The Polyvagal Theory: phylogenetic contributions to social behavior

Abstract

The scientific legacy of Paul MacLean provides important insights into the neural substrate of adaptive social behavior in mammals. Through his research and visionary conceptualizations, current investigators can legitimately study social behavior from a neurobiological perspective. His research and writings provided three important contributions. First, he emphasized the importance of evolution as an organizing principle that shaped both the structure of the nervous system and the adaptive social behavior. Second, by defining the limbic system, he legitimized the biological perspective in the study of emotion. Third, he recognized the important role of the vagal afferents in the regulation of higher brain structures. The paper will focus on the Polyvagal Theory. The Polyvagal Theory is a new conceptualization of the role of vagus and employs several features that MacLean emphasized including the importance of evolution, limbic structures and vagal afferents. The Polyvagal Theory builds on these early findings by MacLean and focuses on the link between phylogenetic changes in the autonomic nervous system and social behavior. By focusing on the phylogenetic changes in the structure of the vagus and the role that the vagus plays in the neural regulation of visceral state, new insights regarding social behavior emerge. Moreover, by articulating the phylogenetically organized hierarchy of neural circuits, insights into benefits of social behavior become evident as do an understanding of the behavioral and physiological features associated with stress and psychiatric disorders.

Introduction

As the scientific knowledge of neuroanatomy and neurophysiology expands, there is a growing interest in the role neural structures play in normal social behavior and in the expression of the atypical social behaviors that have been associated with several psychiatric disorders such as depression, autism and posttraumatic stress disorder. Recent advances in imaging methods have enabled researchers to study brain function and structure in the intact living individual. Now, neuronal function can be studied and the structural hypotheses derived from animal models and postmortem histology can be challenged and explained. The new methods of assaying brain structure and function, coupled with the breakthroughs in molecular genetics, are dominating the research in the neurobiology of social behavior and psychopathology. However, other research strategies, which provide an opportunity to dynamically monitor neural function with noninvasive technologies, are necessary for the development of an integrated neurobiological and neurobehavioral model of social behavior. Because autonomic function is intricately linked to observable motor behaviors, research investigating the neurophysiology of autonomic function is paramount among these strategies.

For decades, researchers studied autonomic function in clinical populations with the hope of gaining a new insight into the etiology of psychiatric disorders. Because noninvasive direct measurements of the nervous system and especially of the brain did not exist, early researchers intuitively monitored autonomic function as a noninvasive index of neural regulation of visceral state. As neuroscience advanced with more sensitive indicators of brain function, interest in the autonomic nervous system waned from a neural emphasis to a more global measurement of arousal and activation. Researchers lost the insight that the autonomic nervous system was not a separate neural system but is integrated into the function of other neural structures.

This paper focuses on how a specific component of the autonomic nervous system, the vagus, is involved in the expression of several of the behavioral, psychological and physiological features associated with social behavior. The vagus will be presented not only as a cranial nerve meandering through the periphery but also as an important bidirectional conduit carrying specialized motor and sensory pathways involved in the regulation of visceral state and affect. Moreover, it will be emphasized that spontaneous social engagement behaviors become more understandable if the autonomic nervous system, and especially the vagus, is included in the integrated model.