misleading. In addition to cardioinhibitory neurons, the mammalian nucleus ambiguus contains primarily branchiomotor (especially visceromotor efferent) neurons for the laryngeal, pharyngeal, and striated esophageal musculature [15], but it controls neither facial expression (facial muscles are innervated by the facial nerve) nor hearing via the middle ear muscles (tensor tympani, innervated by the motor branch of the trigeminal nerve, and stapedius, innervated by the facial nerve) nor other head and neck muscles, as proposed by the PVT. Nor does the facial nucleus, conversely, influence the nucleus ambiguus. All these motor nuclei, including the hypoglossal nucleus, are coordinated by premotor networks in the lateral parvocellular and intermediate reticular formation [16][17][18][19][20]. The intermediate reticular formation, located between the medial magnocellular and the lateral parvocellular region, also contains the neuronal networks for cardiovascular regulation (circulatory center) and the central generators for respiratory rhythm (pre-Bötzinger complex, respiratory center) as well as for swallowing and vomiting. The dorsal motor nucleus of the vagus nerve and the nucleus ambiguus are anatomically and functionally embedded in these networks, but not as coordinators—rather as output elements. Via the solitary nucleus (nucleus tractus solitarii), vagal afferents are connected not only to the motor vagal nuclei (dorsal motor nucleus of the vagus nerve and nucleus ambiguus) but also to the premotor networks of the reticular formation as well as the circulatory and respiratory centers [20]. Equally important for coordinating overall head-and-neck motor function are trigeminal and upper cervical spinal afferents, which are also conveyed to the premotor reticular networks.
1.4 Role of the mesencephalic periaqueductal gray (PAG)
A bilateral periventricular nucleus in the ventral mesencephalon, showing a location similar to the mammalian PAG, has already been described in the lamprey, which belongs to the oldest group of vertebrates still living today [21]. Behavioral states such as fight and flight, immobilization or freezing, and risk assessment—along with their associated motor, autonomic, and endocrine effects—are coordinated by the mesencephalic periaqueductal gray (PAG) [22][23][24][25]. The PAG is connected to the hypothalamus and the limbic system (especially the amygdala and prefrontal cortex) [23][24] as well as to various premotor and autonomic brainstem nuclei that coordinate respiration and the emotional motor system [25]. The PAG receives afferents from almost all sensory systems—not least the nociceptive system—and modulates their processing [24]. Undoubtedly, due to its large afferent component, the vagus nerve has a significant influence on emotions and various behavioral states. Vagal afferents, which make up about 80% of its axons, are relayed via the nucleus tractus solitarii to the PAG, hypothalamus, amygdala, and to the insular, cingulate, and prefrontal cortex, where they are integrated into emotional and cognitive processes [26][27][28][29]. More recent studies suggest that subdiaphragmatic vagal afferents influence innate anxiety, learned fear, and other behaviors [30][31]. In addition, in various experimental models, vagal afferents modulate spinal nociceptive processes [32][33]. Although Porges [34] mentions the depiction of neuroanatomical relationships between the limbic system and the PAG that have long been known, along with the bidirectional connections to the vagal complex, the term “polyvagal” appears to be a misleading misnomer for its characterization, since it is not the ventral vagal complex but the PAG, together with limbic and other brainstem networks, that is responsible as the coordinator of these behavioral states, and since numerous brain regions—if not the entire brain—function as a social engagement system.
1.5 Conclusion
As Grossman and Taylor [11] already showed, phylogenetic references as a basis for the PVT are questionable. Facts of cranial nerve anatomy are also presented partly incorrectly in the PVT. Instead of extending the term ventral vagal complex to all branchiomotor nuclei, it would be more appropriate to preserve their independence and emphasize their coordination by a network of brainstem neurons. The concept of the social engagement system is plausible and appears relevant in practice. However, it is misleading and should be avoided to link it to the “old unmyelinated versus new myelinated vagus” and the term “polyvagal.” In addition, the concept of the social engagement system should also include the hypoglossal nerve, which, although not a branchiomotor nerve, innervates the socially important tongue musculature. The mesencephalic trigeminal nucleus and other sensory trigeminal nuclei are also of great importance for coordinating orofacial motor function. Efferently as well as afferently, the vagus nerve is certainly an important factor in the social engagement system. However, since the “new” vagus nerve in the form of the nucleus ambiguus does not exert a coordinating function over the other branchiomotor nuclei (V, VII, IX, XI)—even if vagal afferents are fed into these coordination networks via the nucleus tractus solitarii—the PVT turns the causal relationships on their head. The term “polyvagal” is therefore a misleading misnomer. The functional construct of the social engagement system should not be linked to the term “polyvagal.” A clarifying renaming may be indicated. Publication: Liem T, Neuhuber W. Critique of the Polyvagal Theory. DO – Deutsche Zeitschrift für Osteopathie. 2021; 19: 34–37. Article on ScienceDirect “The Polyvagal Theory in Osteopathy”
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