POLYVAGAL THEORY of EMOTION

A text version of the full article below appears at http://terpconnect.umd.edu/~sporges/nyas/nyas.txt or visit the website of Steven Porges with more articles at www.stephenporges.info


Paper to be published in C. S. Carter, B. Kirkpatrick, & I.I. Lederhendler (eds.), The Integrative Neurobiology of Affiliation, Annals of the New York Academy of Sciences.

Emotion: An Evolutionary By-Product of the Neural Regulation of the Autonomic Nervous System

Stephen W. Porges
Institute for Child Study
University of Maryland
College Park, Maryland 20742-1131

INTRODUCTION

A new theory, the Polyvagal Theory of Emotion, is
presented which links the evolution of the autonomic nervous
system to affective experience, emotional expression, vocal
communication and contingent social behavior. The Polyvagal
Theory is derived from the well-documented phylogenetic shift
in the neural regulation of the autonomic nervous system that
expands the capacity of the organism to control metabolic
output. The Theory emphasizes the phylogenetic dependence of
the structure and function of the vagus, the primary nerve of
the parasympathetic nervous system. Three phylogenetic
stages of neural development are described. The first stage
is characterized by a primitive unmyelinated vegetative vagal
system that fosters digestion and responds to novelty or
threat by reducing cardiac output to protect metabolic
resources. Behaviorally, this first stage is associated with
immobilization behaviors. The second stage is characterized
by a spinal sympathetic nervous system that is capable of
increasing metabolic output and inhibiting the primitive
vagal system's influence on the gut to foster mobilization
behaviors necessary for "fight or flight." The third stage
is unique to mammals and is characterized by a myelinated
vagal system that can rapidly regulate cardiac output to
foster engagement and disengagement with the environment.
The myelinated vagus originates in a brainstem area that
evolved from the primitive gill arches and in mammals
controls facial expression, sucking, swallowing, breathing,
and vocalization. It is hypothesized that the mammalian
vagal system fosters early mother-infant interactions and
serves as the substrate for the development of complex social
behaviors. In addition, the mammalian vagal system has an
inhibitory effect on sympathetic pathways to the heart, and
thus, promotes calm behavior and pro-social behavior.

The Polyvagal Theory of Emotion proposes that the
evolution of the autonomic nervous system provides the
organizing principle to interpret the adaptive significance
of affective processes. The Theory proposes that the
evolution of the mammalian autonomic nervous system, and
specifically the brainstem regulatory centers of the vagus
and other related cranial nerves, provides substrates for
emotional experiences and affective processes that are
necessary for social behavior in mammals. In this context,
the evolution of the nervous system limits or expands the
ability to express emotions, which in turn may determine
proximity, social contact, and the quality of communication.
The polyvagal construct has been previously introduced1 to
document the neurophysiological and neuroanatomical
distinction between the two vagal branches and to propose
their unique relation with behavioral strategies. This paper
elaborates on the polyvagal construct and proposes that
affective strategies are derivative of the evolutionary
process that produced the polyvagal regulation.

There is a consensus that affect is expressed in facial
muscles and in organs regulated by the autonomic nervous
system. However, with the exception of work by Cannon,2,3
which focused on the sympathetic-adrenal system as the
physiological substrate of emotion, the presumed neural
regulation of affective state has not been investigated.
Even contemporary researchers investigating affective
signatures in the autonomic nervous system4-7 have tacitly
accepted Cannon's assumption that emotions reflect responses
of the sympathetic nervous system.

Unlike the architectural dictum that form (i.e.,
structure) follows function, the function of the nervous
system is derivative of structure. The flexibility or
variability of autonomic nervous system function is totally
dependent upon the structure. By mapping the phylogenetic
development of the structures regulating autonomic function,
it is possible to observe the dependence of autonomic
reactivity on the evolution of the underlying structure of
the nervous system. The phylogenetic approach highlights a
shift in brainstem and cranial nerve morphology and function
from an oxygen-sensitive system (i.e., the primitive gill
arches) to a system that regulates facial muscles, cardiac
output and the vocal apparatus for affective communication.

. . . . . . . . . .


AUTONOMIC DETERMINANTS OF EMOTION

Over the past 100 years we have learned much about the
autonomic nervous system, its evolutionary origins and how it
relates to emotion. Initially, we can distinguish among
three components of the autonomic nervous system (i.e.,
visceral afferents, sympathetic nervous system, and
parasympathetic nervous system) and speculate how each might
be related to affective experiences. First, the visceral
afferents may be assumed to play a major role in determining
"feelings." These mechanisms, which provide us with
knowledge of hunger, also may convey a sense of nausea during
emotional distress. We frequently hear subjective reports of
individuals feeling "sick to their stomach" during periods of
severe emotional strain associated with profound negative
experiences. Similarly, negative states have been associated
with reports of breathlessness or feelings that the heart has
stopped. Second, the sympathetic nervous system and adrenal
activity are associated with mobilization. Activation of the
sympathetic nervous system is usually linked to increased
skeletal movement of the major limbs. Thus, consistent with
Cannon, the sympathetic nervous system provides the metabolic
resources required for fight or flight behaviors. The
sympathetic nervous system enhances mobilization by
increasing cardiac output and decreasing the metabolic
demands of the digestive tract by actively inhibiting gastric
motility. Third, as proposed by Darwin and Bernard, the
parasympathetic nervous system and specifically the vagus are
related to emotional state. Few researchers have
investigated the link between parasympathetic activity and
affective state. However, over the past decade my laboratory
has focused on this issue. We have documented that vagal
tone, a component of parasympathetic control, is related to
affect and affect regulation.9-11 We have presented
theoretical models explaining the importance of vagal
regulation in the development of appropriate social
behavior.12 In general, the parasympathetic nervous system
is associated with fostering growth and restoration.13,14
Moreover, knowledge of the polyvagal system allow an
appreciation of the importance of the brainstem origin of the
specific vagal fibers in the determination of affective and
behavioral response strategies.12,15

Researchers and clinicians have had difficulties in the
organization or categorization of intensive affective states
that appear to have totally different etiologies or
behavioral expressions. For example, intense feelings of
terror might result in a total immobilization or freezing.
In contrast, intense feelings of anger or anxiety might be
associated with massive mobilization activity. This problem
exists, in part, because of a bias toward explanations of
affective states defined in terms of either overt behaviors
such as facial expressions (i.e., following Darwin) or
sympathetic activity (i.e., following Cannon). The emphasis
on sympathetic activity is based upon three historical
factors. First, theories regarding emotions have minimized
or totally neglected the parasympathetic nervous system.
Second, Cannon's focus on the sympathetic efferents and
mobilization responses associated with fight and flight as
the sole domain of autonomic reactivity during emotional
states has not been challenged. Third, the data base of
autonomic correlates of affect, collected to identify
autonomic "signatures" of specific affective states, is
dominated by measures assumed to be related to sympathetic
function.4-7

. . . . . . . . . .


THE SYMPATHETIC NERVOUS SYSTEM:
ADAPTIVE MOBILIZATION SYSTEM FOR FIGHT OR FLIGHT BEHAVIORS.

The sympathetic nervous system is primarily a system of
mobilization. It prepares the body for emergency by
increasing cardiac output, stimulating sweat glands to
protect and lubricate the skin, and by inhibiting the
metabolically costly gastrointestinal tract. The evolution
of the sympathetic nervous system follows the segmentation of
the spinal cord, with cell bodies of the preganglionic
sympathetic motor neurons located in the lateral horn of the
spinal cord. The sympathetic nervous system has long been
associated with emotion. The label "sympathetic" reflects
the historical identity of this system as a nervous system
"with feelings" and contrasts it with the parasympathetic
nervous system, a label that reflects a nervous system that
"guards against feelings."


THE VENTRAL VAGAL COMPLEX: THE MAMMALIAN SIGNALLING SYSTEM FOR MOTION, EMOTION, AND COMMUNICATION

The primary efferent fibers of the Ventral Vagal Complex
(VVC) originate in the nucleus ambiguus. The primary
afferent fibers of the VVC terminate in the source nuclei of
the facial and trigeminal nerves. The VVC has the primary
control of supradiaphragmatic visceral organs including the
larynx, pharynx, bronchi, esophagus, and heart. Motor
pathways from the VVC to visceromotor organs (e.g., heart and
bronchi) and somatomotor structures (e.g., larynx, pharynx,
esophagus) are myelinated to provide tight control and speed
in responding. In mammals, the visceromotor fibers to the
heart express high levels of tonic control and are capable of
rapid shifts in cardioinhibitory tone to provide dynamic
changes in metabolic output to match environmental
challenges. This rapid regulation characterizes the
qualities of the mammalian vagal brake that enable rapid
engagement and disengagement in the environment without
mobilizing the sympathetics.
A major characteristic of the VVC is the fact that the
neural fibers regulating somatomotor structures are derived
from the branchial or primitive gill arches that evolved to
form cranial nerves V, VII, IX, X, and XI. Somatomotor
fibers originating in these cranial nerves control the
branchiomeric muscles including facial muscles, muscles of
mastication, neck muscles, larynx, pharynx, esophagus, and
middle ear muscles. Visceromotor efferent fibers control
salivary and lacrimal glands, as well as the heart and
bronchi. The primary afferents to the VVC come from facial
and oral afferents traveling through the facial and
trigeminal nerves and the visceral afferents terminating in
the nucleus tractus solitarius (NTS). The VVC is involved in
the control and coordination of sucking, swallowing, and
vocalizing with breathing.

. . . . . . . . . .


VOODOO OR VAGUS DEATH?: THE TEST OF THE POLYVAGAL THEORY

The Polyvagal Theory of Emotion provides a theoretical
framework to interpret the phenomenon of Voodoo or fright
death described by Cannon32 and Richter.33 Cannon believed
that extreme emotional stress, regardless of the specific
behavioral manifestation, could be explained in terms of
degree of sympathetic-adrenal excitation. In 1942 Cannon
described a phenomenon known as Voodoo death. 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 Voodoo death would be the
consequence of the state of shock produced by the continuous
outpouring of epinephrine via excitation of the sympathetic
nervous system. According to the Cannon model, the victim
would be expected to breathe very rapidly and have a rapid
pulse. The heart would beat fast and gradually lead to a
state of constant contraction and, ultimately, to death in
systole. Since his speculations were not empirically based
he offered the following challenge to test his model of
Voodoo death:
"If in the future, however, any observer has opportunity
to see an instance of "voodoo death," it is to be hoped
that he will conduct the simpler tests before the
victim's last gasp."

Curt Richter responded to Cannon's challenge with an
animal model. Rats were pre-stressed, placed in a closed
turbulent water tank, and the latency to drowning was
recorded. Most domestic laboratory rats lasted for several
hours, while unexpectedly all of the wild rats died within 15
minutes. In fact, several wild rats dove to the bottom and,
without coming to the surface, died. To test Cannon's
hypothesis, that stress-induced sudden death was sympathetic,
Richter monitored heart rate and determined whether the heart
was in systole or diastole after death. He assumed, based
upon Cannon's speculations, that tachycardia would precede
death and that at death the heart would be in a state of
systole, reflecting the potent effects of sympathetic
excitation on the pacemaker and the myocardium. However,
Richter's data contradicted the Cannon model. Heart rate
slowed prior to death and at death the heart was engorged
with blood reflecting a state of diastole. Richter
interpreted the data as demonstrating that the rats died a
"vagus" death, the result of overstimulation of the
parasympathetic system, rather than of the sympathico-adrenal
system. However, Richter provided no physiological
explanation, except the speculation that the lethal vagal
effect was related to a psychological state of
"hopelessness."

The immediate and reliable death of the wild rats in
Richter's experiment may represent a more global
immobilization strategy. Sudden prolonged immobility or
feigned death is an adaptive response exhibited by many
mammalian species. Hofer34 demonstrated that several rodent
species when threatened exhibited a prolonged immobility that
was accompanied by very low heart rate. For some of the
rodents, heart rate during immobility was less than 50% of
the basal rate. During the prolonged immobility respiration
become so shallow that it was difficult to observe, although
the rate greatly accelerated. Although physiologically
similar, Hofer distinguished between prolonged immobility and
feigned death. The onset of feigned death occurred suddenly
with an apparent motor collapse during active struggling.
Similar to Richter, Hofer interpreted this fear-induced
slowing of heart rate as a vagal phenomenon. In support of
this interpretation, he noted that of the four species that
exhibited prolonged immobility 71% of the subjects had
cardiac arrhythmias of vagal origin; in contrast, in the two
species that did not exhibit immobility behaviors, only 17%
exhibited cardiac arrhythmias of vagal origin.

The Polyvagal Theory of Emotion places Richter's and
Hofer's observations in perspective. Following the
Jacksonian principle of dissolution, the rodents would
exhibit the following sequence of response strategies: 1)
removal of VVC tone, 2) increase in sympathetic tone, and 3)
a surge in DVC tone. It appears that the more docile
domestic rats in Richter's experiment progressed from a
removal of VVC tone, to an increase in sympathetic tone, and
then died via exhaustion. However, the profile of the wild
rats was different. Being totally unaccustomed to
enclosures, handling, and also having their vibrissae cut, a
mobilization strategy driven by increased sympathetic tone
was not functional. Instead, these rats reverted to their
most primitive system to conserve metabolic resources via
DVC. This strategy promoted an immobilization response
characterized by reduced motor activity, apnea, and
bradycardia. Unfortunately, this mode of responding,
although adaptive for reptiles, is lethal for mammals.
Similarly, the onset of feigned death, as described by Hofer,
illustrates the sudden and rapid transition from an
unsuccessful strategy of struggling requiring massive
sympathetic activation to the metabolically conservative
immobilized state mimicking death associated with the DVC.

These data suggest that the vagus contributes to severe
emotion states and may be related to emotional states of
"immobilization" such as extreme terror. The application
of the polyvagal approach enables the dissection of vagal
processes into three strategic programs: 1) when tone of the
VVC is high there is an ability to communicate via facial
expressions, vocalizations, and gestures; 2) when tone of the
VVC is low the sympathetic nervous system is unopposed and
easily expressed to support mobilization such as fight or
flight behaviors; and 3) when tone from DVC is high there is
immobilization and potentially life threatening bradycardia,
apnea, and cardiac arrhythmias.


CONCLUSION

Three important scientific propositions provide the
basis for building this theory. First, Darwin provided the
concept of evolution and the processes that contribute to
phylogenetic variation. Second, John Hughlings Jackson
provided the concept of dissolution as a viable explanation
for diseases of brain function. And, third, Paul MacLean35
provided the concept that the human brain retains structures
associated with phylogenetically more primitive organisms.

The Polyvagal Theory of Emotion focuses on the
evolution of the neural and neurochemical regulation of
structures involved in the expression and experience of
emotion as a theme to organize emotional experience and to
understand the role of emotion in social behavior. Over 100
years ago John Hughlings Jackson, intrigued with Darwin's
model of evolution, elaborated on how evolution in reverse,
termed "dissolution", might be related to disease. According
to Jackson, higher nervous system structures inhibit or
control lower structures or systems and "thus, when the
higher are suddenly rendered functionless, the lower rise in
activity." The Polyvagal Theory of Emotion follows this
Jacksonian principle.

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