The polyvagal theory: phylogenetic substrates of a social nervous system

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Abstract

The evolution of the autonomic nervous system provides an organizing principle to interpret the adaptive significance of physiological responses in promoting social behavior. According to the polyvagal theory, the well-documented phylogenetic shift in neural regulation of the autonomic nervous system passes through three global stages, each with an associated behavioral strategy. The first stage is characterized by a primitive unmyelinated visceral vagus that fosters digestion and responds to threat by depressing metabolic activity. Behaviorally, the first stage is associated with immobilization behaviors. The second stage is characterized by the sympathetic nervous system that is capable of increasing metabolic output and inhibiting the visceral vagus to foster mobilization behaviors necessary for ‘fight or flight’. The third stage, unique to mammals, is characterized by a myelinated vagus that can rapidly regulate cardiac output to foster engagement and disengagement with the environment. The mammalian vagus is neuroanatomically linked to the cranial nerves that regulate social engagement via facial expression and vocalization. As the autonomic nervous system changed through the process of evolution, so did the interplay between the autonomic nervous system and the other physiological systems that respond to stress, including the cortex, the hypothalamic–pituitary–adrenal axis, the neuropeptides of oxytocin and vasopressin, and the immune system. From this phylogenetic orientation, the polyvagal theory proposes a biological basis for social behavior and an intervention strategy to enhance positive social behavior.

Introduction

Embedded in the mammalian nervous system are neuroanatomical structures related to the expression and experience of social and emotional behavior. Several of these structures are shared with other vertebrates and represent the product of phylogenetic development. Comparative research across vertebrate classes provides evidence that mammalian stress and coping response strategies are hierarchically ordered according to a phylogenetic stage (Porges, 1997, Porges, 1998). Although research has demonstrated the relevance of neuroanatomical structures and neurophysiological processes to the expression of emotion and the regulation of social behavior, contemporary theories have not incorporated an ‘evolution’ perspective.

Section snippets

Evolution as an organizing principle

Evolutionary forces have molded both contemporary physiology and behavior. The mammalian nervous system is a product of evolution. Via evolutionary processes, the mammalian nervous system has emerged with specific features that react to challenge in order to maintain visceral homeostasis. These reactions change physiological state and, in mammals, limit sensory awareness, motor behaviors, and cognitive potentials. We can intuitively grasp the limitations of behavior when described in terms such

The social engagement system

Through stages of phylogeny mammals and especially primates have evolved a functional neural organization that regulates visceral state to support social behavior. A social engagement system, which focuses only on the neural regulation of the striated muscles of the face and head and the specific autonomic functions mediated by the myelinated vagus, has been proposed as part of a more global social nervous system. Although other neural systems and behaviors are involved in social behavior, such

Neurophysiology of stress: limitations of arousal theory

For over a century, researchers have measured autonomic variables (e.g. heart rate, palmar sweat-gland activity) as indicators of emotional state related to perceived stress (e.g. fear, mental effort, workload, anxiety). Interest in measuring heart rate and sweat gland activity was theoretically supported by acceptance of the arousal theory. Arousal theory made the assumption that peripheral physiological measures regulated by the sympathetic branch of the autonomic nervous system provided

The evolution of the autonomic nervous system: emergent structures and the expression of emotions

Although there is an acceptance that the autonomic nervous system and the face play a role in emotional expression and social behavior, there is great uncertainty regarding the autonomic signature of specific or discrete emotions and the function of the autonomic nervous system in regulating social behavior. Most researchers evaluating autonomic responses during affective experiences, assumed, as did Cannon, that the sympathetic nervous system was the determinant of emotion, or at least the

Polyvagal theory: three phylogenetic systems

The polyvagal theory (Porges, 1995, Porges, 1997, Porges, 1998) emphasizes the phylogenetic origins of brain structures that regulate social and adaptive survival-oriented defensive behaviors. The polyvagal theory proposes that the evolution of the mammalian autonomic nervous system provides the neurophysiological substrates for the emotional experiences and affective processes that are major components of social behavior. The theory proposes that physiological state limits the range of

The vagal brake

The myelinated mammalian vagus is actively inhibitory of the sympathetic nervous system at the level of the heart. The mammalian vagus may function as an active vagal brake (see Porges et al., 1996) in which rapid inhibition and disinhibition of the vagal tone to the heart can rapidly mobilize or calm an individual. In addition, since the mammalian vagus has distinct pathways involved in the voluntary regulation of the striated muscles (e.g. corticobulbar pathways, afferents from face and

Evolution and dissolution: a hierarchical response strategy

The evolution of the autonomic nervous system provides substrates for the emergence of three adaptive stress and coping subsystems, each linked to structures that evolved during identifiable phylogenetic stages. The polyvagal theory proposes that during danger or threat the older, less social systems are recruited. The older systems, although functional in the short term, may result in damage to the mammalian nervous system when expressed for prolonged periods. Thus, the stress and coping

The social engagement system: an emergent property of the ventral vagal complex

Phylogenetically, the ventral vagal complex (VVC) is the most recent neurophysiological affect system. The VVC is composed of a somatomotor component, consisting of the special visceral efferent pathways, and a visceromotor component, consisting of the myelinated vagal pathways from the nucleus ambiguus to the sinoatrial node of the heart and the bronchi. As illustrated in Fig. 1, the special visceral efferents and the vagal brake collectively constitute an emergent social engagement system.

Measurement

In the psychophysiological literature, there is an assumption that respiratory sinus arrhythmia is an index of vagal influences to the heart. The polyvagal theory distinguishes between the rhythmic beat-to-beat changes in heart rate, mediated via the myelinated vagal pathways that originate in the nucleus ambiguus, and the conservative responses of bradycardia, mediated via the unmyelinated vagal pathways that originate in the dorsal motor nucleus of the vagus.

The nucleus ambiguus is a

Voodoo or vagus death: a test of the polyvagal theory

The polyvagal theory provides a theoretical framework to interpret the phenomenon of Voodoo or fright death described by Cannon (1957) and Richter (1957). Cannon believed that extreme emotional stress, regardless of the specific behavioral manifestation, could be explained in terms of degree of sympathetic-adrenal excitation. Voodoo death was assumed to be directly attributable to emotional stress. Being wed to a sympatho-adrenal model of emotional experience (see above), Cannon assumed that

Structures and functions of the adrenal gland

The adrenal gland exhibits phylogenetic changes in structure and function. Above, because of its complimentary function to the sympathetic nervous system, the adrenal medulla was discussed. However, since the adrenal cortex is treated as an endocrine organ and part of the HPA axis, it is traditionally studied and discussed independently of the adrenal medulla and the autonomic nervous system. Unlike the medulla, which is of ectodermal origin, the cortex is of mesodermal origin. The adrenal

A phylogenetic approach to the study of emotion, stress, and social behavior

The phylogenetic orientation focuses our interest on the neural structures and neurobehavioral systems that we share with, or have adapted from, our phylogenetic ancestry. First, the three response systems proposed in the polyvagal theory (i.e. the cranial nerve regulation of the striated muscles of the face coordinated with a myelinated vagus that inhibits sympathetic activity at the level of the heart, a sympathetic-adrenal system to increase metabolic output, and an inhibitory vagal system

Clinical applications of the polyvagal theory

The polyvagal theory, by describing both the phylogenetically based hierarchy of autonomic states and the specific triggers that cause a dissolution of this hierarchy, provides a new way of investigating atypical behavior. The theory emphasizes that the mammalian nervous system is not only sensitive to environmental demands and perceived stresses and threats, but that the mammalian nervous system will, in a predictable order, also rapidly reorganize to different neural-mediated states. Unlike

Conclusions

The polyvagal theory provides a theoretical platform to interpret social behavior within a neurophysiological context. The emphasis on phylogeny provides an organizing principle to understand the hierarchical sequence of adaptive responses. The social engagement system not only provides direct social contact with others, but also modulates physiological state to support positive social behavior by exerting an inhibitory effect on the sympathetic nervous system. From the polyvagal theory

Acknowledgements

This manuscript is based on an invited keynote address delivered at the 10th World Congress of the International Organization of Psychophysiology, which was held in Sydney, Australia, in February 2000. The preparation of this manuscript was supported in part by grants HD 22628 and MH 60625 from the National Institutes of Health and Human Development. Several of the ideas and concepts described in this paper were the product of discussions with C. Sue Carter during a residency at the Rockefeller

References (62)

  • Bazhenova, O.V., Plonskaia, O., Porges, S.W. Vagal reactivity and affective adjustment in infants during interaction...
  • D.C. Braga et al.

    Central oxytocin modulates exercise-induced tachycardia

    Am. J. Physiol.

    (2000)
  • G.A. Bray

    Autonomic and endocrine factors in the regulation of food intake

    Brain Res. Bull.

    (1985)
  • L. Bueno et al.

    Vagally mediated inhibition of acoustic stress-induced cortisol release by orally administered kappa-opiod substances in dogs

    Endocrinology

    (1989)
  • J.T. Cacioppo et al.

    Heterogeneity in neuroendocrine and immune responses to brief psychological stressors as a function of autonomic cardiac activation

    Psychosom. Med.

    (1995)
  • W.B. Cannon

    The mechanism of emotional disturbance of bodily functions

    N. Engl. J. Med.

    (1928)
  • W.B. Cannon

    ‘Voodoo’ death

    Psychosom. Med.

    (1957)
  • D.O. Carpenter

    Neural mechanisms of emesis

    Can. J. Physiol. Pharmacol.

    (1990)
  • C.S. Carter

    Neuroendocrine perspectives on social attachment and love

    Psychoneuroendocrinology

    (1998)
  • C.S. Carter et al.

    Integrative functions of lactational hormones in social behavior and stress management

    Ann. NY Acad. Sci.

    (1997)
  • Z. Cheng et al.

    Nucleus ambiguus projections to cardiac ganglia of rat atria: an anterograde tracing study

    J. Comp. Neurol.

    (2000)
  • Z. Cheng et al.

    Projections of the dorsal motor nucleus of the vagus to cardiac ganglia of rat atria: an anterograde tracing study

    J. Comp. Neurol.

    (1999)
  • M.D. De Bellis et al.

    Hypothalamic–pituitary–adrenal axis dysregulation in sexually abused girls

    J. Clin. Endocrinol. Metab.

    (1994)
  • W. Fan et al.

    Differential frequency-dependent reflex integration of myelinated and non-myelinated rat aortic baroreceptors

    Am. J. Physiol.

    (1998)
  • A.V. Ferguson et al.

    Functional neural connections of the area postrema

  • K. Fuxe et al.

    Volume transmission in transmitter peptide costoring neurons in the medulla oblongata

  • J. Garcia et al.

    A general theory of aversion learning

  • M.R. Gunnar et al.

    Neonatal stress reactivity: predictions to later emotional temperament

    Child Dev.

    (1995)
  • M.A. Hofer

    Cardiac respiratory function during sudden prolonged immobility in wild rodents

    Psychosom. Med.

    (1970)
  • D.A. Hopkins et al.

    Vagal efferent projections: viscerotopy, neurochemistry, and effects of vagotomy

    Prog. Brain Res.

    (1996)
  • J.H. Jackson

    Evolution and dissolution of the nervous system

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