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This paper is based on the presidential address to the Society for Psychophysiological Research, Atlanta, Georgia, October 8, 1994. The presidential address and the published manuscript are dedicated to the memory of my close friend and collaborator, Robert E. Bohrer. The theory described in this paper evolved from over three decades of research and interactions with colleagues and students. I am indebted to four individuals who have served as scientific guides. David C. Raskin introduced me to psychophysiology. Robert E. Bohrer tutored me in time series statistics. Ajit Maiti mentored me in the neurophysiology and embryology of the brain stem. Evgeny Sokolov provided a model as a mentor and stimulated me to generate an integrative theory. Additionally, I have been fortunate to have outstanding associates, collaborators, and students including Olga Bazhenova, Evan Byrne, Michael Cheung, Aaron Chun, Georgia DeGangi, Janet DiPietro, Yoel Donchin, Jane Doussard-Roosevelt, Nathan Fox, Phil Goddard, Stanley Greenspan, Sandy Larson, Susan Linnemeyer, Phil McCabe, Oxana Plonskaia, Lourdes Portales, Shawn Reed, Todd Riniolo, Pat Suess, and Brandon Yongue who have contributed to the research and development of The Poly-Vagal theory. An additional thanks to Jane Doussard-Roosevelt who provided the intellectual and emotional ballast in my laboratory during my presidency and who contributed to the manuscript and talk by editing earlier versions and generating the graphics. A special thanks to Sue Carter who has patiently supported my scientific curiosity for 25 years and who has provided several helpful comments in the organization of the manuscript. The preparation of this manuscript was support, in part by grant HD 22628 from the National Institute of Child Health and Human Development and by grant MCJ 240622 from Maternal and Child Health Bureau. Address reprint requests to Stephen W. Porges, Department of Human Development, University of Maryland, College Park, Maryland 20742, or email at email@example.com.
Figure 1. Primary brainstem nuclei of the vagus. Nuclei are bilateral and only one of each bilateral pair is illustrated. Figure 2. (a) Bradycardia during fetal distress. (b) Background heart period variability at time of bradycardia. Figure 3. Bradycardia elicited by electrical stimulation of the DMNX in an anesthetized rabbit. Figure 4. Bradycardia elicited by aortic depressor nerve stimulation in an anesthetized rabbit. Figure 5. Topographic organization of the nucleus ambiguus in the rat (Bieger & Hopkins, 1987).
Title of the paper.
The title was selected to emphasize the concept that evolutionary processes have sculpted the neural regulation of autonomic function. Not only has evolution provided obvious divergences in behavior and appearance, but evolution has impacted on the autonomic strategies related to the detection of novelty in the environment. The focus of the paper was not directed at a theory of orienting, nor has the paper attempted to distinguish between the autonomic components of orienting or defensive reflexes. Rather, the paper has focused on the neurogenic regulation of cardiac responses via two vagal responses systems. A primitive system that we have inherited from reptiles produces a rapid neurogenic bradycardia that reduces the activity of our cardiopulmonary system to conserve oxygen. This is the strategy of sit and wait feeders, common to reptiles. In contrast, the evolution of the energy-demanding mammal required two autonomic-behavioral shifts: 1) mammals needed to obtain great amounts of food; and 2) mammals needed to protect their nervous systems from oxygen loss. These two objectives are linked. In the evolution of mammals, success in obtaining food resources was dependent upon the ability to detect threat. Thus, mobilization and attention became two important behavioral dimensions. Unlike reptiles, which orient in response to novelty and attack or return to a quiescent state or lumber off, mammals orient and then attend. Following this phase of attention a mammal may rapidly depart or approach (attack) within the context of the classic fight or flight response. With the increasing complexity of behavior, there is a parallel increase in complexity in the organization and function of the autonomic nervous system. The title also intended to emphasize the concept that evolution has placed mammals in a defensive world. The survival systems of reptiles and other lower phyla can be organized into orienting and defensive dimensions. Mammals, to survive in this defensive and reactive world, had to circumvent these potentially lethal reactions of other species. The evolution of the mammalian nervous system enables mammals to rapidly escape danger and to use neural resources for the complex information processes required to detect subtleties in the environment. Moreover, evolution promoted additional motor systems related to communication. Motor systems developed to communicate conditions related to survival with facial expressions and vocalizations associated with primary emotions. The evolutionary modifications not only had to coexist with the oxygen hungry metabolic system, but by increasing the complexity of motor behaviors, there was an additional increase in oxygen needs. Thus, there is a link between the special visceral efferent actions regulating the communicative processes of emotion, and later language, with the general visceral efferent actions regulating cardiopulmonary function. The ability to detect subtleties in the environment coupled with the ability to communicate threat or comfort via facial expressions and vocalizations contributed to within- species social behavior, parenting, and pairbonding. These complex functions evolved while the demanding oxygen needs of mammals were programmed into the background of nervous system function via the autonomic nervous system.
In discussing any theoretical perspective, it is important to place the ideas and speculations in the context of earlier research conducted by the investigator. My early research focused on the use of heart rate measures as indicators of attention. While conducting research for my master's thesis (Porges & Raskin, 1969), I noted that attention demanding tasks produced heart rate response patterns with two prominent characteristics. First, heart rate exhibited a rapid transitory directional change in response to task onset and stimulus changes. Second, when subjects became involved in the task and focused their attention on the task demands, heart rate variability was reduced. I was intrigued with these observations and speculated on the possible physiological mechanisms. This evolved into a two-component theory of attention in which the components were labeled "phasic or orienting" and "tonic or attention" responses (Porges, 1972). These findings stimulated me to investigate neural mechanisms of heart rate regulation and to develop the Vagal Tone Index () of RSA, which I believed would help provide insight into the mechanisms mediating the more tonic sustained attention response. The preceding sections of this paper provide the basis for the Poly-Vagal Theory and enable an interpretation of the two heart rate components associated with attention. The first component, associated with orienting and the neurogenic bradycardia, is determined reflexively by the vegetative vagus, originating in the dorsal motor nucleus. The second component, associated with voluntary engagement with the environment and depression of RSA, is determined by the smart vagus, originating in the NA. Thus, after years of studying heart rate patterns, a speculative two-component psychophysiological model of attention is evolving into the neuroanatomically and neurophysiologically based Poly-Vagal Theory.
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