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Arousal Theory and Stress Responses visceral homeostasis. Stress, simply defined, is the pro-
duct of demands on the nervous system that result in a
For more than a century, researchers have measured
deviation from homeostasis. In general, the domains of
autonomic variables (e.g., heart rate and palmar sweat
homeostasis, which have been monitored, have focused
gland activity) as indicators of emotional state related
on the visceral systems involved in cardiovascular,
to perceived stress (e.g., fear, mental effort, workload,
digestive, reproductive, and immune functions. Adap-
and anxiety). Historically, arousal theories provided
tive and successful coping to stress results in minimiz-
scientists who studied brain–behavior relations with a
ing the magnitude and duration of this deviation. To
model that assumed that activation of peripheral
survive, mammals must determine friend from foe,
physiological measures regulated by the sympathetic when an environment is safe, and communicate with
branch of the autonomic nervous system provided
their social unit. These survival-related behaviors limit
‘sensitive’ indicators of brain ‘arousal’ or ‘activation.’
the extent to which a mammal can be physically
This view was based on a rudimentary understanding
approached, whether vocalizations will be understood,
of the autonomic nervous system in which changes in
and whether coalitions can be established. Moreover,
easily measured peripheral organs (e.g., sweat glands
these behavioral strategies, which are used to navigate
and heart) were assumed to be accurate indicators
through the ‘stress of life,’ form the bedrock on which
of how the brain was processing emotional stimuli.
social behaviors and higher cognitive processes can
Usually, the emotional states were associated with be developed and expressed. Thus, learning and other
fight-or-flight behaviors and the sympathetic–adrenal
expansive mental processes must be structured, mani-
system (e.g., increases in heart rate, sweat gland activ-
pulated, and studied within the context of how the
ity, and circulating catecholamines) initially described
environment fosters or ameliorates stress-related physio-
by Cannon as well as the increased activity of the
logical states.
hypothalamic–pituitary–adrenal (HPA) axis with an
Table 1 illustrates the phylogenetic differences in
emphasis on cortisol as a dependent variable in stress
the structures that regulate the heart in vertebrates.
research as initially described by Selye.
The heart is selected because the regulation of the heart
Measures due, in part, to their availability and their determines the availability of the metabolic resources
neuroanatomical association with the target organs
required for mobilization as well as for growth and
of the sympathetic nervous system (i.e., sweat and heart
restoration. For example, cardiac output must be regu-
rate) and with secretions from the adrenal medulla
lated to remain calm in safe environments, to mobilize
(i.e., epinephrine and norepinephrine) and the adrenal
for fight-or-flight behaviors, or to immobilize for death
cortex (i.e., cortisol) have become the primary physio-
feigning or avoidance behaviors. To regulate cardiac
logical variables used to assess stress. An acceptance
output, several efferent structures have evolved. These
of a unitary arousal system created a research environ-
structures represent two global and often opposing sys-
ment that neglected several important factors, includ- tems: (1) a sympathetic–catecholamine system includ-
ing an understanding of the brain structures that
ing catecholamine-secreting chromaffin tissue and
regulate autonomic function; how these structures
spinal sympathetic nerves and (2) a vagal system (a
evolved from the most primitive vertebrates to mam-
component of the parasympathetic nervous system)
mals; how the autonomic nervous system interacts with
the immune system, the HPA axis, and the neuropep-
tides, oxytocin, and vasopressin; and the co-evolution Table 1 Phylogenetic shifts in vertebrate cardiac control
of stress and coping strategies with the increasing com-
Group CHM DVC SNS AD/m VVC
plexity of the autonomic nervous system. Missing from
the dialog on stress is the role of the parasympathetic Jawless fish X þ þ
(X )
nervous system and especially the vagus with its bi- Cartilaginous fish Xþ X
directional portal between the brain and specific Bony fish Xþ X Xþ
Amphibians Xþ X Xþ
visceral organs.
Reptiles Xþ X Xþ Xþ
Mammals Xþ X Xþ Xþ X
The Mammalian Nervous System Is CHM, chromaffin tissue; DVC, dorsal vagal complex with vagal
a Product of Evolution efferent pathways originating in the dorsal motor nucleus of the
vagus and vagal afferents terminating in the nucleus tractus soli-
Embedded in the mammalian nervous system are tarius; SNS, spinal sympathetic nervous system; AD/m, adrenal
neuroanatomical structures related to the expression medulla; VVC, ventral vagal complex with efferent pathways ori-
ginating in the nucleus ambiguus that regulate visceral structures
and experience of stress. Via evolutionary processes, (heart, bronchi, and thymus) and striated muscles via special vis-
the mammalian nervous system has emerged with spe- ceral efferents and afferents via the tractus solitarius, trigeminal, and
cific features that react to the challenge to maintain facial nerve.
Stress and Parasympathetic Control 465
with branches originating in the medullary source facial gestures and vocalizations associated with social
nuclei (i.e., dorsal motor nucleus of the vagus and communication. This phylogenetic course results in
nucleus ambiguus). greater central nervous system regulation of behavior,
Unlike other vertebrates with a cardioinhibitory especially that needed to engage and disengage with
vagus, the mammalian vagus contains two branches. environmental challenges.
One branch originates in the dorsal motor nucleus of
the vagus and provides the primary neural regulation
of subdiaphragmatic organs such as the digestive Polyvagal Theory: Three Phylogenetic
tract. However, at the level of the heart and unlike
Systems Related to Stress Reactivity
more primitive vertebrates, the efferent vagal path-
ways that originate in the dorsal motor nucleus of the The polyvagal theory emphasizes the phylogenetic ori-
vagus do not play a major role in the normal dynamic gins of brain structures that regulate social and defen-
regulation of cardiac output. Rather, during embryo- sive behaviors. The polyvagal theory proposes that
logical development in mammals, cells from the the evolution of the mammalian autonomic nervous
dorsal motor nucleus of the vagus migrate ventrally system provides the neurophysiological substrates for
and laterally to the nucleus ambiguus. There, they emotional experiences, affective processes, and stress
form the cell bodies for the visceromotor myelinated responses. The theory proposes that physiological state
axons that provide potent inhibition of the sinoatrial limits the range of adaptive behaviors and psychologi-
node, the pacemaker for the heart. cal experiences. In this context, the evolution of the
Three principles can be extracted by investigating nervous system determines the range of emotional
the phylogeny of the regulation of the vertebrate expression, the quality of communication, and the
heart. First, there is a phylogenetic shift in the regula- ability to regulate bodily and behavioral state includ-
tion of the heart from endocrine communication to ing the expression and recovery of stress-related
unmyelinated nerves and, finally, myelinated nerves. responses. Relevant to adaptive stress responses, the
Second, there is a development of opposing neural theory makes the following assumptions:
mechanisms of excitation and inhibition to provide
1. Evolution has modified the structures of the auto-
rapid regulation of graded metabolic output. Third,
nomic nervous system.
with increased cortical development, the cortex exhi-
2. The mammalian autonomic nervous system retains
bits greater control over the brain stem via direct
vestiges of phylogenetically older autonomic ner-
(e.g., corticobulbar) and indirect (e.g., corticoreticu-
vous systems.
lar) neural pathways originating in motor cortex and
3. Emotional regulation and social behavior are
terminating in the source nuclei of the myeli-
functional derivatives of structural changes in the
nated motor nerves emerging from the brain stem
autonomic nervous system due to evolutionary
(e.g., specific neural pathways embedded within cra-
processes.
nial nerves V, VII, IX, X, and XI), controlling viscer-
4. In mammals, the autonomic nervous system re-
omotor structures (i.e., heart, bronchi, and thymus)
sponse strategy to challenge follows a phylogenetic
and somatomotor structures (muscles of the face and
hierarchy, starting with the newest structures and,
head) that results in a neural circuit that functions
when all else fails, reverting to the most primitive
to facilitate social behavior and to maintain calm
structural system.
behavioral states.
5. The phylogenentic stage of the autonomic nervous
These phylogenetic principles provide a basis for
system determines the behavioral, physiological,
investigating the parasympathetic contribution to
and affective features of stress reactivity.
stress reactions and recovery. In general, phylogenetic
development results in increased neural control of the The polyvagal theory emphasizes and documents the
heart via the myelinated mammalian vagal system, neurophysiological and neuroanatomical distinction
which can promote transitory mobilization and the between the two branches of the vagus (i.e., the tenth
expression of sympathetic tone without requiring cranial nerve) and proposes that each vagal branch
sympathetic or adrenal activation. With this new is associated with a different adaptive behavioral and
vagal system, transitory incursions into the environ- physiological response strategy to stressful events. The
ment or withdrawals from a potential predator can be theory describes three phylogenetic stages of the devel-
initiated without the severe biological cost of the opment of the mammalian autonomic nervous system
metabolic excitation associated with sympathetic– (Table 2). These stages reflect the emergence of three
adrenal activation. Paralleling this change in neural distinct subsystems, which are phylogenetically ordered
control of the heart is an enhanced neural control of and behaviorally linked to communication (e.g., facial
the face, larynx, and pharynx that enables complex expression, vocalization, and listening), mobilization
466 Stress and Parasympathetic Control
Table 2 Phylogenetic stages of the neural control of the heart proposed by the polyvagal theory
III Myelinated vagus (ventral vagal Social communication, self-soothing and calming, Nucleus ambiguus
complex) inhibit ‘arousal’
II Sympathetic–adrenal system Mobilization (active avoidance) Spinal cord
I Unmyelinated vagus (dorsal vagal Immobilization (death feigning, passive avoidance) Dorsal motor nucleus of the
complex) vagus
The studies conceptualize the afferent vagus as the dorsal vagal complex to these two neuropeptides
providing a signal alerting the central structures (the differential effects of central and systemic release
regulating immune function. A few studies have on visceral function and a potential level dependency)
described motor pathways via the vagus to the thy- results in a wider range of response options, including
mus. The link between the vagal function and the maximizing mobilization behaviors and the co-opting
immune system is not clear. However, it might be of the primitive vagal system associated with immobi-
plausible to speculate that the neural mediation of lization to support ‘antistress’ functions such as social
the myelinated vagus, via direct influence on thymus engagement and growth and restoration.
and direct inhibition of the sympathetic nervous sys-
tem, may trigger a physiological state that would
Phylogenetic Approach to
promote immune function. Likewise, withdrawal of
the Study of Stress
vagal tone to the heart, increased sympathetic tone,
and the release of cortisol have been associated with The phylogenetic orientation focuses our interest on
suppressed immune function. the parasympathetic neural structures and neurobeha-
vioral systems that we share with or have adapted
from our phylogenetic ancestry. First, the three
Oxytocin/Vasopressin
response systems proposed in the polyvagal theory
Because the peripheral influences of oxytocin and (i.e., cranial nerves to regulate the face, sympathetic–
vasopressin function through feedback, primarily via adrenal system to increase metabolic output, and an
afferent vagal pathways, the peripheral effects of these inhibitory vagal system to decrease metabolic output
peptides are less clear and may be level dependent or and promote freezing and defecation) are the pro-
differ as a function of acute versus chronic exposure. ducts of distinct neurophysiological systems. Second,
For example, it is possible that peripheral vasopressin, these distinct neurophysiological systems represent a
by stimulating vagal afferents, may trigger massive phylogenetically dependent hierarchy, with the use
vagal responses via the dorsal motor nucleus of the of cranial nerves to regulate facial expression emerg-
vagus. In support of this speculation, it is known that ing in mammals (well developed in primates); the
in humans, peripheral vasopressin, and not oxytocin, is sympathetic–adrenal system shared with other verte-
related to the nausea experienced during motion sick- brates including reptiles; and the inhibitory vagal sys-
ness. In addition, systemic vasopressin may induce a tem shared with more primitive vertebrates, including
baroreceptor-mediated bradycardia and a decrease in amphibians, bony fish, and cartilaginous fish. The
plasma concentration of norepinephrine. three systems represent different phylogenetic stages
Based on the polyvagal theory, the mammalian of neural development. This phylogenetic develop-
vagus, with myelinated motor fibers originating in ment starts with a primitive behavioral inhibition
the nucleus ambiguus, provides a system for volun- system, progresses to a fight-or-flight system, and, in
tary engagement with the environment, with special humans (and other primates), culminates in a complex
features associated with the prosocial behaviors of facial gesture and vocalization system. Thus, from
communication. Paralleling this evolutionary shift a phylogenetic perspective, the nervous system of
in the vagus is a mammalian modification of the vertebrates evolved to support a greater range of
hypothalamic regulation of the dorsal vagal complex behaviors and physiological states, including states
(i.e., source nucleus of the afferent and efferent path- that are often associated with stress.
ways of the unmyelinated vagus originating in the The physiological responses associated with stress
dorsal motor nucleus of the vagus and the nucleus of in mammals do not concisely fit into a single neuro-
the solitary tract) via both oxytocin and vasopressin. physiological system. Although cortisol has often been
The advent of specific receptors for oxytocin and labeled as the stress hormone, other systems clearly
vasopressin has increased the range of adaptive func- respond to stress. Moreover, there are situations of
tions involving the unmyelinated vagus. In mammals, severe stress in which cortisol is neither responsive
the dorsal motor nucleus of the vagus, the motor nor at a high level. By expanding the phylogenetic
component of the dorsal vagal complex, is sensi- model proposed in the polyvagal theory to emphasize
tive to oxytocin and insensitive to vasopressin. In the interactions between parasympathetic mechanisms
contrast, the sensory components of the vagus, the and the HPA axis, the hyporesponsive HPA can be
nucleus of the solitary tract and area postrema, are interpreted as reflecting a primitive passive avoidance
most sensitive to vasopressin. Although the nucleus system. Thus, several systems with target organs at
of the solitary tract has receptors for oxytocin, area the periphery contribute to the organism’s adaptation
postrema may not be directly influenced by oxytocin. to challenge and stress. These neurobiological systems
The differential sensitivity of specific components of are not solely stress systems. Rather, they are intimately
Stress and Parasympathetic Control 469
involved in the dynamic regulation of homeostasis, self-motion and nausea in man. Journal of Clinical Endocrinol-
growth and restoration, metabolism, and mobilization. ogy and Metabolism 71: 1269–1275.
Landgraf R, Mallkinson T, Horn T, et al. (1990) Release of vaso-
These systems form a complex set of mutually interact- pressin and oxytocin by paraventricular stimulation in rats.
ing neurophysiological pathways that communicate American Journal of Physiology 258: 155–159.
via nerves and neurally active chemicals (e.g., neuro- Langley JN (1921) The Autonomic Nervous System, vol. 1.
transmitters, neuropeptides, and hormones) to cope Cambridge: Heffer and Sons.
Michelini LC (1994) Vasopressin in the nucleus tractus solitarius:
with survival challenges.
A modulator of baroreceptor reflex control of heart rate.
See also: Autonomic Nervous System; Parasympathetic Brazilian Journal of Medical and Biological Research 27:
1017–1032.
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Stress Response: Neural and Feedback Regulation of the
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Further Reading Porges SW (1995) Orienting in a defensive world: Mammalian
modifications of our evolutionary heritage. A polyvagal theory.
Berlyne DE (1960) Conflict, Arousal, and Curiosity. New York: Psychophysiology 32: 301–318.
McGraw-Hill. Porges SW (1998) Love: An emergent property of the mamma-
Bueno LM, Gue MJ, Fargeas M, et al. (1989) Vagally mediated lian autonomic nervous system. Psychoneuroendocrinology
inhibition of acoustic stress-induced cortisol release by orally 23: 837–861.
administered kappa-opioid substances in dogs. Endocrinology Porges SW, Doussard-Roosevelt JA, Portales AL, and Greenspan SI
124: 1788–1793. (1996) Infant regulation of the vagal ‘brake’ predicts child
Bulloch K and Pomerantz W (1984) Autonomic nervous system behavior problems: A psychobiological model of social behav-
innervation of thymic-related lymphoid tissue in wildtype and ior. Developmental Psychobiology 29: 697–712.
nude mice. Journal of Comparative Neurology 228: 58–68. Schwaber JS (1986) Neuroanatomical substrates of cardiovas-
Cannon WB (1928) The mechanism of emotional disturbance cular and emotional–autonomic regulation. In: Magro W,
of bodily functions. New England Journal of Medicine 198: Osswald W, Reis D, and Vanhoutte P (eds.) Central and
877–884. Peripheral Mechanisms of Cardiovascular Regulation, pp.
Darrow CW (1943) Physiological and clinical tests of autonomic 353–384. New York: Plenum.
function and autonomic balance. Physiological Reviews 23: Selye H (1956) The Stress of Life. New York: McGraw-Hill.
1–36. Vanhoutte PM and Levy MN (1979) Cholinergic inhibition of
Darwin C (1872) The Expression of Emotions in Man and adrenergic neurotransmission in the cardiovascular system. In:
Animals. New York: Appleton. Brooks CMcC, Koizumi K, and Sato A (eds.) Integrative Func-
Gray JA (1971) The Psychology of Fear and Stress. New York: tions of the Autonomic Nervous System, pp. 159–176. Tokyo:
McGraw-Hill. University of Tokyo Press.
Hess WR (1954) Diencephalon, Autonomic and Extrapyramidal Watkins LR, Goehler LE, Relton JK, et al. (1995) Blockade of
Functions. New York: Grune & Stratton. interleukin-1 induced hyperthermia by subdiaphragmatic
Koch KL, Summy-Long J, Bingaman S, Sperry N, and Stern RM vagotomy: Evidence for vagal mediation of immune-brain com-
(1990) Vasopressin and oxytocin responses to illusory munication. Neuroscience Letters 183: 27–31.