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Ethological Causes and Consequences of the Stress
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James A. Carr
Texas Tech University
Cliff H. Summers
University of South Dakota
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Greenberg, Neil; Carr, James A.; and Summers, Cliff H., "Ethological Causes and Consequences of the Stress Response" (2002).
Ecology and Evolutionary Biology Publications and Other Works.
Integrative & Comparative Biology, Volume 42, Issue 3 pp. 508-516 (2002)
Ethological Causes and Consequences of
the Stress Response
Neil Greenberg, James A. Carr, Cliff H. Summers
Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville
Department of Biological Sciences, Texas Tech University, Lubbock
Department of Biology, University of South Dakota, Vermillion
Presented at the SICB Symposium, "Stress --Is it More Than a Disease? A Comparative Look at Stress and
2001 SICB Annual Meeting, Chicago Hilton and Towers, January 3-7, 2001
SYNOPSIS. Stress involves real or perceived changes within an organism or in
the environment that activate an organisms attempts to cope by means of
evolutionarily ancient neural and endocrine mechanisms. Responses to acute
stressors involve catecholamines released in varying proportion at different
sites in the sympathetic and central nervous systems. These responses may
interact with and be complemented by intrinsic rhythms and responses to
chronic or intermittent stressors involving the hypothalamic-pituitary-adrenal
axis. Varying patterns of responses to stressors are also affected by an animal=s
assessment of their prospects for successful coping. Subsequent central and
systemic consequences of the stress response include apparent changes in
affect, motivation, and cognition that can result in an altered relationship to
environmental and social stimuli. This review will summarize recent
developments in our understanding of the causes and consequences of stress.
Special problems that need to be explored involve the manner in which
ensembles of adaptive responses are assembled, how autonomic and
neurohormonal reflexes of the stress response come under the influence of
environmental stimuli, and how some specific aspects of the stress response
may be integrated into the life history of a species.
Stressors are real or perceived challenges to an organisms=s ability to meet its real or
perceived needs. In most vertebrates the responses that have evolved to cope with
such challenges are constrained by a threshold for detection of challenge, for attention
based on real or perceived relevance, and for capacity to respond at any particular
level once the challenge is detected. Depending on the intensity and timing of the
stressor, each of these can vary independently.
Stressors that challenge homeostasis, often regarded as the most urgent of needs, are
the best known. When an organism=s competence to maintain homeostasis within a
specific range is exceeded, responses are evoked that enable the organism to cope by
either removing the stressor or facilitating coexistence with it (Antelman and
Caggiula, 1990). While many stressors can evoke dramatic neural and endocrine
responses, a more modest or subclinical response may be exhibited in response to
milder stimuli. These responses may build on or extend homeostatic mechanisms or
they may be more or less tightly linked to homeostatic responses in a hierarchical
manner creating a functional continuum. For example, such a hierarchical system was
described for thermoregulation in mammals by Satinoff (1978) in which more
recently evolved regulatory mechanisms are invoked when more conservative ones
are unable to restore balance. This continuum is expressed in numerous physiological
responses, often measured as an inverted U (Sapolsky, 1997). Although the
inverted-U physiology of stress hormones such as corticosteroids presents the
conundrum of opposing actions at different dosages, progress over the last twenty
years has elucidated some of the physiology involved. For example, both membrane-
bound (Orchinik et al., 1991) and two types of intracellular receptors (Ruel et al.,
1987) help explain how acute glucocorticoid responses may differ from long-term
responses. Membrane receptors acting by means of G proteins stimulate more rapid
cellular response than classic receptors that act as transcription factors: type I (
mineralocorticoid or MR) and type II (glucocorticoid or GR) receptors. Based on the
differences in affinity and capacity, type II receptors only become bound during
circadian or stress-evoked peaks in plasma glucocorticoids. We can now envision how
a gradual succession from low levels of corticosteroids binding to type I receptors
turns the corner on the U as progressively higher titers bind more effectively to
type II receptors (Ruel et al., 1987). Basal levels of glucocorticoid (involving type I
receptors) are proactively permissive for defense mechanisms at tonic and
circadian levels, while reactively suppressive actions are invoked at higher, stress-
induced levels of glucocorticoid (involving type II receptors) and help protect the
organism from a damaging overcompensation that elevated levels of hormone
might induce (Meijer et al 2000). Many if not all of the hormones involved in stress
responses possess, in addition to their direct effects, pleiotropic or collateral
consequences that may or may not reinforce the direct or primary effect. It is likely
that many of these other effects can provide the basis of mechanisms that might serve
other, unrelated adaptive needs.
At one level, coping with challenge is what life is all about. Stress is inevitable, and as
Hans Selye emphasized, a necessary part of life (1976). There is, however, a problem
defining stress as coping with a challenge. The implication that stress is something to
be avoided is a legacy from the clinical perspective dominated by the mandate to
remediate dysfunction, including the stress-evoked diseases of adaptation. Selye
(1976) himself tried to correct this one-sided over-generalization by distinguishing
eustress from distress, but the legacy lives on. The perception that stress
responses, by reallocating resources from growth to coping with a challenge, are not
good, suggests that stress facilitated coping is forced upon organisms by occasional
unfortunate circumstances. However, organisms exist in continually changing
environments and their very existence can be construed as an expression of that
coping. The mechanisms that have evolved to cope with change are organized within
a nested hierarchy. The most conservative functions deal with homeostasis, the most
ancient and urgent of needs. But homeostasis is not an organisms only need, and
Bruce McEwens succinct definition is an excellent beginning to a fuller appreciation
of that fact: Stress may be defined as a threat, real or implied, to the psychological
or physiological integrity of an individual (McEwen,1999a:1).
Survival in the changing external environment depends on the flexible stability of an
organisms internal environment, which is itself always in flux. The flexibility is
attributable to the fact that physiological functions can proceed effectively within a
range of more or less tolerance for deviation from their respective setpoints. The
necessity for organisms to attain some measure of independence from the vagaries of
the external environment was described by Claude Bernard in the 19th century.
Bernard recognized that the stability of the milieu interieur depended on ensembles of
compensating mechanisms (Bernard, 1878). Fifty years later, Walter Cannon (1929)
introduced the term homeostasis to describe the dynamic, interactive nature of
these mechanisms in maintaining the stability of the internal environment. He further
identified the autonomic nervous system (ANS) as an orchestrator of responses when
an organism is suddenly challenged. The famous fight or flight response is one
such ensemble of responses. Within a decade, Hans Selye shifted attention from the
ANS to the adrenal glands by identifying a General Adaptation Syndrome (GAS) in
which the initial sympatho-adrenomedullary system (SAMS) response to an
emergency was augmented by an hypothalamic-pituitary-adrenal (HPA) response as
the body mobilized resources to cope with a sustained stressor (Selye, 1936; 1937).
This was of particular interest to medical science as the coping mechanisms of the
stress response became seen, over time, as potentially deadly diseases of
adaptation. Here, organs fail as their resources become reallocated to deal with a
continuing stressor, possibly leading to exhaustion and death (Selye 1946). By the
early 1970's, stress was no longer viewed mainly as a threat to survival, and Seymour
Levine (1971) was able to state that the normal expression of adaptive behavior
depends upon some optimal level of stress.
Stressors may be acute, sequential, episodic, chronically intermittent, sustained, or
anticipated (Sapolsky et al. 2000). Alternative strategies may be evoked by the
organisms perception or experience of their effectiveness in coping. The clinical
view of the stress response was that it was largely nonspecific, but it has become clear
that many stressors evoke specific combinations of physiological and behavioral
responses depending in part on their respective potentials for effective coping in a
given context. Stressors perceived as uncontrollable will evoke different ensembles of
responses than those believed to be controllable (see for example, Cabib and Puglisi-
Allegra 1996, Huether 1996). Stressors also can be additive, creating the appearance
of a trivial stressor having a disproportionate effect. The endocrine environment may
also be a significant variable for the action of stress hormones.
The present understanding of stress and behavior has been nicely summarized in
several reviews. In the early 1970's, Mason (1971) called attention to the potency of
psychological stimuli in the stress response. A large literature has emerged since
Christian=s original insights in the 1950's and 1960's that at high densities, mammals
manifest enlarged adrenals indicative of increased stress and also showed increased
mortality and reduced reproduction. These psychoendocrine effects reinforced
perceptions of stress in terms of Selyes (1946, 1976) General Adaptation
Syndrome (see Christian & Davis 1964, Christian 1980). Lee and McDonald (1985)
reviewed this and related literature and appealed for additional research and more
direct evidence for the effects of stress in natural populations. Axelrod and Reisine
(1984) summarized the multiple regulatory mechanisms and interactions of stress
hormones, identifying corticotropin (ACTH) as a principal nexus; Goldstein (1987)
provided a helpful collation of stress-induced actions of the sympathetic nervous
system; Johnson and colleagues (1992) reviewed mechanisms with an emphasis on
the dynamic nature of endocrine and behavioral mechanisms. Neural pathways were
recently reviewed by Van de Kar and Blair (1999) who pointed that prolactin,
oxytocin, and renin have been neglected as stress-sensitive endocrine systems because
they are coordinated by slightly different neural pathways. Saavedra (1999) recently
reviewed evidence of a widespread role for angiotensin in modulating stress and
cortocotrophic releasing hormone (CRH), which has significant stress response
coordinating functions aside from its triggering a corticosterone response (e.g.
Leshner, 1978; Koob, 1991)
A review of the diversity of glucocorticoid actions in the stress response by Sapolsky,
Romero, and Munck (2000) provides a valuable synthesis of the seeming
contradictory functions of glucocorticoids. The permissive actions of glucocorticoids
that are based on tonic levels associated with homeostasis are seen to be distinct from
the suppressive and stimulatory actions that result from stress-induced elevation of
circulating levels. Sapolsky et al. also express an appreciation for the ethological
perspective in developing what they have termed the preparative functions of
glucocorticoids, and caution laboratory researchers to be sensitive to the organism
perspective of what constitutes a stressor.
TABLE 1 SEE BELOW
Understanding the causes and consequences of stress in nonhumans has taken on an
urgency of its own as a result of a growing concern for animal welfare as well as a
search for more robust and relevant animal models. This interest in the role of stress in
life history has proven a valuable counterbalance to well-intentioned perceptions by
scientists and citizens who too frequently view stress in a stereotypical way as
necessarily deleterious. Ignorance of the real needs of the animals (echoing
Sapolskys appeal for appreciation for the unique needs of the subject) is most
obvious when well cared for animals fail to thrive or reproduce. Further, freedom
from stress attainable in the laboratory is as serious as inadvertently introduced stress
in compromising the external validity of findings. Attempts to bring perspective to
this issue are proliferating (for example, Broom and Johnson 1994, SCAW 2000)
some of which target nonmammalian vertebrates (e.g., Schaeffer et al., 1992;
Warwick et al., 1995, Greenberg 1994). Other efforts try to deal with issues of
definition and clarity. For example, Moberg (1999) has attempted to identify the
boundary between stress and distress at a point where the cost of coping impairs
functions critical to well-being.
COMPLICATIONS IN DEFINING CAUSE AND CONSEQUENCE:
LESSONS FROM ETHOLOGY
Stress researchers and physiological ethologists often emphasize that stress is evoked
by a perceived challenge to the status quo as well as a physical experience. Since we
now more fully understand that not all change is bad and not all stressors are
deleterious there is renewed attention to the relationships between stress and emotion.
The now distant dispute between proponents of the James-Lange theory of emotion
(that the experience of an emotion was secondary to the physiological events) and WB
Cannon=s view (that physiological changes were subsequent to an emotional
experiences) persists because, as Leshner (1978) points out, both positions have some
validity. Leshner=s review of the problem concluded that at least some hormones may
have a general effect on arousal which then feeds back to evoke enhanced
catecholamine and glucocorticoid responses. For example, maternal care-giving is
positively correlated with cortisol levels in humans (Fleming et al., 1987) but may
also be accounted for by enhanced attention to stimuli. Therefore, endocrine and
neuroendocrine events proceed in an interdependent manner to regulate multiple,
variable stress responses, each unique, but influenced by previous events (Summers,
2001). Taking this a step further, arousal can evoke an emotion which will be tested
against experience and cognition and then by means of a positive feedback loop can
lead to progressively more focused expression.
The hormonal mechanisms responsible for behavioral changes during mild stress are
rarely obvious, as many stress hormones have structurally-related and biologically
active counterparts with multiple receptors and receptor subtypes. For example,
corticotrophin releasing hormone (CRH) and the structurally related peptide urocortin
act on multiple receptor types to rapidly inhibit feeding. It has is only recently that
researchers have been able to identify the respective contribution of each peptide and
receptor type to stress-induced alterations in feeding (Cone, 2000). In some respects
the selective facilitation or inhibition of normal behavioral patterns evoked by mild
stress is analogous to subclinical symptoms of a disease.
Indeed, the expression of many behavioral patterns are stress-sensitive in that their
expression may be secondary to neurotransmitter or hormone-induced increases in
non-specific arousal and selective attention (see Mason 1968, Nelson, 2000). The
actions of stress hormones may also be constrained by the activity of other hormones
and by environmental circumstances. For example, the rapid behavioral (perch-
hopping) response to corticosterone in white-crowned sparrows is influenced by
photoperiod. During a long-day (breeding) photoperiod, but not short-day (winter)
photoperiod, corticosterone will increase activity (Breuner & Wingfield, 2000).
Testosterone is subject to seasonal variation and social dynamics in many species, and
its activity appears to facilitate or enhance responsiveness to stressors both directly
and indirectly. Reduced androgen, such as might be seen in subordinate males,
appears to ameliorate the normal stress-evoking effects of certain stimuli (e.g.,
Greenberg et al., 1984 in the lizard, Anolis). As a female counterpart to the fight-or-
flight responses of males, Taylor (et al. 2000) proposed a tend-and-befriend
response to stress in females where (for example) the effects of oxytocin are
moderated by the presence of estrogen and endogenous opioids. In this response,
female mammals under stress will manifest enhances caregiving and attachment
There is a great diversity of adaptive behavioral patterns that appear to have built on
specific elements of the stress axes (Table 1). No tabulation can be exhaustive but the
one we have assembled underscores the diversity of effects at different levels of
specificity. It is a continuing challenge to distinguish primary from secondary
behaviors: Are the effects of stress on behavior a consequence of hormones acting
directly on specific neural structures mediating actions? Might they be collateral
actions on secondary targets? Or might the manifest behavioral pattern be secondary
to enhanced attention, arousal, cognitive activity, or even sensitivity of sensory
receptors? Collateral effects are particularly rich sources of alternative behavioral
patterns. For example, releasing factors such as corticotropic releasing hormone
(CRH) (Koob et al., 1993) and pituitary hormones frequently have multiple target
tissues. CRH has many behavioral effects mediated through CNS receptors in addition
to its central role in simulating pituitary ACTH secretion and indeed, CRH may
arguably be the principle coordinating regulator of central stress responsiveness,
influencing central serotonergic (Price et al., 1998; Lowry et al., 2000) and
catecholaminergic activities (Dunn and Berridge, 1987; Curtis et al., 1997). CRH is
also believed to have direct effects on behavioral patterns such as locomotion (Lowry
and Moore, 1991), startle responses (Pelton et al., 1997), and learning (Radulovic et
al., 1999; Wang et al., 2000). Significant direct central (extra-adrenal) effects of
ACTH are also well known (Leshner, 1971). Thus, simply administering exogenous
corticosterone as a way of determining its effects on behavior is complicated by the
fact that while it may act directly on a target tissue, it may also be acting indirectly by
means of feedback suppression of CRF or ACTH (Brain, 1972). In addition, as
mentioned above, the same hormone can have opposite effects when present at
different absolute amounts or temporal regimens. Opposing actions of adrenal axis
hormones and central stress peptides stem from an inverted-U dose physiology that is
a part of a framework of optimal stress response mechanisms (Sapolsky, 1997). Also,
different receptor types have alternative effects when stimulated by the same hormone
and different stressors can evoke different patterns of endocrine response. For
example, the stimuli involved in an aggressive exchange between two males
competing for social dominance will elicit comparable corticosteroid release in both
animals, but following such an encounter, the winner will also experience a
testosterone surge (e.g., Coe et al., 1982 for squirrel monkeys; Greenberg and Crews,
1990 for lizards). Further, if they continue in a long-term dominant-subordinate
relationship, the subsequent responsiveness to stress-evoking stimuli will be different
in the two animals.
THE EVOLUTION OF STRESS AND BEHAVIORAL COPING
Autonomic responses are among the richest sources of adaptive behavioral patterns.
Tightly yoked somatic and autonomic effects involving sympathetic activation and
occasionally, parasympathetic rebound, have been identified in situations that involve
frustration or conflict (Morris, 1956). It is reasonable to imagine that in sophisticated
decision-making organisms such as humans, there is competence to reflect, at least in
part, on processes that guide the selection of alternative ensembles of adaptive
pathways such as Afight or flight@ (Cannon, 1929), Aflee or freeze@ (Rand, 1964, for a
lizard), or active versus passive coping (Bandler et al., 2000). Interestingly, in
humans, there is evidence that at a critical level of acute stress, cognitive mechanisms
of the prefrontal cortex are suppressed and more rapid, conservative responses are
invoked (Arnsten 1997, 2000); chronic stress may also work through several other
long-term mechanisms to impair cognitive function (McEwen and Sapolsky, 1995).
AIn animals, almost invariably, a change in behavior is the crucial factor initiating
evolutionary innovation,@ Mayr tells us (1988:408). Also, selection pressures can be
altered by behavior that modifies the environment in which an animal must survive
and thrive (see Deacon=s 1997 review of Mark Baldwin). The role of stress in guiding
the evolution of coping mechanisms cannot be overestimated. It is likely that stress
responses are a first means of dealing with altered selection pressures caused by the
inevitable environmental changes organisms are subjected to. A further link is likely
between the stress-evoked changes in behavior when confronted with novel selection
pressures and the ultimate changes identifiable as evolutionary innovations which
seem more abundant in rapidly changing environments (Jablonski & Bottjer 1990,
Hoffmann & Hercus 2000). As brains change in response to specific selection
pressures, the larger contexts in which resolutions to act are made involve the systems
that subsume motivation, affect, and cognition. More conservative coping strategies
are reasonably mediated by more ancient parts of the brain (Paradiso et al., 1999).
Candidate mechanisms for the developmental influence of stress on brain and
behavior, including the effects of corticosteroids impairing the growth of specific
neural areas (see Thomas and Devenport 1988) and the integrity of the highly plastic
hippocampus, are now well established (for example, Fuchs & Flugge 1998 and
McEwen 1999b for recent reviews). Indeed, a major influence of stress on the
evolution of brain structures that selectively respond to stressful stimuli or are
activated by stress hormones was suggested by Huether (1996) in his
conceptualization of a Acentral adaptation syndrome.
CONCLUSIONS AND NEED FOR FUTURE STUDY
One of the more striking effects of confronting such a diverse assortment of stress-
sensitive phenomena is vivid sense of the versatility and flexibility of the system. The
stress response is orchestrated by a deeply embedded, highly conservative sense of
biological priorities and an impressive economy. By assembling and reassembling a
relatively small numbere of possible responses into a diversity of new combinations,
natural selection deals with an almost infinite array of possible challenges. Clearly,
physiological stress responses need not be manifest as conveniently conspicuous
behavioral patterns or pathologies to have adaptive significance. As David Goldstein
(1990) put it, they can be evoked whenever an organism experiences Aexpectations ---
whether genetically programmed, established by prior learning, or deduced from
circumstances[that] do not match the current or anticipated perceptions of the
internal or external environment (p. 243). In addition, the modulation of stress
responses by perceived control or helplessness (see Cabib and Puglisi_Allegra ,
and see Seligman , Seligman et al., ) allows us to envision how an
animals perception of the prospects for future remediation of a mismatch can
influence the expression of an appropriate compensating response (Bandler et al.,
Stress research is compelling not only as a fascinating puzzle that helps make sense of
many previously scattered observations, but is also compelling medically and socially.
Medical researchers (and then the rest of us) began with Selye=s insights about
diseases of adaptation, the clinical expressions of chronic stress. However, we have
learned much about developmental neuroplasticity. Early nurturing experiences (Liu
et al 1997), prenatal stress syndrome, and brief but intense episodes of stress (such as
childhood abuse), have all been implicated in causing enduring neurological changes.
In this regard it is significant that a significant number of violent criminals have
atypical autonomic responses (Raine et al., 2000), often associated with early
experiences of intense stress. The principal function of stress is protective and many
elements of the stress response can also be viewed as a kind of cure chemotherapy
without drugs, in Antelman and Caggiulas terms-- but sometimes the cure can be
worse than the disease. This was Walter Cannon=s insight when he wrote that the
development of pathological functions in a system is quite consistent with its usual
performance of normal functions.
The adaptive value of responsiveness to stressors in animals in nature may provide
invaluable information regarding the dynamics and flexibility of neuroendocrine
stress responses. Absolute levels of transmitters or hormones may not matter in the
production of significant and adaptive results. Relative elevation or inhibition
accruing from previous experience may adjust specific neural centers to produce
relevant output specifically related to the appropriate environmental context. The
neural mechanisms for transduction of relevant information are of necessity very
plastic, with many transmitter, neuromodulator and peripheral hormone systems
interacting. These systems influence behavioral and physiological stress responses,
but are also influenced by that output.
Our goal in this brief review has been more to be provoke than postulate. The
references selected from the vast literature of overlapping behavioral, neurological,
and endocrine reports applicable to stress were exemplary, not exhaustive. Many of
the findings about the reciprocity of behavioral patterns and stress physiology
underscores the fact that systems usually expressed as an ensemble are often cobbled
together by multiple selection pressures. A sense of this opens researchers to creative
hypotheses and the value of the comparative method. By training and disposition,
researchers apply Occam=s Razor to available evidence no matter how fragmentary,
but if the prevailing views of mechanisms cannot assimilate or accommodate new
data, new views must be sought.
The lesson beyond the obvious one of humility in the face of nature=s imagination, has
been one of openness to the myriad possibilities for the organization and
reorganization of the relatively small numbers of ways that hormones, brains, and
behavior can interact. We have often heard that research has become a more
collaborative affair. This is the only solution to the problem of the isolation that
attends explorations of great disciplinary depth. A continuing challenge must be to
enhance the reciprocal influences of the laboratory and the real world in which traits
of interest have evolved. This will require renewed efforts at mutual understanding for
researchers specializing in the unique questions and methodologies of each research
approach. Efforts must be taken to place the limited validity of highly controlled
laboratory studies at the service of less exact field research, and to present the insights
of observers in the real world to bench scientists. In a small way this resembles the
tension between ideologies of freedom and control that plague all would-be
collaborative social groups, but the richness of the reward justifies all possible efforts.
The symposium was made possible by funding from the NIMH (R13 MH62670), NSF
(IBN 0100532), the Center for Biomedical Research Excellence (CoBRE, P20
RR15567) at the University of South Dakota on Neural Mechanisms of Adaptive
Behavior, South Dakota EPSCoR, and the USD Office of Research.
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TABLE 1. REPRESENTATIVE BEHAVIORAL
RESPONSES TO STRESS
the original TABLE 1 is below; for an annotated and
(revised as appropriate) click here
Epi intensified but does not evoke affect
Stress narrows attention onto specific stimuli
GC (acute) enhances salience of stimuli
Stress impairs sustained attention
Stress impairs selective attention
McEwen et al., 1986
Stress modulates hippocampus and septum to
effect selective perception (attention)
CRH activates behavior and intensifies response
to stress independently of HPA axis
Koob et al., 1993
Excitatory or inhibitory effects of GCs on neurons
may depend on their state of activation
Joëls and de Kloot, 1992
AVP associated with "defensive" arousal,
attention, or vigilance
Carter and Altemus, 1997
CRH facilitates acoustic startle
Social defeat diminishes nocioception in mice
Miczek et al., 1982
Handling and species-specific stress-evoking
odors cause analgesia in rats
Fanselow and Sigmundi,
CRH-induced in familiar habitat
Sutton et al., 1982
CRH-inhibited in unfamiliar habitat
Britton et al 1982
CRH_induced walking and swimming (newt)
Lowry et al., 1996
Feeding and grooming correlated with subsequent
increase in GC
Shiraishi et al., 1984
GC/stress involved in seasonal population
dispersal in birds
Lee and McDonald, 1985;
Silverin, 1997; Wingfield
et al., , 1997
GC restores exploratory activity eliminated by
Veldhuis et al., 1982
CRH enhances effects of novelty
ACTH excitatory with novel stimulus and
inhibitory with prolonged stimulus
ACTH but not GC impairs habituation to an
acoustic stimulus and reduces exploration
Some elements enhanced, others impaired in
lizards; stress affects ameliorated in castrates
GC evokes rapid (nongenomic) locomotor
response in rats in novel but not familiar cage
Sandi et al., 1996
Hippocampal GC receptors mediate stress
responsiveness to novel habitats
Hiebert et al., 2000
Diurnal torpor in hummingbird
Epi facilitates acquisition
CRH facilitates acquisition of visual
ACTH facilitates and corticosterone impairs
Melanocortins facilitate habituation (toad)
Carpenter and Carr, 1996
Melanocortin enhance learned avoidance and
approach behavior was contrasted with
Bohus and de Wied, 1980
Attenuated acquisition and performance of
McEwen et al., 1986
Stress facilitates classical conditioning in males
but not females
Shors et al., 1992, 2000;
Wood & Shors, 1998
Stress-facilitated learning depends on stressor
intensity, duration and context
Shors and Servatius, 1997
Stress-induced rise in natural benzodiazepine
levels rise and apparently enhance the inhibitory
neurotransmitter GABA, preventing retention of
Levine, 1971; Izquierdo
and Medina, 1991
GC increases submissiveness
Leshner and Politch, 1979
Losers of territorial fights become subordinate in
the lab (lizard)
Greenberg et al., 1984
Endorphins block gonadotropin releasing factor
and CS impairs gonadal responsiveness to
CRF inhibits sexual behavior in female rats
Sirinathsinghji et al., 1983
ACTH can induce transient increase in
testosterone while sustained CS suppresses
Can be facilitated by presumed stress of
Antelman and Caggiula,
Prenatal stress syndrome: stressed pregnant rats
deliver feminized male pups
Ward & Weisz, 1980;
Greenberg and Wingfield,
Stereotypies: precipitated by stress
Broverman et al., 1974,
Cooper & Nicol, 1991,
1993, but see Mason 1991
ACTH-induced stretch-yawn syndrome and
MSH induces grooming behavior in rats
O'Donohue et al., 1981
Subordinate rats increase alcohol consumption
Blanchard et al., 1993
Addictions, neuroses and psychoses precipitated
Atress catalyzes hyperexcitability in fear-
mediating circuits leading to anxiety disorders
Rosen and Shulkin, 1998
ACTH, adrenocorticotrophic hormone; EPI, epinephrine; GC, glucocorticoid; MSH, melanocyte-