Cardiac vagal tone: a neurophysiological mechanism that evolved in mammals to dampen threat reactions and promote sociality

Abstract

The evolutionary journey from asocial reptiles to social mammals is highlighted by a reorganized autonomic nervous system with unique structural and functional changes in the vagus. These changes enable mammals to suppress defensive strategies in order to support and express sociality. The product of this transition is an autonomic nervous system with capacities to self-calm, to socially engage others, and to mitigate threat reactions in ourselves and others through social cues. For mammals, whose survival is dependent on their ability to cooperate, to connect, and to co-regulate, the ancient defense programs dependent on sympathetic activation supporting fight/flight behaviors, and vagal activation supporting death feigning, had to be harnessed and repurposed. This process resulted in a reorganized brainstem area, the ventral vagal complex, from which a unique branch of the vagus nerve enabled the expression of several uniquely mammalian features, including the ability to calm and to signal safety. Thus, sociality became embedded within specific neurobiological processes that had capabilities to mitigate threat and support mental and physical health. When this “calming” system is disrupted, prominent markers of chronic stress and core features shared by several psychiatric conditions are expressed (e.g., flat facial affect, poor vocal prosody, hypervigilance, hyper-reactivity, auditory and visual hypersensitivities). Anatomically, this vagal pathway is myelinated and originates in the brainstem structure called nucleus ambiguus. It provides the primary vagal regulation of organs above the diaphragm. This is distinct from the vagal pathways originating in the dorsal vagus nucleus, which are unmyelinated and provide the primary vagal regulation of organs below the diaphragm. The ventral vagal complex also regulates the striated muscles of the face and head and is greatly influenced by afferent pathways traveling through the vagus, trigeminal and facial nerves. Thus, in mammals, the brainstem areas regulating the heart and bronchi are interconnected with the areas regulating ingestion, facial expression, listening, breathing and vocalizations, to form an integrated social engagement system. In fact, intonations of vocalizations are mediated by the vagus, enabling prosodic features of voice to convey a relatively accurate index of vagal regulation of the heart1. Following the work of Jackson2, the polyvagal theory3 assumes a phylogenetic hierarchy in which the newer circuits inhibit the older. Thus, when the ventral vagus and the social engagement system are dampened or go offline, which frequently is observed during chronic stress and in response to threat, the autonomic nervous system moves into a sympathetic state that supports mobilization (e.g., fight/flight). If this functional shift in state does not lead to a positive outcome, then the autonomic nervous system may abruptly shut down via the dorsal vagal circuit (e.g., syncope, death feigning). Jackson described this process of sequentially disinhibiting older structures as dissolution or evolution in reverse. He used dissolution to explain the consequence of brain damage and disease, while polyvagal theory applies the principle to adaptive autonomic reactions to cues of threat, which may be reversible by cues of safety. In the realm of mental health, loss of access to the ventral vagus may be a product of chronic threat or a measurable core feature of several psychiatric disorders (e.g., post-traumatic stress disorder, PTSD), developmental disabilities (e.g., autism, Prader Willi syndrome), and disabling chronic pain. To survive, mammalian offspring must initially nurse as the primary mode of ingesting food. To nurse the infant must suck, a process dependent on a brainstem circuit involving the ventral vagal complex. Survival is dependent on the infant's nervous system efficiently and effectively coordinating suck-swallow-breathe-vocalize behaviors with vagal regulation of the heart through the ventral vagal pathways originating in the nucleus ambiguus. Through maturation and socialization, this “ingestive” circuit provides the structural neural platform (i.e., social engagement system) for sociality and co-regulation as major mediators to optimize homeostatic function leading to health, growth and restoration. In mammals, there is a dependency between reactions to contextual cues and the function of this circuit. Cues of threat may disrupt, while cues of safety may enhance function. The sensory branches of the facial and trigeminal nerves provide major input into the ventral vagal complex. Functionally, changes in the state of this circuit, through the process of dissolution, will either “disinhibit” phylogenetically older autonomic circuits to support defense (e.g., predator, disease, physical injury) or inform all aspects of the autonomic nervous system, including the enteric system4, to optimize homeostatic function. Polyvagal theory introduces “neuroception”, a neural process that evaluates risk and safety and reflexively triggers shifts in autonomic state without requiring conscious awareness. This reflexive process, distinct from perception, detects environmental and visceral features that are safe, dangerous or life-threatening5. Although many vertebrates have a capacity to detect pain and threat, mammals repurposed the neuroception capacity of their reptilian ancestors to not only react instantaneously to threat, but also to calm instantaneously to cues of safety. It is this latter feature that enables mammals to downregulate defensive strategies to promote sociality by enabling psychological and physical proximity without the consequences of injury. It is this calming mechanism that adaptively adjusts the central regulation of autonomic function to dampen sympathetic activation and to protect the oxygen-dependent central nervous system, especially the cortex, from the metabolically conservative defensive reactions of the dorsal vagal complex (e.g., syncope, diarrhea). This potential to calm autonomic state via the social engagement system is compromised in many psychiatric conditions, and leads to a variety of autonomic dependent comorbidities, including irritable bowel syndrome, migraine and fibromyalgia. However, being a common feature of several disorders limits the potential utility of measures of ventral vagal function in differential diagnoses, although it would highlight the potential of recruiting the ventral vagal pathway as a portal for treatment via technologies (e.g., vagal nerve stimulation). Our research documents that the quantification of the respiratory-related component of heart rate variability, known as respiratory sinus arrhythmia, provides a sensitive metric of the ventral vagus function (i.e., cardiac vagal tone)6. Applications of our method confirmed that respiratory sinus arrhythmia was even more sensitive than the assumed “gold standard” of cardiac vagal tone (i.e., changes in heart rate in response to vagal blockade). Respiratory sinus arrhythmia is a physiological phenomenon with an identifiable underlying neural mechanism reflecting ventral vagal control of the heart. With an accurate measure of ventral vagal function, there is the possibility to monitor autonomic adjustments to threat and safety. From a clinical perspective, the ability to monitor dampened vagal regulation would provide insight into understanding the mechanisms underlying clinical features. For example, chronic stress, clinical depression, or a life-threatening traumatic experience that may lead to PTSD could profoundly dampen ventral vagal regulation of the heart and the structures regulated by ventral vagal complex constituting the social engagement system7, 8. Disrupting the brainstem locus of social engagement system would functionally impair social communication and co-regulation by reducing vocal prosody and facial affect, and, through the loss of neural tone to the middle ear muscles, influence auditory processing by inducing hypersensitivity to low frequency background sounds and hyposensitivity to voice. In concert with these changes, brainstem communication with higher brain structures would impair cognitive function and affect regulation, while supporting the defense strategies of fight or flight or shutdown (e.g., syncope, dissociation). Monitoring ventral vagal function may provide an objective neurophysiological marker of clinical improvement9.

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