The vagal paradox: A polyvagal solution

Although there is a consistent literature documenting that vagal cardioinhibitory pathways support homeostatic functions, another less frequently cited literature implicates vagal cardioinhibitory pathways in compromises to survival in humans and other mammals. The latter is usually associated with threat reactions, chronic stress, and potentially lethal clinical conditions such as hypoxia. Solving this 'vagal paradox' in studies conducted in the neonatal intensive care unit served as the motivator for the Polyvagal Theory (PVT). The paradox is resolved when the different functions of vagal cardioinhibitory fibers originating in two anatomically distinguishable brainstem areas are recognized. One pathway originates in a dorsal area known as the dorsal motor nucleus of the vagus and the other in a ventral area of the brainstem known as nucleus ambiguus. Unlike mammals, in all ancestral vertebrates from which mammals evolved, cardioinhibitory vagal fibers primarily originate in the dorsal motor nucleus of the vagus. Thus, in mammals the vagus nerve is 'poly' vagal because it contains two distinct efferent pathways. Developmental and evolutionary biology identify a ventral migration of vagal cardioinhibitory fibers that culminate in an integrated circuit that has been labeled the ventral vagal complex. This complex consists of the interneuronal communication of the ventral vagus with the source nuclei involved in regulating the striated muscles of the head and face via special visceral efferent pathways. This integrated system enables the coordination of vagal regulation of the heart with sucking, swallowing, breathing, and vocalizing and forms the basis of a social engagement system that allows sociality to be a potent neuromodulator resulting in calm states that promote homeostatic function. These biobehavioral features, dependent on the maturation of the ventral vagal complex, can be compromised in preterm infants. Developmental biology informs us that in the immature mammal (e.g., fetus, preterm infant) the ventral vagus is not fully functional and myelinization is not complete; this neuroanatomical profile may potentiate the impact of vagal cardioinhibitory pathways originating in the dorsal motor nucleus of the vagus. This vulnerability is confirmed clinically in the life-threatening reactions of apnea and bradycardia in human preterm newborns, which are hypothetically mediated through chronotropic dorsal vagal pathways. Neuroanatomical research documents that the distribution of cardioinhibitory neurons representing these two distinct vagal source nuclei varies among mammals and changes during early development. By explaining the solution of the 'vagal paradox' in the preterm human, the paper highlights the functional cardioinhibitory functions of the two vagal source nuclei and provides the scientific foundation for the testing of hypotheses generated by PVT.

Keywords: Autonomic nervous system; Dorsal vagus; Engagement system; Feelings of safety; Neuroception; Polyvagal theory; Threat reactions; Ventral vagal complex.

PMID: 38108034 PMCID: PMC10724739 DOI: 10.1016/j.cpnec.2023.100200