ArticlePDF AvailableLiterature Review

Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity


Abstract and Figures

Biological reactivity to psychological stressors comprises a complex, integrated, and highly conserved repertoire of central neural and peripheral neuroendocrine responses designed to prepare the organism for challenge or threat. Developmental experience plays a role, along with heritable, polygenic variation, in calibrating the response dynamics of these systems, with early adversity biasing their combined effects toward a profile of heightened or prolonged reactivity. Conventional views of such high reactivity suggest that it is an atavistic and pathogenic legacy of an evolutionary past in which threats to survival were more prevalent and severe. Recent evidence, however, indicates that (a) stress reactivity is not a unitary process, but rather incorporates counterregulatory circuits serving to modify or temper physiological arousal, and (b) the effects of high reactivity phenotypes on psychiatric and biomedical outcomes are bivalent, rather than univalent, in character, exerting both risk-augmenting and risk-protective effects in a context-dependent manner. These observations suggest that heightened stress reactivity may reflect, not simply exaggerated arousal under challenge, but rather an increased biological sensitivity to context, with potential for negative health effects under conditions of adversity and positive effects under conditions of support and protection. From an evolutionary perspective, the developmental plasticity of the stress response systems, along with their structured, context-dependent effects, suggests that these systems may constitute conditional adaptations: evolved psychobiological mechanisms that monitor specific features of childhood environments as a basis for calibrating the development of stress response systems to adaptively match those environments. Taken together, these theoretical perspectives generate a novel hypothesis: that there is a curvilinear, U-shaped relation between early exposures to adversity and the development of stress-reactive profiles, with high reactivity phenotypes disproportionately emerging within both highly stressful and highly protected early social environments.
Content may be subject to copyright.
Biological sensitivity to context: I. An
evolutionary–developmental theory of the
origins and functions of stress reactivity
University of California, Berkeley; and
University of Arizona
Biological reactivity to psychological stressors comprises a complex, integrated, and highly conserved repertoire of
central neural and peripheral neuroendocrine responses designed to prepare the organism for challenge or threat. De-
velopmental experience plays a role, along with heritable, polygenic variation, in calibrating the response dynamics
of these systems, with early adversity biasing their combined effects toward a profile of heightened or prolonged re-
activity. Conventional views of such high reactivity suggest that it is an atavistic and pathogenic legacy of an evolu-
tionary past in which threats to survival were more prevalent and severe. Recent evidence, however, indicates that ~a!
stress reactivity is not a unitary process, but rather incorporates counterregulatory circuits serving to modify or tem-
per physiological arousal, and ~b!the effects of high reactivity phenotypes on psychiatric and biomedical outcomes
are bivalent, rather than univalent, in character, exerting both risk-augmenting and risk-protective effects in a
context-dependent manner. These observations suggest that heightened stress reactivity may reflect, not simply exag-
gerated arousal under challenge, but rather an increased biological sensitivity to context, with potential for negative
health effects under conditions of adversity and positive effects under conditions of support and protection. From an
evolutionary perspective, the developmental plasticity of the stress response systems, along with their structured,
context-dependent effects, suggests that these systems may constitute conditional adaptations: evolved psychobio-
logical mechanisms that monitor specific features of childhood environments as a basis for calibrating the develop-
ment of stress response systems to adaptively match those environments. Taken together, these theoretical
perspectives generate a novel hypothesis: that there is a curvilinear, U-shaped relation between early exposures to
adversity and the development of stress-reactive profiles, with high reactivity phenotypes disproportionately emerg-
ing within both highly stressful and highly protected early social environments.
Biological reactivity to environmental stress-
ors is now widely implicated in the processes
linking psychological adversity to psychiatric
and biomedical disorder. The neuroendocrine
changes that reliably accompany stressful
events, in humans and other species, are the
physiological, homeostatic means by which
survival under threat is protected, but are also
among the dysregulatory pathways by which
psychological trauma is transmuted into patho-
genic biological processes. Individual differ-
ences in such “stress reactivity” are thought to
underlie the broad variability in stress–illness
associations and to reflect constitutional vari-
ation in susceptibility to stressful challenge.
Highly reactive phenotypes, in which affected
individuals mount vigorous and0or persistent
Theresearch onwhich thispaper wasbased wassupported
by grants from the John D. and Catherine T. MacArthur
Foundation’s Research Network on Psychopathology and
Development, the National Institute of Child Health and
Human Development ~1RO1 HD 24718!, and by the Di-
vision of Intramural Research of NICHD. The first author
is particularly indebted to Dr. Steve Suomi and Dr. Jan
Genevro for a series of conversations that directly influ-
enced the ideas upon which this paper is based. We also
thank Dr. Jay Belsky and Dr. David Bjorklund for their
helpful comments on an earlier draft of this paper.
Address correspondence and reprint requests to: W.
Thomas Boyce, Institute of Human Development, School
of Public Health, Public Health CHHD ~U90!, 570 Uni-
versity Hall, University of California, Berkeley, CA94720-
1190; E-mail:
Development and Psychopathology 17 ~2005!, 271–301
Copyright © 2005 Cambridge University Press
Printed in the United States of America
DOI: 10.10170S0954579405050145
autonomic, adrenocortical, or other biological
responses to stressors, have been viewed as
an atavistic health risk factor, a legacy of
physiological responses more commensurate
with the perils of prehistoric human environ-
ments. As such, exaggerated stress reactivity
is generally viewed as a maladaptive, mono-
tonically harmful heritage of an ancient pre-
paredness for endangerment. High reactivity,
so the argument goes, is a heritable response
disposition, often unmasked by traumatic ex-
periences in early life, which places individu-
als at heightened risk for disorders of mental
and physical health. It is the central claim of
this two-part series that this view, that high
reactivity phenotypes are uniformly harmful
psychobiological reversions to primitive and
maladaptive modes of response, is mistaken.
Rather, an evolutionary reinterpretation of
evidence regarding reactivity and health sug-
gests that highly reactive phenotypes can be
more usefully viewed as reflecting heightened
biological sensitivity to context ~BSC!,an
attribute that may have conferred selective ad-
vantages in certain social and ecological con-
texts during human evolution. Further, although
a substantial literature documents the capacity
of early developmental trauma to predispose
an individual toward high biological reactiv-
ity, an evolutionary formulation of recent find-
ings suggests a different and novel hypothesis:
that the association between early adversity
and reactivity is curvilinear in character, with
both highly stressful and highly protective
environments yielding disproportionate num-
bers of highly reactive children. In this paper,
the theoretical and evidential grounds for this
new hypothesis are presented, and in the
second paper, exploratory data analyses in
two studies of early development and psycho-
pathology are used to generate empirical
observations commensurate with the same
hypothesis. Together, the papers present both
theoretical and empirical lines of argument
that converge upon a single thesis: that highly
reactive phenotypes are forms of enhanced,
neurobiologically mediated sensitivity to con-
text, which have been favored by natural se-
lection due to their fitness-enhancing effects
in both minimally and maximally stressful
environments. This evolutionary paradox, of
reactive phenotypes being selected within
two oppositional categories of environments,
can be resolved, it will be argued, by the sup-
position that BSC increases adaptive compe-
tence in highly stressful environments by
augmenting vigilance to threats and dangers
and in highly protective environments by in-
creasing susceptibility to social resources and
ambient support. In the sections that follow,
we ~a!describe the structure and phylogeny
of the neural circuits implicated in stress
reactivity, ~b!delineate genetic and environ-
mental contributions to the calibration of
such reactivity, ~c!review past and recent find-
ings linking stress reactivity and health, and
~d!conclude that phenotypic expressions of
unusually heightened reactivity reflect an
underlying biological sensitivity to contex-
tual signals. Finally, exploring this reconcep-
tualization of exaggerated reactivity as context
sensitivity, we construct an evolutionary–
developmental theory of the origins and
functions of the human stress response and
formulate new hypotheses characterizing the
relation between early adversity and the mag-
nitude of biological responses to stress. This
theory and derivative hypotheses are founded
on the concept of conditional adaptation, in
which a single genotype supports a range of
environmentally contingent phenotypic expres-
sions, enabling an adaptive correspondence
between the developing organism and its
The Structure and Phylogeny of the
Human Stress Response
Environmental events signaling threats to sur-
vival or well being produce a set of complex,
highly orchestrated responses within the
neural circuitry of the brain and peripheral
neuroendocrine pathways regulating meta-
bolic, immunologic, and other physiological
functions. As first described in the work of
Claude Bernard on homeostasis ~Bernard,
1878!and the subsequent research of 20th
century stress physiologists Walter Cannon
~1929!and Hans Selye ~1950!, this elaborate
and tightly integrated repertoire of responses
results in an immediate, relatively automatic
272 W. T. Boyce and B. J. Ellis
shift to a state of biological and behavioral
preparedness, involving increases in heart
rate and blood pressure, metabolic mobiliza-
tion of cellular nutrients, preferential redirec-
tion of energy resources and perfusion to the
brain, and the induction of behavioral vigi-
lance and fear. Comprehensively detailed in
the writings of neuroscientists such as Chrou-
sos ~1998!, Meaney ~2001!, and McEwen
~1998!, the neural substrate for the organism’s
stress response comprises two anatomically
distinct but functionally integrated circuits,
the corticotropin-releasing hormone ~CRH!
system and the locus coeruleus–norepinephrine
~LC-NE!system. The coactivation of the these
two systems, along with their linkages to lim-
bic structures, such as the amygdala and an-
terior cingulate, as well as the mesolimbic
dopaminergic system and the medial prefron-
tal cortex, produce the coordinated biobehav-
ioral changes associated with the stress
response in mammalian species.
The CRH system actually comprises two
distinguishable subsystems, one centered in
the paraventricular nucleus ~PVN!of the hy-
pothalamus and involved in the homeostatic
regulation of the hypothalamic–pituitary–
adrenocortical ~HPA!axis, and the other
involved in the corticolimbic circuitry of
the amygdala and its connections. Within the
former subsystem, CRH is released into the
portal blood supply of the pituitary in a
pulsatile ~and, under normative conditions,
circadian!fashion by neurons in the PVN and
serves, along with synergistic effects of
arginine vasopressin ~AVP!, as the primary
secretagogue for expression of pro-opio-
melanocortin ~POMC!polypeptide by the
anterior pituitary. In the second subsystem,
CRH cell bodies are more widely represented
in loosely related, extrahypothalamic loca-
tions, including the amygdala, the substantia
innominata, the bed nucleus of the stria termi-
nalis, and in the prefrontal, insular, and cingu-
late regions of the cortex ~Gold & Chrousos,
2002; Owens & Nemeroff, 1991!. Two or more
types of CRH receptors have been elucidated,
with species variation in the expression of spe-
cific receptor types. CRH
receptors are found
in the anterior pituitary and other brain re-
gions and are involved in generating fear-
related behavior, and CRH
receptors, found
mostly in the periphery, may play a counter-
regulatory role in anxiogenesis. POMC is
cleaved into its component proteins, cortico-
tropin ~ACTH!and b-endorphin ~Smith et al.,
1998!, and ACTH is transported in plasma to
the zona fasciculata of the adrenal cortex, trig-
gering secretion of cortisol, the principal
human glucocorticoid regulating blood pres-
sure, glucose metabolism, and immune com-
petence. Glucocorticoids also inhibit those
neuroendocrine axes promoting growth and
reproduction ~Gold, Goodwin, & Chrousos,
The intracellular actions of cortisol are me-
diated through binding to a widely distributed
cytoplasmic receptor, translocation to the nu-
cleus of the target cell, and subsequent direct
effects on gene transcription and inhibition
of other, proregulatory transcription factors
such as c-jun0c-fos, and NF-kB ~van der Saag,
Caldenhoven, & van de Stolpe, 1996!. Al-
though such actions acutely facilitate essen-
tial biological responses to stress and threat,
chronic glucocorticoid secretion is associated
with a variety of pathogenic processes and
disease states, including major depression, in-
sulin resistance and diabetes, hypertension and
atherosclerosis, bone loss, and disorders re-
lated to diminished immune functions ~Gold
& Chrousos, 1999; McEwen, 1998!. The hip-
pocampus, a brain region closely involved in
memory and learning, is particularly suscep-
tible to the effects of glucocorticoids, show-
ing decreased dendritic branching and neuronal
loss in the CA3 area, as well as changes in
synaptic terminal structure and inhibition of
neuron regeneration ~Bremner & Vermetten,
2001; Sapolsky, 1996!. Under more norma-
tive circumstances, circulating cortisol there-
fore adaptively regulates the activation level
of the HPA axis through a process of feedback
inhibition at the hypothalamus, the pituitary,
and extrahypothalamic centers such as the hip-
pocampus and frontal cortex ~Dallman,Akana,
Cascio, Darlington, Jacobson, & Levin, 1987!.
The LC-NE system comprises the norad-
renergic cells of the medulla and dorsal pons
and their projections to the amygdala, hippo-
campus, mesolimbic dopamine system, and
the medial prefrontal cortex ~Aston–Jones,
Biological sensitivity to context: I 273
Rajkowski, Kubiak, Valentino, & Shipley,
1996!. LC activation of hypothalamic centers
also contributes to activation and regulation
of the autonomic nervous system ~ANS!, ini-
tiating the so-called fight or flight responses
to challenge. The ANS, comprising sympa-
thetic, parasympathetic, and enteric branches,
modulates physiologic arousal and recovery
in the periphery and produces the familiar bio-
logical concomitants of severely stressful en-
counters, including heart rate and respiratory
rate acceleration, sweat production, dry mouth,
and, if sufficiently severe, loss of urinary or
fecal continence. These biological responses
are mediated both by direct autonomic inner-
vation of target organs by postganglionic neu-
rons and by secretion of epinephrine and
norepinephrine by the adrenal medulla. Im-
mune regulatory effects of the catecholamines,
as well as those of CRH and the glucocorti-
coids, appear due to differential effects on
T-helper-10T-helper-2 cells and type 10type 2
cytokine production ~Habib, Gold, & Chrou-
sos, 2001!. Through such direct effects on im-
mune cells, experiences of severe or prolonged
stress may influence susceptibility to a variety
of infectious, autoimmune0inflammatory, or
neoplastic diseases ~Elenkov & Chrousos,
1999!. NE from the LC may also contribute to
vulnerability to stress-related symptoms by fa-
cilitating emotional memory retention in the
hippocampus and striatum ~Introini–Collison,
Dalmaz, & McGaugh, 1996!.
Although anatomically distinct, the neural
functioning of the CRH and LC-NE systems
is highly integrated and cross-regulatory. CRH-
expressing neurons in the central nucleus of
the amygdala, for example, project directly
to the LC, escalating the firing rate of LC
neurons, enhancing NE release within the
ascending noradrenergic system, and produc-
ing many of the fear-related behaviors associ-
ated with stressful experience ~Meaney, 2001;
Valentino, Curtis, Page, Pavcovich, & Florin–
Lechner, 1998!. These CRH-mediated path-
ways from the amygdala to the LC may also
serve as the neural substrate for many of the
symptoms of anxiety disorders, such as in-
creased acoustic startle responses, vigilance,
symptoms of avoidance, and recurrent emo-
tional memories. Reciprocally, activation of
NE secreting neurons in the LC has been shown
to increase CRH production in the PVN ~Habib
et al., 2001!. This cross-regulatory process is
only one of several ways in which the LC-NE
and CRH are functionally interactive ~Gold &
Chrousos, 2002; Viau, 2002!, and together con-
stitute a primary integrative pathway by which
psychologically and emotionally relevant en-
vironmental signals are transmuted into the
behavioral, autonomic, and immunologic man-
ifestations of human pathology ~Cacioppo,
Berntson, Malarkey, Kiecolt–Glaser, Sheri-
dan, Poehlmann, Burleson, Ernst, Hawkley, &
Glaser, 1998; Heilig, Koob, Ekman, & Brit-
ton, 1994; McEwen & Stellar, 1993!. Dysreg-
ulated activation has been implicated, as well,
in the genesis and presentation of the major
neuropsychiatric disorders ~Bloom & Kupfer,
1995!, and the experimental administration of
neurohormonal products from the CRH and
LC-NE systems produces many of the physi-
ological and behavioral symptoms that char-
acterize affective and anxiety disorders ~Dunn
& Berridge, 1990; Heilig et al., 1994!.
Both stress response systems, as well as
their central and peripheral components, ap-
pear early in phylogeny and have been exten-
sively conserved in the evolutionary history
of vertebrate and mammalian species. Steroid
hormones are derived from cholesterol and
occur widely in both animal and plant species,
exhibiting chemical activities reminiscent even
of the mammalian glucocorticoids ~Bentley,
1998!. Different forms of C
, and C
adrenal corticosteroids appear in all the major
vertebrate groups, with both cortisol and
corticosterone found in primitive, cartilagi-
nous fish and aldosterone and corticosterone
identified in the higher fish, amphibians, and
reptiles. The glucocorticoid receptors of mam-
malian species are thought to have evolved
from a 500 million year old ancestral gene,
such as that coding for the single steroid re-
ceptor expressed in teleost fish. Such fish cor-
ticosteroid receptors exhibit a 97% homology
in their DNAbinding region to the amino acid
sequence of the human glucocorticoid recep-
tor. Even pituitary hormones similar to those
found in the vertebrate HPA axis are present
in some invertebrates, including mollusks and
274 W. T. Boyce and B. J. Ellis
Catecholaminehormones of theLC-NEand
ANShave a similarlylong phylogeny.Theyare
presentin many invertebrates, suchasthe chor-
dateAmphioxus arrow worm,andeven in some
ciliated protozoans, where they function met-
abolically in a manner remarkably similar to
their roles in higher animal species. Like ste-
roidreceptors, catecholaminereceptorsare also
representedin primitivespeciesand have trans-
membrane domains that have been highly con-
served. The complexity of the ANS appears to
haveincreased phylogeneticallywiththat ofthe
CNS,attainingapproximatelysimilar levels of
organization and complexity within the am-
niote classes of reptiles, birds, and mammals.
Taken together, these observations from
the human and infrahuman neurosciences sug-
gest the following interim observations. First,
homeostatic systems protecting survival and
stability under conditions of stress are phylo-
genetically ancient, showing both genetic ex-
pression and comparable biological functions
in animal species from invertebrates to pri-
mates. Second, the CRH and LC-NE systems
subserve a complex, highly interactive reper-
toire of central and peripheral stress responses,
which mobilize neurobiological and behav-
ioral resources in defense of the organism’s
integrity and well being. Third, although these
neurobiological responses are protective and
essential in acutely stressful conditions, they
can become themselves pathogenic when per-
sistently activated under circumstances of
chronic or overwhelming stress and adversity.
Genes, Environments, and Reactive
Reactivity has been defined ~Matthews, 1986!
as “the deviation of a physiological response
parameter from a comparison or control value
that results from an individual’s response to a
discrete,environmental stimulus.” Broad indi-
vidual variation in reactivity to psychological
stressorshas been documentedin human adults
~Cacioppoet al.,1998!, humanchildren~Alkon,
Goldstein, Smider, Essex, Kupfer, & Boyce,
2003;Allen& Matthews,1997!,and bothyoung
andmature laboratory animals~Meaney,2001;
Suomi, 1987a!. Although the origins of such
individual differences in reactivity, which is
the central focus of the present papers, remain
incompletelyunderstood, thereis wideacknowl-
edgement that both the genome and early ex-
perienceaccount for someshare of thevariance
in phenotypic stress responses.
Within rodent and other subprimate mam-
malian models of reactivity developed by
Meaney and colleagues ~Liu & Meaney, 1997;
Meaney, 2001!and others ~Reis & Golanov,
1997!, there is evidence that individual differ-
ences are determined by strain-related genetic
variations, by aspects of early maternal–infant
experience, and by interactions among gene
expression and experiential factors. On the one
hand, clear biobehavioral differences exist be-
tween strains of mice and rats on dimensions
such as behavioral and adrenocortical reactiv-
ity to stressors. BALBc mice, for example, are
inherently more fearful and show more vigor-
ous glucocorticoid responses to stressors than
do C57 mice ~Zaharia, Kulczycki, Shanks,
Meaney, & Anisman, 1996!, and comparable
differences exist between Fisher 344 and Long–
Evans rats ~Dhabhar, McEwen, & Spencer,
1993!. Such biobehavioral differences in strains
are likely due, at least in part, to heritable
variation in the alleles that regulate stress re-
sponsive biological systems in these animals.
On the other hand, Meaney and others have
shown that perturbations in early experience
resulting in changed maternal–infant behavior
can also have profound regulatory effects on
the calibration of biological systems, includ-
ingthe CRHsystemand HPAaxis~Hofer,1994;
Meaney, 2001; Plotsky & Meaney, 1993!.An
experimental procedure known as “handling,”
in which rodent pups are separated from their
mothers for 3–15 min each day over the first
severalweeks oflife, resultsin permanentdown-
regulatory changes in the CRH system at the
level of the PVN and central nucleus of the
amygdala and, as a consequence, produces a
decreased exposure to the adrenocortical and
autonomic effects of stressful events. Such
downregulatoryeffectshave been shown to re-
sultfrom increased glucocorticoid receptor ex-
pression following changes in mothering
behavior, that is, the intensity of licking and
grooming and other characteristic maternal
behaviors,upon thepups’return tothenest. Fur-
ther,handling can override the genetic propen-
Biological sensitivity to context: I 275
sities shared with a fearful, highly reactive
motherby inducingmaternal behaviorsthatpro-
duce long term underarousal in the infants’ ad-
renocortical and autonomic response systems
~Champagne & Meaney, 2001!. It remains un-
clear at present whether the regulatory effects
of these maternal behaviors are constrained to
a “critical,” early period of development or are
in infancy or beyond.
When early maternal–infant separations are
more prolonged, however, in a regimen involv-
ing true deprivation of maternal care for as
long as 180 min, the effect on biological stress
response systems is exactly opposite that of
handling ~Meaney, 2001!. Separated rodent
pups develop chronically upregulated CRH ac-
tivity in the HPA axis, the amygdala, bed nu-
cleus of the stria terminalis, and the LC, as
well as behavioral changes consistent with fear-
fulness and inhibition under conditions of nov-
elty ~Sanchez, Ladd, & Plotsky, 2001!. There
is also evidence for effects of prenatal stress-
induced maternal glucocorticoids on fetal, and
later infant, physiology and development. Ma-
ternal glucocorticoid exposures are associ-
ated, for example, with elevations of CRH
~Cratty, Ward, Johnson, Azzaro, & Birkle,
1995!and CRH receptors ~Ward, Johnson,
Salm, & Birkle, 2000!in the amygdala of off-
spring, and with downregulation of 11b-
hydroxysteroid dehydrogenase, the placental
enzyme that inactivates fetal steroidal effects
~Benediktsson, Lindsay, Noble, Seckl, & Ed-
wards, 1993!. Both down- and upregulatory
alterations in CRH system regulation ~those
produced by handling and by maternal sepa-
ration, respectively!can have detrimental
effects on disease and survival, depending upon
the kinds of exposures that the animals later
sustain. Handled animals have been shown to
be more susceptible, for example, to immune-
mediated disorders, such as experimental al-
lergic encephalomyelitis ~Laban, Dimitrijevic,
von Hoersten, Markovic, & Jankovic, 1995!,
while those experiencing extended maternal
separations have shown increased vulner-
ability to stress-related hippocampal damage
and deficits in learning or memory ~Issa, Rowe,
Gauthier, & Meaney, 1990; Sapolsky, 1996!.
These studies suggest both heritable and ex-
periential influences on the expression of
stress reactivity in rodent models and reveal
influences that are bivalently regulatory in
their effects on psychobiological response
Studies of nonhuman primates have simi-
larly contributed important evidence to an
understanding of constitutional and contex-
tual determinants of stress reactivity. Suomi
and colleagues ~Byrne & Suomi, 2002; Cham-
poux & Suomi, 1994; Suomi, 1987b!, for
example, have increasingly documented the
influence of heritable genetic factors on
the neurobiological systems that underpin tem-
peramental differences in behavior. One study
comparing neurobiological differences be-
tween Indian origin and Chinese hybrid
rhesus monkeys found significantly lower
cerebrospinal fluid ~CSF!5-hydroxyindole-
acetic acid levels ~a metabolite of serotonin!
in Chinese hybrid monkeys beginning at 6
months of age, suggesting “strain” differences
in the magnitude of central serotonergic activ-
ity ~Champoux et al., 1997!. Serotonergic neu-
rons are implicated in the neural circuitry of
the stress response and in brain structures
involved in the processing of emotional
information ~Rolls, 1999!. Another study by
Lyons, Yang, Sawyer–Glover, Moseley, and
Schatzberg ~2001!showed that stress-related
hippocampal atrophy is partially heritable,
raising questions regarding an attribution of
hippocampal volume variation to purely expe-
riential factors. Further, primate studies by Hi-
gley and others have demonstrated heritable
variation in central serotonergic drive, which
is in turn related to aspects of behavioral re-
activity ~Higley & Linnoila, 1997!, and have
identified both genetic and environmental con-
tributions to differences in serotonin and do-
pamine metabolites in the cerebrospinal fluid
of young macaques ~Higley,Thompson, Cham-
poux, Goldman, Hasert, Kraemer, Scanlan,
Suomi, & Linnoila, 1993!.
Although the above research suggests at
least partial genetic regulation of stress re-
sponse systems, studies of nonhuman pri-
mates have also revealed a capacity for early,
stress-engendering disruptions of social expe-
rience to produce long-term changes in neuro-
biological reactivity ~Sanchez et al., 2001!.
276 W. T. Boyce and B. J. Ellis
Research on early deprivation, beginning with
the seminal work of Harlow and colleagues at
the University of Wisconsin Primate Labora-
tory ~Harlow, Harlow, & Suomi, 1971!, has
demonstrated the centrality of maternal–infant
relationships in the emergence of species
normative behavior, and the capacity for
isolate- or peer-rearing conditions to disrupt
behavioral and psychobiological regulatory
functions in several Old and New World pri-
mate species. Accompanied by behavioral
changes such as protest vocalizations, autistic-
like stereotypies, nonnutritive sucking, and
self-mutilation, maternal separations produce
predictable changes in peripheral and central
neural circuitry. Among these are alterations
in functional immune competence ~Lubach,
Coe, & Ershler, 1995!, upregulation of auto-
nomic responses to physical stressors ~Mar-
tin, Sackett, Gunderson, & Goodlin–Jones,
1988!, increased CRH expression in CSF
~Coplan, Andrews, Rosenblum, Owens, Fried-
man, Gorman, & Nemeroff, 1996!, and dys-
regulatory changes in HPA axis reactivity
~Shannon, Champoux, & Suomi, 1998!.As
comprehensively reviewed by Sanchez et al.
~2001!, dysregulatory changes in the CRH sys-
tem have reliably been found following expo-
sures of infant monkeys to isolated or deprived
early rearing conditions, but the character and
direction of such changes remain indetermi-
nate in the existing literature. Although some
groups have shown consistent elevations in
cortisol expression under conditions designed
to undermine maternal attentiveness ~Cham-
poux, Hwang, Lang, & Levine, 2001; Lyons,
Wang, Lindley, Levine, Kalin, & Schatzberg,
1999!, others have detected no differences in
HPA responses to stressors among isolation
reared rhesus infants ~Meyer & Bowman,
1972!. In one study by Boyce, Champoux,
Suomi, and Gunnar ~1995!, peer rearing of
infant macaques appeared associated with
blunted, downregulatory changes in the circa-
dian periodicity of cortisol secretion. Further,
the work of Sapolsky ~1990; Sapolsky & Share,
1994!among wild olive baboons has revealed
associations between dominance status and ad-
renocortical activation, suggesting either that
experiences related to social adeptness and
dominant hierarchical status tended to lower
cortisol levels or that constitutionally less re-
active individuals occupied higher status po-
sitions. Comparable to observations within
rodent models of stress reactivity, studies of
nonhuman primates offer further evidence for
both genetic and contextual influences on the
calibration of stress response systems.
Finally, a growing number of studies in
human children and adults have similarly re-
vealed both genomic and environmental ori-
gins for the individual differences observed
in biological reactivity ~Heim & Nemeroff,
1999!. In parallel to genetic evidence from
nonhuman primates, studies of children and
their parents ~Matthews, Manuck, Stoney,
Rakaczky, McCann, Saab, Woodall, Block,
Visintainer, & Engebretson, 1988!, adults in
preidentified genetic pedigrees ~Cheng, Car-
melli, Hunt, & Williams, 1997!, as well as
mono- and dizygotic twins ~Bartels, de Geus,
Kirschbaum, Sluyter, & Boomsma, 2003; Bus-
jahn, Faulhaber, Viken, Rose, & Luft, 1996;
Turner & Hewitt, 1992!have all affirmed a
moderate heritability of reactivity pheno-
types. A parental history of hypertension has
frequently been shown to be predictive of au-
tonomically mediated blood pressure reactiv-
ity in both children ~e.g., Lemne, 1998!and
young adults ~e.g., Adler & Ditto, 1998!. El-
evated cortisol levels have also been identi-
fied in the nondepressed, first-degree relatives
of patients with major depression, suggesting
that hypercortisolism might be appropriately
viewed as a trait measure of a heritable diath-
esis to affective disorders ~Holsboer, Lauer,
Schreiber, & Krieg, 1995!.
In addition, the research programs of a
number of investigators have produced find-
ings supporting experiential, contextual con-
tributions to the emergence of high reactivity.
A number of studies in human children sug-
gest, for example, that disruptions in early
attachment relationships are associated with
regulatory influences on and disturbances in
stress–responsive biological systems ~Herts-
gaard, Gunnar, Erickson, & Nachmias, 1995;
Meyer, Chrousos, & Gold, 2001; Nachmias,
Gunnar, Mangelsdorf, Parritz, & Buss, 1996;
Willemsen–Swinkels, Bakermans–Kranenburg,
Buitelaar, van, & van Engeland, 2000!. Fur-
ther, a prospective, longitudinal study by Es-
Biological sensitivity to context: I 277
sex, Klein, Cho, and Kalin ~2002!demonstrated
that, parallel to the findings of animal re-
search, early exposures to stressors such as
maternal depression can sensitize children’s
CRH systems to subsequent adversities, result-
ing in the development of mental health symp-
toms. In a singular study of healthy women by
Heim, Newport, Heit, Graham, Wilcox, Bon-
sall, Miller, and Nemeroff ~2000!, partici-
pants with a history of abusive experiences in
childhood had dramatically increased levels
of pituitary ~ACTH!and autonomic reactivity
to a standardized laboratory stress protocol.
Abused women with current major depression
exhibited sixfold greater ACTH responses than
age-matched controls and were the only group
to show significantly elevated cortisol re-
sponses, as well. De Bellis, Baum, Birmaher,
Keshavan, Eccard, Boring, Jenkins, and Ryan
~1999!similarly found increased 24-hr uri-
nary excretion of cortisol and norepinephrine
among children with abuse-related posttrau-
matic stress disorder ~PTSD!symptoms, in
comparison to healthy controls, and Perry
~1994!reported diminished adrenergic recep-
tors on platelets and increased heart rates in a
group of severely abused children. Aseries of
studies by Yehuda and coworkers ~Yehuda,
2002; Yehuda, Halligan, & Bierer, 2001; Ye-
huda, Halligan, & Grossman, 2001!has fur-
ther documented the psychobiological sequelae
of early abusive experiences. Sexual abuse was
associated with elevated 24-hr urinary corti-
sol excretion ~Yehuda et al., 2001!, increased
density of lymphocyte glucocorticoid recep-
tors, and enhanced suppression of plasma
cortisol responses to dexamethasone ~Stein,
Yehuda, Koverola, & Hanna, 1997!, each re-
flecting disturbances in the regulation of the
HPA axis. In an interesting parallel to the ob-
servations in nonhuman primates mentioned
above, Yehuda et al. ~2001!also reported that
emotional abuse and PTSD were associated
with diminished, rather than elevated, 24-hr
urinary cortisol levels. In studies of broader
societal influences on the development of stress
responses, Lupien, King, Meaney, and Mc-
Ewen ~2000!found that lower socioeconomic
status was associated with higher salivary cor-
tisol levels in children as young as 6 years of
age, and Fernald and Grantham–McGregor
~1998!observed higher salivary cortisol lev-
els and greater cardiovascular reactivity among
growth-stunted children growing up in impov-
erished neighborhoods in Jamaica.
Taken together, rodent, nonhuman primate,
andhuman research all pointto a common con-
clusion: that both genetic and environmental
factors contribute to the calibration of biolog-
ical stress response systems over the course of
early development. These studies further sug-
gestthat, while stable individual differencesin
stress reactivity emerge with maturation, there
is pronounced early plasticity in the neurobio-
logical systems that subserve such reactivity
~Davidson, Jackson, & Kalin, 2000!. Stress
reactivity, like many developmentally ac-
quired phenotypic features, appears to become
“canalized”overtime,revealing progressively
greater resistance to change and diminishing
plasticity ~Turkheimer & Gottesman, 1991;
Waddington, 1966!. Within the setting of hu-
man development, however, little is under-
stood of the developmental time course over
which such canalization occurs. Some of the
developmental role of primary attachment re-
lationships and maternal behavior in shaping,
constraining, and regulating psychobiological
responsesto experiencesof futurechallengeand
adversity.Suchfindings suggest,althoughwith
considerable imprecision, that social contex-
tual effects over the first 3–5 years of life may
have particular potency in the calibration of
stress responsive biological systems.
Stress Reactivity and Health
The CRH and LC-NE systems together con-
stitute a primary integrative pathway by which
psychologically and emotionally relevant en-
vironmental signals are transmuted into the
behavioral, autonomic, and immunologic man-
ifestations of human pathology ~Cacioppo
et al., 1998; Heilig et al., 1994; McEwen &
Stellar, 1993!. Dysregulated activation has been
implicated, as well, in the genesis and presen-
tation of the major neuropsychiatric disorders
~Bloom & Kupfer, 1995!, and the experimen-
tal administration of neurohormonal products
from the CRH and LC-NE systems produces
manyof the physiologicalandbehavioral symp-
278 W. T. Boyce and B. J. Ellis
tomsthat characterizeaffectiveand anxietydis-
orders ~Dunn & Berridge, 1990; Heilig et al.,
1994!.In epidemiologicandobservational stud-
ies of humans, individual differences in adre-
nocortical and autonomic reactivity have been
associated with a variety of mental and physi-
cal disorders, including internalizing and ex-
ternalizing psychopathology ~Boyce, Quas,
Alkon, Smider, Essex, & Kupfer, 2001; Ka-
gan,1994; Raine,Venables,&Mednick,1997!,
psychologicalandphysical symptoms ~Boyce,
Chesney, Alkon–Leonard, Tschann, Adams,
Chesterman,Cohen, Kaiser,Folkman, &Wara,
1995; Gannon, Banks, Shelton, & Luchetta,
1989!, risk for atherosclerotic heart disease
~Lynch,Everson,Kaplan,Salonen, & Salonen,
1998!, injuries ~Boyce, 1996!, and risk-taking
behavior~Liang, Jemerin,Tschann,Irwin,Wara,
& Boyce, 1995!. As reviewed by Cacioppo,
Berntson,Sheridan, andMcClintock~2000!, as-
sessments of stress reactivity to challenge, in a
variety of physiological modalities, enhances
significantly the clinical predictions of health
outcomes that are possible on the basis of rest-
ing or static measures alone.
The conventional understanding of stress
reactivity is that it represents a pathogenic
biobehavioral atavism: a vestige of physiolog-
ical responsivity to prehistoric environments
that is no longer adaptive within the intensity
and challenges of modern life and, conse-
quently, increases risk for the development of
various morbidities. This view has been con-
vincingly articulated by a generation of inves-
tigators, including René Dubos, the pioneering
20th century human biologist, and Randolph
Nesse, an eminent evolutionary psychiatrist at
the University of Michigan’s Institute for So-
cial Research:
Another illustration of the fact that modern man
retains essential traits of his evolutionary past is
the persistence in him of hormonal and metabolic
responses which were developed to meet threaten-
ing situations during his animal ancestry, but which
no longer fit the needs of life in civilized societies
. . . what was once an advantage is increasingly
becoming a handicap under the conditions of mod-
ern human life. ~Dubos, 1965, p. 29!
Despite the amount of stress we experience, how-
ever, our ancestors almost certainly experienced
more. With no police, no food reserves, no medi-
cine, no laws, rampant infections, and prevalent
predators, danger could come at any time . . . Per-
haps in that environment, where stressors were more
often physical, the stress response was more useful
than it is now. Today, we mainly face social and
mental threats, so the actions of the HPA system
may yield net costs. This is plausible and supports
the many efforts to reduce stress and to find drugs
that block the stress response. ~Nesse & Young,
2000, p. 83!
A full rendition of this widely endorsed ac-
count comprises the following twin premises:
~a!because stress responses evolved in ances-
tralenvironments characterizedbyfrequent, se-
vere threats to survival, a unitary system of
physiological arousal emerged, which readies
the organism for confrontation or retreat, often
in a manner disproportionate to the actual haz-
ardsencountered; and ~b!prolonged activation
or acute overactivation of such pathways ulti-
mately undermines the health of organisms by
impairing, rather than activating, the function
of target organs. Although the essential, pro-
tective aspects of these neurobiological re-
sponsesto adversityarebroadly acknowledged,
it has become an article of faith that overreac-
tivity promotes the genesis of disease. Com-
pelling and intuitive as the two premises have
appeared, both are now challenged by evi-
dence suggesting that stress reactivity is not a
unitary physiological process, because adver-
sity often results in down- rather than upregu-
latorychanges incomponent neuralcircuits,and
that high reactivity exerts bidirectional, rather
thanunivalent, influences on health.It is to this
now turns.
Anomalous findings on stress reactivity
and health
The first premise, that stress reactivity consti-
tutes a unitary, unidirectional set of biological
responses to threat, has been contested by a
collection of observations and new hypoth-
eses suggesting that the components of the
stress response system often act in opposition
to, rather than in alliance with, each other.
More than 40 years ago, Lacey ~1959!criti-
Biological sensitivity to context: I 279
cized the concept of uniform arousal, arguing
that, even within the ANS, different neural
components pursue different profiles of re-
sponse. His observations were followed by
those of other investigators such as Ekman,
Levenson, and Friesen ~1983!, who main-
tained that no general state of “arousal” ex-
ists, and that specific emotional experiences
are linked to specific constellations of ANS
and central neural activity. In 1984, Munck,
Guyre, and Holbrook advanced a new and then
counterintuitive proposal. They hypothesized
that glucocorticoids and the HPA axis, rather
than constituting the hormonal sine qua non
of stress-induced arousal, as had been widely
believed since the inception of stress research,
function instead as a buffering or counterreg-
ulatory influence, essentially “braking” the du-
ration or intensity of an otherwise overly
exuberant physiological response. It may thus
be the more slowly activated HPA axis that is
responsible for the termination or tempering
of the immediate, autonomically mediated fight
or flight state, by the glucocorticoids’ physio-
logical opposition to the effects of adrenergic
arousal. Such a view would resolve, they ar-
gued, the paradoxical observation that dis-
eases with known associations to psychological
stressors, such as rheumatoid arthritis or in-
flammatory bowel disease, can actually be
treated with glucocorticoids. Such sequences
of paired, counterregulatory processes are com-
mon in biological systems, such as the neuro-
nal action potential and the clotting cascade,
in which the same stimuli that activate initial
responses ~e.g., the opening of sodium chan-
nel gates or the cleaving of fibrinogen into
fibrin!also activate a delayed suppressor ~e.g.,
the closing of sodium channels or the activa-
tion of plasminogen to plasmin to lyse clots!,
which is required to restore a homeostatic state.
Munck’s proposal is, in fact, consistent with
a number of empirical observations that have
been reported since. Most recently, for exam-
ple, Bauer ~2002!found, in a cross-sectional
study, that the absolute levels of activation in
either the sympathetic or adrenocortical sys-
tem were less predictive of serious behavior
problems in 4- to 8-year-old children than
was the lack of concordance between the sys-
tems. Children with symmetrical activation
or no activation at all had the fewest behavior
problems, whereas children with activation
asymmetries had the most, suggesting that
dissociations between the sympathetic and
adrenocortical arousal under conditions of
challenge put children at risk for early psycho-
pathology, a conclusion commensurate with
Munck’s hypothesis. Similarly, a review pa-
per by Yehuda, McFarlane, and Shalev ~1998!
concluded that, among adult patients follow-
ing an acutely stressful event, the combina-
tion of low cortisol levels and high heart rates,
indicating a disjunction between adrenocorti-
cal and sympathetic responses, was most pre-
dictive of later PTSD symptoms. The findings
of both groups are also consistent with more
recent observations that catecholamines and
glucocorticoids interact in a variety of com-
plex ways, involving conjoint ~but sometimes
counterregulatory!effects on such functions
as lymphoproliferative responses, appetite, and
memory ~e.g., Sapolsky, Romero, & Munck,
Another collection of findings, recently
summarized by Gunnar and Vazquez ~2001!
and Heim, Ehlert, and Hellhammer ~2000!,
also challenges the first premise with evi-
dence of paradoxical suppression of HPA
activation under conditions of stress. Such “hy-
pocortisolism,” that is, lower basal cortisol
levels, less HPA reactivity, or a flattening of
the circadian cortisol cycle among higher risk
samples, has been noted in both animal and
human research, by multiple investigators, and
in a variety of research settings. In the previ-
ously noted study by Boyce, Champoux, et al.
~1995!, for example, peer rearing of infant
macaques was associated with blunted, down-
regulatory changes in the circadian periodic-
ity of cortisol secretion. Similarly, although
Gunnar, Morison, Chisholm, and Schuder
~2001!found persistent elevations in salivary
cortisol levels among children adopted out of
Romanian orphanages, Carlson and Earls
~1997!found low morning cortisol levels and
an absence of the normal circadian decline in
cortisol among children continuing to live in-
side of Romanian institutions. Infants with colic
~White, Gunnar, Larson, Donzella, & Barr,
2000!, children with psychosocial dwarfism
~Vazquez, Watson, & Lopez, 2000!, and chil-
280 W. T. Boyce and B. J. Ellis
dren living near the epicenter of a major earth-
quake ~Goenjian, Yehuda, Pynoos, Steinberg,
Tashjian,Yang, Najarian, & Fairbanks, 1996!
have all shown lower morning cortisol levels
and a flattening of the normal circadian cycle,
relative to control children without such con-
ditions or experiences. Children characterized
as shy or introverted similarly showed dimin-
ished cortisol reactivity to normative stressors
such as the beginning of a new school year
~Davis, Donzella, Krueger, & Gunnar, 1999;
de Haan, Gunnar, Tout, Hart, & Stansbury,
1998!. These findings with regard to the HPA
system are notably similar to those of two
other studies in which stressful life events were
found inversely related to cardiovascular
~rather than adrenocortical!reactivity in
children or youth ~Chesterman, Boyce, &
Winkleby, 1989; Musante, Treiber, Kapuku,
Moore, Davis, & Strong, 2000!. In an interest-
ing parallel to such observations in children,
Heim, Ehrlert, et al. ~2000!reviewed evi-
dence for associations between hypocortisol-
ism and stress-related disorders in adults and
similarly concluded that low cortisol patterns
are sometimes associated with experiences of
stress or adversity or with stress-related disor-
ders. Yehuda et al. ~2001!reported, for exam-
ple, that among adult children of Holocaust
survivors those with a self-reported history of
childhood trauma showed diminished, rather
than elevated, 24-hr urinary cortisol levels,
relative to a comparison group with no history
of trauma.
In summary, the often tacit, but largely con-
ventional, impression that stress reactivity rep-
resents a singular, unitary biological response
to adversity is weakened by two categories of
new evidence. First, recent findings suggest
that components of the stress response system
may act in a coordinated but counterregula-
tory manner, as proposed by Munck and col-
leagues ~1989!, some operating to dampen,
rather than magnify, the physiological effects
of others. Second, traumatic events and severe
stressors may be associated, in both children
and adults, with a downregulated HPA axis, a
diminution in circadian cortisol secretion, and
a reduction in cardiovascular reactivity.
The second premise, that exaggerated or
persistent reactivity is univalently associated
with stress-related morbidities, has also been
questioned in a growing number of studies
revealing that high reactivity phenotypes un-
der specific environmental conditions may be
associated with protective, rather than harm-
ful, effects and generate normative or im-
proved health outcomes. Such bivalent effects
of stress reactivity on human and primate mor-
bidities have thematically characterized a
series of studies reported by Boyce and col-
leagues over the past decade. Examining car-
diovascular and immunologic reactivity in two
cohorts of 3- to 5-year-old children, for exam-
ple, significant interactions ~see, e.g., Fig-
ure 1A!were detected with environmental
stressors in the prediction of respiratory ill-
ness incidence over the ensuing several month
periods ~Boyce, Chesney, et al., 1995!. Spe-
cifically, the noted interactions suggested bi-
directional effects of reactivity on illness
incidence: highly reactive children in high-
stress families or childcare centers sustained
significantly higher rates of respiratory illness
than their low reactive peers, but equally re-
active children in low-stress settings were the
healthiest of all children in the samples. By
contrast, the respiratory illness incidence of
low reactivity children was unresponsive to
environmental stress levels, showing approx-
imately the same, midlevel illness rates in both
low- and high-stress conditions. Similarly sig-
nificant interactions were found for injury in-
cidence ~Boyce, 1996!.
Although prospective in design, both of
these studies were observational in nature and
lacked experimental data on the incidence of
illnesses or injuries among the same group of
highly reactive children in both low- and high-
stress conditions. In a subsequent study of
semifree-ranging rhesus macaques, however,
such quasiexperimental conditions were satis-
fied ~Boyce, O’Neill–Wagner, Price, Haines,
& Suomi, 1998!. The troop of macaques, which
had been previously assessed for their degree
of biobehavioral reactivity to novel or chal-
lenging stimuli, lived in a 5-acre wooded hab-
itat in rural Maryland, on the grounds of the
National Institutes of Health Primate Center.
In 1993, the troop encountered a 6-month pe-
riod of protective confinement to a small, 1000-
square foot building, during a construction
Biological sensitivity to context: I 281
project on the habitat grounds. The confine-
ment proved highly stressful, however, and
the incidence of violent injuries increased five-
fold during the 6-month period. Blinded ascer-
tainment of medically attended injury rates
from veterinary records produced evidence for
a significant interaction between reactivity sta-
tus and confinement stress, which is plotted in
Figure 1B. As with the prior studies of chil-
dren, low reactivity individuals showed little
effect of the confinement, while those with
high reactivity showed dramatically higher
rates of violent injuries in the high-stress sit-
uation but lower rates in the preceding, low-
stress condition.
These findings documenting Reactivity 3
Context interactions in the prediction of bio-
medical outcomes have been supplemented by
recent observations from the same group of
investigators and several others on associa-
tions among stressors, reactivity and psycho-
logical symptoms in children and young adults.
There is reason to believe that the influence of
biological reactivity on mental health out-
comes may be even more profound than those
observed for biomedical disorders. Worth-
man, Angold, and Costello ~1998!, utilizing
data from the Great Smoky Mountains Study,
found associations in Appalachian children be-
tween high adrenocortical reactivity and fu-
ture diagnoses of anxiety disorders and between
low reactivity and diagnoses of conduct disor-
der. In other work examining cross-sectional
data from the Wisconsin Study of Families
Figure 1. The interactions among laboratory-based stress reactivity and environmental stressors in
predicting health outcomes. ~A!Immune reactivity ~changes in pokeweed nitrogen response!3family
stressful events and respiratory illness incidence in kindergartners ~N599; adapted from Boyce,
Chesney, et al., 1995!.~B!Biobehavioral reactivity3confinement stress and injury incidence in a troop
of semi-free-ranging rhesus monkeys ~N536; adapted from Boyce et al., 1998!.
282 W. T. Boyce and B. J. Ellis
and Work, main effects of autonomic reactiv-
ity on risk for both internalizing and external-
izing spectrum psychopathology in middle
childhood have been reported ~Boyce et al.,
2001!. Children with high levels of parasym-
pathetic reactivity to laboratory stressors were
significantly more likely to fall into the top
20% on mother and teacher reports of inter-
nalizing symptoms, while those with low
reactivity in both sympathetic and parasympa-
thetic branches of the ANS were significantly
more likely to display high rates of external-
izing behavior problems ~see also Scarpa &
Raine, 1997!. A third paper by Gannon et al.
~1989!, reporting on a cross-sectional study of
college students, found that participants with
laboratory evidence of exaggerated auto-
nomic reactivity showed higher rates of phys-
ical symptoms and depression under stressful
circumstances, but lower than average rates
under low or minimally stressful conditions.
Finally, a recent randomized experimental
study by Quas, Bauer, and Boyce ~2004!again
showed an interaction effect between auto-
nomic reactivity and social context, with highly
reactive children showing significantly better
memory for a previous, standardized stress-
ful event in a supportive social environment
and poorer memory under conditions of low
support, relative to a low reactivity compari-
son group. Although not all research examin-
ing Reactivity 3Context interactions have
replicated these findings ~see, e.g., Musante
et al., 2000!, a sufficiently substantial number
of studies have produced homologous results
to suggest a robust phenomenon worthy of
further and more explicit analysis.
Recent findings from a variety of investiga-
torsandsettingsthus call into question the sec-
ond of the premises that circumscribe the
prevailing conceptualization of stress reactiv-
ity. Rather than acting as a unidirectional risk
factor for poor health outcomes, as the second
premisewould assert, high-stress reactivityhas
been shown repeatedly to operate in a bivalent
manner, most often escalating the risk of mal-
adaptive outcomes in high-stress contexts, but
diminishing such risk and acting protectively
under supportive, low-stress conditions. Such
evidence signifies the need for a reconceptual-
ization of high reactivity phenotypes and sug-
gests that highly reactive individuals may be
more accurately described as biologically sen-
sitiveto the health-erodingor health-sustaining
effects of particular social and physical con-
texts.BSC isthereforeadvanced hereas ameans
of denoting and characterizing this bidirec-
tionalinfluence ofhigh-stressreactivity onpsy-
chiatric and biomedical health endpoints. As
argued above, stress reactivity is a nonunitary,
multifacetedcomplex of central andperipheral
neural responses. The present thesis, however,
is that heightened reactivity in each stress re-
sponsesystem is reflective ofamore elemental
biologicalpredisposition tocontextresponsive-
ness. In the remainder of this paper, we there-
fore refer to BSC as a phenotypic property of
individuals, which has both constitutional and
experiential origins, and is indexed by height-
ened reactivity in one or more of the stress re-
sponse systems.
BSC: The Dandelion and the Orchid
Such evidence for bivalent, context-dependent
health effects of highly reactive phenotypes
suggests that reactivity may reflect not simply
overarousal of neurobiological pathways, but
rather sensitivity to both harmful and protec-
tive contextual effects. Highly reactive chil-
dren appear to experience either the best or
the worst of psychiatric and biomedical out-
comes, within the populations from which they
are drawn. Under conditions of adversity, such
children sustain higher rates of disease, disor-
der, and injuries than their more normatively
reactive peers from the same environments.
On the other hand, equally reactive children
in low-stress, protective social environments
experience substantially lower rates of health
problems than their low reactive peers. These
results suggest that the highly reactive biolog-
ical profiles found in this subset of children
reveal a unique sensitivity or “permeability”
to the influence of environmental conditions
~Boyce, Chesney, et al., 1995!.
A Swedish idiomatic expression, maskros-
barn ~dandelion child!, refers to the capacity
of some children, not unlike those with low
reactive phenotypes, to survive and even thrive
in whatever circumstances they encounter, in
much the same way that dandelions seem to
Biological sensitivity to context: I 283
prosper irrespective of soil, sun, drought, or
rain. Observations of such children have gen-
erated, for example, an extensive developmen-
tal literature on the phenomenon of resilience,
the capacity for positive adaptation despite
experiences of significant adversity ~Luthar,
Doernberger, & Zigler, 1993; Masten, 2001!.
A contrasting Swedish neologism, orkide-
barn ~orchid child!, might better describe the
context-sensitive individual, whose survival
and flourishing is intimately tied, like that of
the orchid, to the nurturant or neglectful char-
acter of the ambient environment. In condi-
tions of neglect, the orchid promptly declines,
while in conditions of support and nurture, it
is a flower of unusual delicacy and beauty.
This metaphorical invocation of children
with contrasting environmental sensitivities is
reminiscent of Belsky’s ~1997, 2000!theory
of individual differences in susceptibility to
rearing influence. Belsky has proposed that
some individuals have traits and developmen-
tal trajectories that are more fixed by their
genetic endowment, while others are more
plastic and susceptible to rearing influence.
Employing an evolutionary framework, he sug-
gests that parents have been selected to “hedge
their bets” against an uncertain future by pro-
ducing both types of offspring: more fixed
types capable of achieving higher reproduc-
tive success in the particular ecological niche
that matches their genotype, and more plastic
types capable of fitting and thriving in a
wider range of niches, depending upon rear-
ing conditions encountered during ontogeny.
The latter, more malleable individuals are hy-
pothesized to monitor features of early child-
hood environments and to adjust biobehavioral
development accordingly. As summarized by
Belsky ~2000, 2005!, it is infants who are high
in negative emotional reactivity who appear
most susceptible to early rearing influences.
Although Belsky and the theoretical frame-
work presented here both equate heightened
reactivity with susceptibility to environmental
influence, and both theories posit that reactiv-
ity moderates relations between the quality of
early family environments and salient devel-
opmental outcomes, the theories differ in their
definitions of reactivity and their conceptual-
izations of its origins and consequences. First,
the current theory defines BSC as heightened
reactivity in one or more of the neurobiologi-
cal stress response systems, whereas Belsky
operationalizes reactivity at the behavioral
level. Comparisons between biological and be-
havioral reactivity have yielded inconsistent
results ~Kagan, 1994; Quas, Hong, Alkon, &
Boyce, 2000!, and are in need of further clar-
ification and study. Second, the current theory
specifies a conditional adaptation model of
the developmental origins of BSC, emphasiz-
ing gene–environment interactions. Belsky, by
contrast, focuses on heritable variation in sus-
ceptibility to rearing influence and does not
specify environmental antecedents of this vari-
ation. Third, the current theory conceptualizes
highly reactive phenotypes as orchidebarnen,
which are pointedly not adaptable to a broad
range of rearing milieus, but tend to do espe-
cially well in conditions of high social re-
sources and support. Belsky, by contrast,
conceptualizes emotionally reactive infants as
more developmentally malleable and capable
of entraining biobehavioral development to fit
a relatively wide range of niches.
A substantial body of other work provides
a broad but reasonably consistent picture
of behavioral predispositions found among
context-sensitive, biologically reactive orchide-
barnen. The research of Kagan and colleagues,
for example, has documented the tendency for
behaviorally inhibited, shy children to share
particular psychobiological features reflect-
ing exaggerated activation of both peripheral
and central stress response circuitries ~Kagan,
1994, 1997; Snidman, Kagan, Riordan, &
Shannon, 1995!. In cohorts of infants and chil-
dren followed by Kagan and others, those dis-
playing shy or fearful behaviors in social or
novel situations were significantly more likely
to have low heart periods ~and thus high heart
rates!, diminished heart period variability, and
greater pupillary dilatation, reflecting sympa-
thetic activation and parasympathetic with-
drawal, as well as higher baseline and reactive
salivary cortisol levels, indicating heightened
adrenocortical activation ~Kagan, Reznick,
& Snidman, 1987, 1988; Reznick, Kagan,
Snidman, Gersten, Baak, & Rosenberg,
1986!. Other studies ~Calkins, Fox, & Mar-
shall, 1996; Fox, Rubin, Calkins, Marshall,
284 W. T. Boyce and B. J. Ellis
Coplan, Porges, Long, & Stewart, 1995;
Schmidt, Fox, Schulkin, & Gold, 1999!have
similarly revealed associations between behav-
ioral inhibition and high, stable heart rates,
elevated measures of cortisol secretion, and
increased acoustic startle responses. In addi-
tion, in a series of studies by Fox and col-
leagues ~Fox, 1991; Fox et al., 1995; Fox,
Henderson, Rubin, Calkins, & Schmidt, 2001!,
a pattern of asymmetrical, right frontal EEG
activation was described among shy children,
possibly signaling individual differences in pre-
frontal regulation of amygdalar and limbic fear
circuitry ~Davidson & Irwin, 1999!.
Further, associations noted between behav-
ioral inhibition and biological reactivity have
not been limited to human children; the re-
search of Suomi and colleagues at the NIH
Laboratory of Comparative Ethology has pro-
duced systematic evidence of upregulated
adrenocortical and autonomic responses to
challenge among the fearful, inhibited subsets
of several primate species ~Byrne & Suomi,
2002; Suomi, 1997!. Although associations be-
tween temperamental differences in inhibition
and aspects of central and peripheral stress
reactivity have been frequently documented,
negative results have also been reported ~Asen-
dorpf & Meier, 1993; Calkins & Fox, 1992!,
and there have been suggestions that other
developmental factors, such as mother–child
attachment, could play moderating roles in
such relations. Stevenson–Hinde and Mar-
shall ~1999!, for example, found the predicted
association between low inhibition and high
vagal ~or parasympathetic!tone only among
securely attached children, and Nachmias et al.
~1996!reported adrenocortical reactivity in
novel coping conditions only for toddlers with
both behavioral inhibition and insecure attach-
ment. As reviewed by Fox and Card ~1999!
and Carter ~1998!, studies examining attach-
ment, mother–child behavior, and psychophys-
iological processes have met with varying and
sometimes contradictory results. Given the
known neuroendocrine correlates of social
bonding behavior in lower mammals, how-
ever, such relations remain a promising and
understudied area of investigation. More gen-
erally, the findings noted above indicate asso-
ciations of moderate magnitude between
BSC and behavioral inhibition and suggest
the possibility that the character of parent–
child relationships could constrain or modify
the emergence of high reactivity–high inhibi-
tion phenotypes.
Anotherliterature closely relatedto the con-
struct of context sensitivity, whether by anal-
ogyor, moredirectly,byits status as apotential
neurobiologicalsubstrate, is abody of workad-
dressing neurosensory “gating.” Operational-
ized as attenuations in either the component
amplitudes within auditory event-related po-
tentials or in the capacity for prepulse inhibi-
sensorygating is acomplex, multifaceted
neural function thought to protect higher cor-
ticalcenters from being floodedwithincoming
sensory stimuli ~Boutros, Torello, Barker, Tu-
eting, Wu, & Nasrallah, 1995!, and is thus one
candidate modality by which “BSC” might be
instantiatedin thebrain circuitrythatcould plau-
sibly subserve such sensitivity. Deficits in gat-
ing the P50 wave component following paired
auditory signals have been found among pa-
tients with PTSD ~Neylan et al., 1999!and
schizophrenia ~Braff & Geyer, 1990!, and in
their first-degree relatives ~Waldo, Myles–
and similar deficits in prepulse inhibition have
been identified among boys with comorbid
Tourette syndrome and attention-deficit0
hyperactivitydisorder ~Castellanos, Fine,Kay-
sen, Marsh, Rapoport, & Hallett, 1996!.A
variety of brain regions have been implicated
in the filtering of incoming sensory informa-
tion, including the temporal cortex ~Boutros
et al., 1995!, prefrontal cortex ~Shimamura,
2000!andthalamus ~McCormick&Bal, 1994!.
Potential linkages between sensory gating
deficitsand dysregulationin stressresponsesys-
tems are found in observations that glucocor-
ticoids~Stevens, Bullock, &Collins, 2001!and
catecholamines~Adler,Pang, Gerhardt,&Rose,
1988!are capable of disrupting gating func-
tions, that impairments in gating are found
among clinical populations with stress-related
disorders ~Neylan et al., 1999!, and that labo-
ratory protocols used for the induction of car-
1. Prepulse inhibition is the inhibition of an acoustic star-
tle response by a weaker stimulus presented just be-
fore the auditory probe.
Biological sensitivity to context: I 285
diovascular reactivity, such as the cold pressor
test, also diminish auditory gating ~Johnson &
Adler, 1993!. BSC, evoked and measured as
autonomicor adrenocortical reactivity to chal-
lenges in laboratory paradigms, thus appears
to have analogous expressions in neural path-
ways involved in sensory gating.
Personality and BSC
Individualdifferencesrelevantto BSChave also
receivedconsiderableattention from personal-
ity researchers interested in the neurobiologi-
calbases ofpersonality.Ofparticularrelevance
is the personality construct of reactivity ~Stre-
lau, 1983!, which indexes relatively stable in-
dividual differences in the intensity ~or
magnitude!of response to stimulation. Higher
reactivity indicates less gating of internal in-
formation stemming from external events, and
morereactive individuals arethereforesuscep-
tible to relatively weak environmental signals,
have comparatively low optimal levels of
arousal, and are less able than others to endure
strongstimulation forprolongedperiods oftime
~Kohn, 1991; Strelau, 1983!. Variation in re-
activityis, moreover,acommon,underlyingele-
mentof many biologicallyorientedpersonality
traits. Specifically, high “reactivity” individ-
uals, “introverts,” “augmenters,” and “sensa-
tion avoiders” all tend to avoid situations and
activities that involve strong stimulation and
arousal, whereas low “reactivity” individuals,
“extraverts,” “reducers,” and “sensation seek-
ers” are all predisposed to pursue such situa-
tionsand activities ~Strelau & Eysenck, 1987!.
Forexample, individuals on the reactive endof
these personality traits tend to seek out quieter
study rooms in libraries ~Campbell & Hawley,
1982!and reside in less stimulating suburban
neighborhoods~Strelau, 1983!; setvolumelev-
els lower when listening to music ~Davis,
Cowles, & Kohn, 1984; Kohn, Hunt, Cowles,
& Davis, 1986!or performing a learning task
~Geen, 1984!; choose hobbies and professions
that involve relatively low levels of stimula-
tion~Strelau, 1983;Zuckerman,1984!; anddis-
play lower tolerance for pain and discomfort
~Kohn, 1991!.
Paralleling BSC, a central feature of Stre-
lau’s concept of reactivity is susceptibility to
environmental influence. Compared with lower
reactivity individuals, those with higher reac-
tivity profiles are more adversely affected by
environmental stressors and distractions when
performing learning and decision-making tasks
~Eliasz, 1987; Klonowicz, 1987; Strelau, 1983!
and appear more susceptible to social pressure
in conformity experiments ~Eliasz, 1987!.
Moreover, unless intense or prolonged stimuli
are used, highly reactive people tend to de-
velop conditioned responses more easily and
quickly than do their peers with less reactive
profiles ~Strelau, 1983!.
Aron and Aron ~1997, p. 362!provide an
important further elucidation of the reactivity
construct in their discussion of sensory-
processing sensitivity and suggest that “there
is an underlying differentiating characteristic
regarding how some individuals process stim-
uli, involving a greater sensory-processing
sensitivity, reflectivity, and arousability.” An-
ticipated by early investigators noting ex-
ceptional sensitivities in young children
~Bergman & Escalona, 1949!, Aron and Aron
posit that individuals high in sensory-
processing sensitivity tend to be more atten-
tive, discriminating, and reflective, especially
as the complexity of incoming stimuli in-
creases. Linked to both conscientiousness and
low impulsivity, sensory-processing sensitiv-
ity may function as a “pause and check” sys-
tem that results in temporary inhibition of
activity ~Aron & Aron, 1997!and increases
susceptibility to environmental influence. This
increased susceptibility has been suggested
by a series of retrospective studies showing
that, for at least men, sensory-processing sen-
sitivity moderates the relation between the
quality of early family environments and child-
hood adjustment ~Aron & Aron, 1997!.
Complementing these retrospective stud-
ies, a number of prospective studies have now
documented a similar moderating role for
context sensitivity ~as indexed by negative
emotional reactivity in infants!in associations
between family environment and child behav-
ioral outcomes ~reviewed in Belsky, 2000,
2005!. Specifically, links between quality of
parenting and indices of child adjustment have
been found to be reliably stronger among emo-
tionally reactive infants. For example, Kochan-
286 W. T. Boyce and B. J. Ellis
ska ~1993, 1997!has found much larger effects
of maternal discipline ~e.g., reliance on gentle
guidance vs. forceful control!on develop-
ment of self-control among infants and tod-
dlers who are high in fearfulness and negative
emotionality than among those who are low
on these traits ~see also Feldman, Greenbaum,
& Yirmiya, 1999!. Similar moderating effects
of infant negative emotionality have also been
documented in the relations between quality
of parenting and the development of both ex-
ternalizing and internalizing behavior prob-
lems ~Belsky, Hsieh, & Crnic, 1998; Blair,
2002; Deater–Decker & Dodge, 1997!. Bel-
sky ~1997, 2005!has argued convincingly that
these interactions provide evidence of greater
susceptibility to rearing influence among tem-
peramentally reactive children.
High susceptibility to environmental influ-
ence implies that the personality development
of reactive children will be especially context
dependent, and the multidimensional systems
ofpersonality advancedbyEysenck ~e.g.,1967;
Eysenck& Eysenck,1985!and Gray~e.g., 1982,
1990!provide a framework for conceptualiz-
ing this context dependency ~see Figure 2!.
Eysenck specifies introversion versus extra-
version and neuroticism versus emotional sta-
bility as major dimensions of personality and
locatesthem atrightangles toeachother intwo-
dimensionalspace. Gray,by contrast, specifies
anxiety and impulsivity as major dimensions
ofpersonality.AlthoughGray alsolocatesthese
dimensions at right angles from each other,
herotates them approximately 30 ~conceptual!
degreesawayfromEysenck’s introversionand
neuroticism dimensions ~see Figure 2!. Thus,
in Gray’s system, individuals who are both
neuroticand somewhatintrovertedareregarded
as most anxious, whereas individuals who are
both introverted and fairly emotionally stable
are viewed as least impulsive. Given that in-
reactivityto moderatelevels ofstimulation ~Bul-
lock& Gilliland,1993;Taub,1998!,andshould
thus reflect sensitivity to context, the process
through which temperamental differences
in introversion in children ~often labeled
shyness or inhibition!develop into stable indi-
vidual differences in personality should be es-
pecially sensitive to the quality of family
environments.Under conditionsof familystress,
characterized by harsh, insensitive, and0or in-
consistent parenting, the position of relatively
shy,inhibitedchildren~highintroversion inFig-
ure 2!may be developmentally rotated to the
right toward high anxiety; conversely, under
conditions of family support characterized by
sensitive and responsive parenting, the posi-
tion of such children may be developmentally
rotated to the left toward low impulsivity ~see
Figure 2!.
Figure 2. The relation between Eysenck’s dimensions of extraversion and neuroticism and Gray’s
dimensions of impulsivity and anxiety.
Biological sensitivity to context: I 287
Thistheoretical positionis supported byclus-
teranalyses conductedbyAron andAron ~1997!
on individuals high in sensory-processing sen-
sitivity. In analysis of three diverse samples,
two distinct clusters of highly sensitive people
consistentlyemerged.Onegroup hadmore trou-
bled childhoods and scored relatively high on
measuresof socialintroversion andfearfulness0
anxiety. The other group was more similar in
childhood adjustment and personality to those
who were not highly sensitive. Aron andAron,
who conceptualize sensory-processing sensi-
tivityas abasicdimension oftemperament, sug-
gestthat the developmentalimplications of this
dimension depend on environmental factors.
Based on their interviews with prototypically
high sensitivity people, Aron andAron ~1997,
p. 363!conclude: “Sensitive individuals from
home environments that support their temper-
ament seem quite successful in their lives and
adept at making their sensitivity an asset while
avoiding shyness or over-self-consciousness.”
An Evolutionary–Developmental Theory
of BSC
The framework constructed above provides
the theoretical groundwork for an alternative
explanatory account of the ontogeny and func-
tions of BSC, within an evolutionary model.
As reviewed above, there are enduring indi-
vidual differences in BSC; such differences
emerge from the coaction of genetic and envi-
ronmental influences; different BSC pheno-
types yield different costs and benefits in
different childhood environments; and individ-
ual differences in BSC are hypothesized to
constitute variations in susceptibility to envi-
ronmental influence.
What are the evolutionary origins of such
individual differences in BSC? One possibil-
ity is that this variation is simply random ~i.e.,
evolutionary noise!, much as differences be-
tween people in the length of their toes is
random, owing to selection-irrelevant genetic
variation, the random effects of sexual recom-
bination, and nonadaptive phenotypic plastic-
ity in response to experience. Such variation
could still be heritable, and somewhat predict-
able in response to environmental factors, but
would not be the product of natural selection
and would have had little bearing on fitness in
ancestral environments.
Another possibility is that variation in BSC
is adaptively patterned. If this were the case,
then different levels of BSC should produce
mean differences in survival and reproductive
outcomes when all individuals are constrained
to a single environment, but similar survival
andreproductive outcomeswhendifferent BSC
phenotypes are allowed to covary with salient
features of the environment ~i.e., when indi-
vidualswith differentreactivity profilescan em-
ploy strategies and inhabit niches that are
matched to those profiles; see Mealey, 2001!.
As cited above, a quasiexperimental study of
theeffects ofstressreactivity undervaryingen-
vironmentalconditions in rhesusmonkeys sug-
gested that individual differences in stress
reactivity may meet these criteria. Specifi-
cally, during a 6-month confinement period,
when behavioral strategies available to troop
members were severely curtailed, highly reac-
tivemonkeys suffereddramatically higher rates
of violent injuries than did their less reactive
peers ~Figure 1B!. In the free-ranging wooded
habitat, however, where a wide range of be-
havioral strategies could be employed, includ-
ing escape from conflict, highly reactive
monkeys suffered comparatively low rates of
violent injury.
The claim advanced here is that variation
in stress reactivity has been produced and main-
tained by natural selection, because differ-
ences in BSC reliably produced different fitness
outcomes in different childhood environ-
ments encountered over evolutionary history.
This functional model, which conceptualizes
individual differences in BSC as underlying
variation in susceptibility to features of the
social environment, both positive and nega-
tive, can be described by the following three
interrelated propositions:
1. As suggested by both the human and ani-
mal literature, individuals who experience
traumatic, high-stress environments in early
childhood tend to develop exaggerated
stress reactivity profiles. High-stress reac-
tivity in this context may function to in-
crease the overall capacity and readiness
of individuals to deal with the very real
288 W. T. Boyce and B. J. Ellis
dangers in their environment, even when
such a strategy results in chronic over-
arousal and associated sequelae. Gunnar
~1994!has suggested, for example, that
higher levels of both sympathetic and para-
sympathetic reactivity in inhibited chil-
dren cause lower thresholds for anticipating
threat in new, unfamiliar situations and sup-
port greater vigilance and wariness.
2. In addition to increasing awareness of and
sensitivity to threat, the stress response sys-
tems may also enable children to experi-
ence and absorb more fully the beneficial,
protective features of supportive, predict-
able environments. Reactive, sensitive chil-
dren have been found, for example, to be
more reflective and perhaps more con-
scious of self and environment ~Aron &
Aron, 1997; Kagan, Snidman, Zentner, &
Peterson, 1999; Lewis & Ramsay, 1997;
Patterson & Newman, 1993!. Biologically
reactive phenotypes should thus also en-
able children to flourish under stable and
nurturant low-stress environments and eco-
logical conditions, where they may partic-
ularly benefit from high levels of parental
3. The third, complementary assertion is that
low reactive phenotypes may have also been
favored by natural selection, because they
enabled children to cope more effectively
within the highly prevalent, moderate stress
environments encompassing the broad, nor-
mative range of familial and ecological
stressors. Low biological stress reactivity
may have served a protective function for
children in these environments, by way of
increased gating of the emotional signals
from chronic stressors, which allowed
greater resilience under difficult condi-
tions. These benefits of low reactivity, how-
ever, should be specific to conditions of
chronic, moderate level stress and threat,
and could pose liabilities under develop-
mental conditions characterized by either
very high or very low stress ~where heavy
gating could interfere with responsiveness
to the environment!.
Thus, phenotypic variation in biological
stress reactivity may be adaptively patterned;
that is, it may increase the capacity and ten-
dency of different individuals to respond adap-
tively to specific types of early childhood
This post hoc explanation of observed phe-
notypic variation in stress reactivity, however,
does not meet minimum standards of evolu-
tionaryepistemology~Ketelaar & Ellis, 2000!.
As Lakatos ~1970, 1978!has shown, it is rela-
tively easy to construct new explanations or to
tinker with old ones to accommodate what is
already known. Indeed, there are few empiri-
cal findings in psychology and medicine that,
after the fact, could not be claimed by multiple
theoriesas falling withintheirexplanatory pur-
view. A good evolutionary explanation must
thereforenotonlyaccount for known facts, but
also “stick its neck out” by predicting experi-
mental results that are not known in advance
~Ellis& Ketelaar,2000;Ketelaar& Ellis,2000!.
Inthe final sections of thispaper,we presentan
evolutionary theory of the developmental ori-
gins of BSC in children, which is based on the
conceptof “conditional adaptation,”and which
generates a novel hypothesis about environ-
mental sources of variation in stress reactivity.
Thishypothesisis then explored empirically in
the second paper of this sequence.
The concept of conditional adaptation
Over the last 2 decades, theory and research
in evolutionary biology has begun to acknowl-
edge that, in most species, single “best” strat-
egies for survival and reproduction are unlikely
to evolve ~Gangestad & Simpson, 2000; Gross,
1996!. This is because the best strategy var-
ies as a function of the physical, economic,
and social parameters of one’s environment
~Crawford & Anderson, 1989!, and thus a strat-
egy that promotes success in some environ-
mental contexts may lead to failure in others.
Selection pressures therefore tend to favor
adaptive phenotypic plasticity, the capacity
of a single genotype to produce a range
of phenotypes ~manifested in morphology,
physiology, and0or behavior!in response to
particular ecological conditions that recur-
rently influenced fitness during a species’
evolutionary history ~Belsky, Steinberg, &
Draper, 1991; Chisholm, 1999; Hrdy, 1999!.
Biological sensitivity to context: I 289
Importantly, the development of alternative
phenotypes is a nonrandom process; that is, it
is the outcome of a structured transaction be-
tween genes and environment that was shaped
by natural selection to increase the capacity
and tendency of individuals to track their de-
velopmental environments and adjust their
phenotypes accordingly.
Phenotypic plasticity is necessarily a con-
strained process. Although it would seem
advantageous for individuals to respond to
environmental changes quickly, appropri-
ately, and flexibly throughout their lives, high
levels of responsiveness are not always either
possible or desirable. Instead, for many phe-
notypic characteristics, individuals have been
selected to register particular features of their
childhood environments as a basis for entrain-
ing relevant developmental pathways early in
life. There are several reasons to expect early
entrainment. First, many complex adaptations
are “built” during development and cannot
be easily rebuilt when environments fluctuate.
For example, the neural and hormonal path-
ways underlying the stress response sys-
tems are set down and calibrated during the
early years of development, when the plastic-
ity of neural circuits and structures is at its
zenith ~Davidson et al., 2000!. Second, pro-
longed practice and attention is required for
the successful execution of many behavioral
strategies ~Draper & Harpending, 1982!. For
example, individuals who pursue an early and
stable life strategy of predatory social inter-
actions ~i.e., primary sociopathy!are gener-
ally better at executing social deception than
individuals who contingently adopt this life
strategyat alater age~i.e., secondarysociopathy;
seeMealey,1995!. Third, extrememalleability
ofpersonality in responseto environmental cir-
cumstances is not plausible, because different
personalitysystems compete andinterferewith
each other. For example, high levels of the Big
Five Factor Agreeableness, which underlies
variationin theextentto whichindividualsseek
out and enjoy intimate, committed relation-
ships ~MacDonald, 1995!, would surely inter-
ferewith sociopathy.Indeed,the socialemotions
characteristicof individuals highinAgreeable-
ness ~e.g., love, compassion, empathy!are es-
sentially absent in sociopaths ~Mealey, 1995!.
Although the developmental pathways un-
derlying many phenotypic characteristics are
likely to be entrained early in life, a capacity
for responding to immediate contingencies is
also important. As Richard Alexander notes:
“It would be the worst of all strategies to enter
the competition and cooperativeness of social
life, in which others are prepared to alter their
responses, with only pre-programmed behav-
iors” ~cited in Mealey, 2000, p. 59!. Selection
should therefore favor a hierarchy of mecha-
nisms for tracking and responding to environ-
mental information ~Slobodkin & Rapoport,
1974; but see also Chisholm, 1999!. At the top
of this hierarchy are psychological mecha-
nisms underlying general and social intelli-
gence. These mechanisms enable quick and
flexible responses to changing opportunities
and threats in the immediate environment.
Lower in the hierarchy are anatomical, phys-
iological, endocrine, and developmental mech-
anisms, which track slower and more pervasive
changes in the environment. These mecha-
nisms often take the form of conditional ad-
aptations: that is, evolved mechanisms that
detect and respond to specific features of child-
hood environments, features that have proven
reliable over evolutionary time in predicting
the nature of the social and physical world
into which children will mature, and entrain
developmental pathways that reliably matched
those features during a species’ natural selec-
tive history. Conditional adaptations, which
reflect systematic gene–environment inter-
actions, underpin development of contingent
survival and reproductive strategies and thus
enable individuals to function competently in
a variety of different environments.
Illustrations of conditional adaptation
There are myriad examples of conditional ad-
aptation found in the natural world. Although
the best examples are found in plants, insects,
and fish, there are good mammalian examples,
as well, and emerging evidence in humans.
Environmentally triggered polymorphism in
caterpillars. The caterpillar Nemoria ari-
zonaria develops almost completely different
morphologies depending upon its diet in the
first 3 days of life ~Greene, 1989, 1996!. These
290 W. T. Boyce and B. J. Ellis
caterpillars inhabit oak woodlands in the Amer-
ican Southwest and produce both spring and
summer broods. Although the two broods have
the same appearance when they first hatch,
the spring brood feeds on oak catkins and
develops the appearance of the oak’s drooping
flowers, whereas the summer brood feeds on
oak leaves and develops the appearance of
twigs. The flower morphology enables the
spring brood to blend into the environment
while feeding on the ubiquitous spring catkins.
Likewise, the twig morph provides camou-
flage for the leaf-eating summer brood. If
either the spring or summer broods are ex-
perimentally fed out-of-season food, they
develop the corresponding out-of-season mor-
phology and become highly vulnerable to
predation. These caterpillars have therefore
evolved physiological mechanisms that regis-
ter features of diet in the first 3 days of life
and activate alternative developmental path-
ways, which function to match the organism’s
morphology to its feeding ecology ~see Greene,
1989, 1996!.
Weaning effects on play behavior in kittens.
Nursing cats on restricted diets wean their off-
spring early. Kittens respond to early weaning
by engaging in significantly more object play,
but not more social play, compared to normal
controls ~Bateson, Mendl, & Feaver, 1990!.
Although early weaning does not affect over-
all levels of play, it does change the quality of
play toward a more object-oriented form. Dur-
ing the cat’s natural selective history, early
weaning would have been reliably associated
with environments where food was scarce, ma-
ternal nurturance was limited, and young cats
were required to hunt for themselves at a rel-
atively early age. Object play is especially
important in the development of hunting skills
in cats, and high rates of object play prepare
kittens to hunt at an earlier age. Bateson et al.
~1990, p. 524!conclude “It seems likely that,
by responding to cues from the mother, the
individual animal is able to move along a de-
velopmental route that is appropriate to the
conditions it will encounter in later life.” Thus,
kittens appear to have evolved mechanisms
for registering information about maternal feed-
ing as a basis for upregulating the develop-
ment of motivational systems involved in
object play.
Paternal investment and development of fe-
male reproductive strategies. Draper and
Harpending ~1982, 1988!together with Bel-
sky et al. ~1991!have proposed a conditional
adaptation theory of adolescent sexual devel-
opment. Drawing on the concept of sensitive-
period learning, the theory posits that the
physiological and motivational systems under-
lying variation in timing of girls’ sexual de-
velopment are especially sensitive to the
father’s role in the family in approximately
the first 5 years of life. Specifically, experi-
ences associated with early father absence and
father–daughter distance are hypothesized to
entrain the development of reproductive strat-
egies that are matched to the social niche into
which the daughter was born, a niche in which
male parental investment is relatively unreli-
able and unimportant. Girls in this context are
predicted to develop in a manner that speeds
rates of pubertal maturation, accelerates onset
of sexual activity, and orients the individual
toward relatively unstable pair bonds. Con-
versely, experiences associated with early fa-
ther presence and father–daughter closeness
are hypothesized to entrain the opposite pat-
tern of sexual development. Either way, the
girl “chooses” a developmental trajectory that,
in the adult social environment into which she
was born, was likely to have promoted repro-
ductive success during human evolutionary
There is now a substantial body of empiri-
cal data that are consistent with this theory.
Specifically, studies in the United States
~Doughty & Rodgers, 2000; Ellis & Garber,
2000; Ellis, McFadyen–Ketchum, Dodge, Pet-
tit, & Bates, 1999!, Canada ~Surbey!, New
Zealand ~Moffitt, Caspi, Belsky, & Silva,
1992!, and Australia ~Jones, Leeton, McLeod,
& Wood, 1972!have all found that girls from
homes where the fathers are absent tend to
experience earlier pubertal development than
girls from homes where the fathers are present.
In addition, Ellis et al. ~1999!presented lon-
gitudinal data showing that girls who had more
distant relationships with their fathers during
the first 5 years of life experienced earlier
Biological sensitivity to context: I 291
pubertal development, and in studies in the
United States and New Zealand, early onset of
father absence has been found to have a dra-
matic effect on rates of early sexual activity
and teenage pregnancy ~Ellis, Bates, Dodge,
Fergusson, Horwood, Pettit, & Woodward,
2003!. It is important to acknowledge that the
apparent effects of father absence and other
experiences within families on developmental
endpoints, such as pubertal timing, could also
be a consequence of genetic influences on both.
Comings, Muhleman, Johnson, and MacMur-
ray ~2002!, for example, have shown that a
variant of the X-linked androgen receptor gene
is associated both with paternal divorce and
father absence in males and with early menar-
che and early sexual activity in females. Taken
together, the cited findings support the plau-
sibility of both experiential and genetic ac-
counts for associations between father absence
and the development of precocious reproduc-
tive strategies ~reviewed in Ellis, 2004!.
A conditional adaptation theory of BSC
The present theory posits that natural selec-
tion has favored developmental mechanisms
~conditional adaptations!that function to ad-
just levels of BSC to match familial and eco-
logical conditions encountered early in life.
Just as the timing of girls’ sexual development
may be sensitive to paternal investment, indi-
vidual differences in BSC may track specific
features of childhood environments. Specifi-
cally, humans may have evolved developmen-
tal mechanisms that detect and internally
encode information about levels of support-
iveness versus stressfulness in early child-
hood environments, as a basis for calibrating
the activation thresholds and response magni-
tudes within stress response systems to match
those environments.
Based on the claim that individual differ-
ences in stress reactivity constitute variation
in susceptibility to features of the social envi-
ronment, both positive and negative, the cur-
rent theory postulates a U-shaped, curvilinear
relationship between levels of supportiveness
versus stressfulness in early childhood envi-
ronments and the development of BSC ~see
Figure 3!. The right side of Figure 3 depicts
expected reactivity levels for individuals who
experience very high levels of stress in early
childhood. Consistent with the experimental
animal and epidemiologic human research
summarized above, these individuals are hy-
pothesized to develop heightened reactivity
profiles. We do not, however, expect reactiv-
ity to decline monotonically with decreasing
childhood stress. The left side of Figure 3
shows predicted reactivity levels for individ-
uals whose early childhoods are characterized
by intensive, stable caregiving and family sup-
port. These individuals are also hypothesized
to develop exaggerated reactivity profiles,
which function in this context to garner the
health and survival benefits of highly support-
ive rearing environments. Finally, the middle
of Figure 3 reflects the anticipated, relatively
muted reactivity profiles of individuals whose
early childhood experiences are characterized
by moderate levels of ongoing stress and threat.
These individuals, occupying the broad, nor-
mative range of species-typical contextual
stressors, are hypothesized to develop compar-
atively low reactivity profiles as a way of gat-
ing or filtering highly prevalent, moderate level
For the present purposes of sim-
2. Note that we are not claiming that moderate level
stressors result in extremely low reactivity or biologi-
cal insensitivity to context. Rather, “low reactivity”
here refers to low to moderate levels of biological
response, relative to the high reactivity individuals
we predict would be disproportionately represented in
very low and very high stress environments. Our
evolutionary–developmental theory of BSC is thus ag-
nostic with regard to the contextual origins of the
extremely low reactivity individuals examined, for ex-
ample, in the work of Raine et al. ~1997!.
3. Of possible but uncertain interest is the commonality
between the hypothesized quadratic association be-
tween early adversities and BSC and the historical ob-
servations of an inverted U-shaped relation between
arousaland performance~Yerkes&Dodson, 1908!.Al-
though the former hypothesis addresses the experien-
tialoriginsof biologicalreactivity,thelatter observation
describes its consequences within cognitive function-
ing. The Yerkes–Dodson association has been con-
tested in recent years ~Neiss, 1988!, and the construct
of“arousal” maybe onlydistantly allied to reactivity or
BSC. Nonetheless, future theoretical and0or empirical
work might benefit from a deeper examination of how
the two phenomena may be linked or related.
292 W. T. Boyce and B. J. Ellis
plicity and tractability, we further suggest that
this curvilinear, quadratic association with early
adversity will hold for reactivity in both the
LC-NE and CRH systems, acknowledging
that far greater complexity in the interplay
and balancing of the two stress response sys-
tems will likely surface as these relations are
Although the U-shaped curve depicted in
Figure 3 specifies environmental sources of
variation in BSC, genetic sources of varia-
tion and gene–environment interactions are
also important and need to be addressed in a
comprehensive theory of BSC. Children who
are genetically disposed toward high reactiv-
ity, for example, may alter levels of stress
and support in their home environments in
ways that further increase BSC. Children may
also differ in the location of reaction norms
underlying the spectrum of variation in BSC.
A reaction norm is a genetically inherited con-
straint that specifies the range of phenotypes
that will be produced by a genotype in differ-
ent environmental contexts ~Schlichting &
Pigliucci, 1998!. Given equivalent life expe-
riences, children with reaction norms that are
located on the upper end of the BSC spec-
trum should be more likely to develop highly
reactive phenotypes than children with reac-
tion norms on the lower end of the spectrum,
and vice versa. In addition, children may dif-
fer in the breadth of reaction norms. That is,
genotypes can be expected to differ in the
extent to which they are capable of produc-
ing a range of different BSC phenotypes
~cf. Belsky, 2005!, even given comparable on-
togenetic histories. The current evolutionary–
development model should be more successful
in accounting for the development of individ-
ual differences in BSC among children with
wider reaction norms. Finally, consistent with
the principle of “equifinality” ~von Bertalan-
ffy, 1968!, we expect that the effects of dif-
ferent BSC phenotypes on child health and
adjustment will be equivalent, regardless of
whether a child develops a given phenotype
primarily as a result of a narrow reaction norm
or as a result of particular childhood experi-
ences operating within a relatively broad re-
action norm.
Developmental mechanisms for adjusting
BSC in response to early childhood experi-
ences may have resulted from a long and re-
current evolutionary history in which ~a!
Figure 3. The hyopthesized curvilinear relation of biologic reactivity to early stress and adversity.
Comparisons of subjects at points Aand B would result in a conclusion that early adversity is associated
with greater stress reactivity. Conversely, comparisons at points C and D would generate the inference
that early adversity produces diminished reactivity.
Biological sensitivity to context: I 293
different children confronted substantially dif-
ferent rearing environments; ~b!highly reac-
tive children experienced better survival and
reproductive outcomes, on average, in both
intensely stressful and highly supportive rear-
ing environments; and ~c!less reactive chil-
dren experienced generally better survival and
reproductive outcomes in developmental set-
tings characterized by moderate levels of stress
and threat. Such an account would reconcile
important contradictions, reviewed above, in
the existing literature on the origins and con-
sequences of stress reactivity in children. In-
vestigators comparing individuals from points
A and B in Figure 3, for example, would con-
clude, as have Yehuda ~2002!, De Bellis et al.
~1999!, and many others, that experiences of
family and environmental stress are associ-
ated with upregulatory calibrations in biolog-
ical reactivity systems. On the other hand,
studies comparing individuals from points C
and D would find, as have those reviewed by
Gunnar and Vazquez ~2001!and Heim, Ehrl-
ert, et al. ~2000!, that early stressors are rather
associated with downregulatory changes in sa-
lient biological responses. The current theory,
which posits two oppositionally distinctive on-
togenies for BSC, explains both of these up-
and downregulatory effects.
Our principal aim in the present paper has
been to articulate the precepts and rationale
for a new claim about the nature of relations
between early life experience and stress reac-
tivity, a claim that we further explore empiri-
cally in the companion paper, which follows.
The logic of the argument we have sought to
present can be summarized in the following
way. Biological reactivity to psychological
stressors consists of an elaborated, highly co-
ordinated, but phylogenetically primitive set
of neural and peripheral neuroendocrine re-
sponses, designed to ready the organism for
external challenges and threats to survival.
Standard explanations of such responses’ role
in the pathogenesis of human disorders sug-
gest that prolonged or exaggerated reactivity,
such as that seen in highly reactive biobehav-
ioral phenotypes, exerts deleterious and im-
pairing effects on a broad range of target
organs, including structures within the brain,
leading to decrements in health, cognition, and
functional capacities. Often overlooked in such
accounts is a body of anomalous observa-
tions, revealing oppositional, counterregula-
tory processes within the stress response
circuitry itself and, even more compellingly,
bivalent effects of reactivity on biomedical
and psychiatric outcomes. Highly reactive chil-
dren sustain disproportionate rates of morbid-
ity when raised in adverse environments but
unusually low rates when raised in low-stress,
highly supportive settings.
Such bidirectional, environment-dependent
health effects suggest that BSC is the core,
defining feature of highly reactive pheno-
types. These observations call into question
the presumably unitary pathogenic effects of
high reactivity and suggest that its protective
effects within specific developmental ecolo-
gies might explain the conservation of such
phenotypic variation within evolutionary his-
tory. Furthermore, conditional adaptations, in
which a single genotype supports a range of
environmentally contingent phenotypic expres-
sions, enable entrainment of biological and
behavioral development to adaptively match
early ~and predicted future!social environ-
ments. Given past evidence that early trauma
can evoke upregulatory changes in stress re-
activity and new evidence that high reactivity
can be protective in highly supportive set-
tings, we postulate a curvilinear, U-shaped re-
lation, shown in Figure 3, between levels of
early adversity and the magnitude of biologi-
cal response dispositions. Specifically, we hy-
pothesize that ~a!exposure to acutely stressful
childhood environments upregulates BSC, in-
creasing the capacity and tendency of individ-
uals to detect and respond to environmental
dangers and threats; ~b!exposure to exception-
ally supportive childhood environments also
upregulates BSC, increasing susceptibility to
the social and developmental benefits of such
environments; and ~c!typical of the large ma-
jority of children, exposure to childhood envi-
ronments that are extreme in neither direction
downregulates BSC, buffering individuals
against the chronic stressors encountered in a
294 W. T. Boyce and B. J. Ellis
world that is neither highly threatening nor
universally safe.
Because evolutionary “stories” of the kind
advanced here are especially vulnerable to the
perils of post hoc explanation, it is essential
that the current evolutionary–developmental
theory of the origins and functions of stress
reactivity be put eventually to rigorous tests
of its predictive strength. In the paper that
follows, we offer a provisional, “promissory
note” on such a requirement, by presenting
exploratory analyses from two studies, in geo-
graphically and culturally distinctive settings,
that produce empirical derivations of the same
hypothesis first advanced here on conceptual
grounds. Such convergence of theoretical and
empirical reasoning, we would argue, por-
tends well for the validity of the evolutionary–
developmental hypothesis. In the presentation
of its conceptual and analytical origins, it is
our hope that new knowledge concerning the
causes and consequences of children’s respon-
sivity to stress will be uncovered, and that
richer, more protective environments will be
fostered in which highly sensitive children can
develop and thrive.
Adler, L. E., Pang, K., Gerhardt, G., & Rose, G. M.
~1988!. Modulation of the gating of auditory evoked
potentials by norepinephrine: Pharmacological evi-
dence obtained using a selective neurotoxin. Biologi-
cal Psychiatry,24, 179–190.
Adler, P. S., & Ditto, B. ~1998!. Psychophysiological ef-
fects of interviews about emotional events on off-
spring of hypertensives and normotensives.
International Journal of Psychophysiology,28,
Alkon, A., Goldstein, L. H., Smider, N., Essex, M., Kupfer,
D., & Boyce, W. T. ~2003!. Developmental and con-
textual influences on autonomic reactivity in young
children. Developmental Psychobiology,42, 64–78.
Allen, M. T., & Matthews, K.A. ~1997!. Hemodynamic
responses to laboratory stressors in children and ado-
lescents: The influences of age, race, and gender. Psy-
chophysiology,34, 329–339. @erratum p. 730#
Aron, E. N., & Aron,A. ~1997!. Sensory-processing sen-
sitivity and its relation to introversion and emotional-
ity. Journal of Personality and Social Psychology,73,
Asendorpf, J. B., & Meier, G. H. ~1993!. Personality ef-
fects on children’s speech in everyday life: Sociability-
mediated exposure and shyness-mediated reactivity
to social situations. Journal of Personality and Social
Psychology,64, 1072–1083.
Aston–Jones, G., Rajkowski, J., Kubiak, P., Valentino,
R. J., & Shipley, M. T. ~1996!. Role of the locus
coeruleus in emotional activation. Progress in Brain
Research,107, 379–402.
Bartels, M., de Geus, E. J., Kirschbaum, C., Sluyter, F., &
Boomsma, D. I. ~2003!. Heritability of daytime corti-
sol levels in children. Behavior Genetics,33, 421–433.
Bateson, P. P. G., Mendl, M., & Feaver, J. ~1990!. Play in
the domestic cat is enhanced by rationing of the mother
during lactation. Animal Behaviour,40, 514–525.
Bauer,A. S. ~2002!.Concurrent sympathetic and adreno-
cortical activity as correlates of behavior in middle
childhood. Unpublished master’s thesis, University of
California, Berkeley.
Belsky, J. ~1997!. Variation in susceptibility to environ-
mental influence: An evolutionary argument. Psycho-
logical Inquiry,8, 182–186.
Belsky, J. ~2000!. Conditional and alternative reproduc-
tive strategies: Individual differences in susceptiblity
to rearing experiences. In J. L. Rodgers, D. C. Rowe
& W. B. Miller ~Eds.!,Genetic influences on human
fertility and sexuality: Theoretical and empirical
contributions from the biological and behavioral sci-
ences ~pp. 127–145!. Boston: Kluwer Academic.
Belsky, J. ~2005!. Differential susceptibility to rearing
influence: An evolutionary hypothesis and some evi-
dence. In B. J. Ellis & D. F. Bjorklund ~Eds.!,Origins
of the social mind: Evolutionary psychology and child
development ~pp. 139–163!. New York: Guilford Press.
Belsky, J., Hsieh, K., & Crnic, K. ~1998!. Mothering,
fathering, and infant negativity as antecedents of boys’
externalizing problems and inhibition at age 3: Differ-
ential susceptibility to rearing influence? Develop-
ment and Psychopathology,10, 301–319.
Belsky, J., Steinberg, L., & Draper, P. ~1991!. Childhood
experience, interpersonal development, and reproduc-
tive strategy: An evolutionary theory of socialization.
Child Development,62, 647–670.
Benediktsson, R., Lindsay, R. S., Noble, J., Seckl, J. R., &
Edwards, C. R. ~1993!. Glucocorticoid exposure in
utero: New model for adult hypertension. Lancet,
341~8841!, 339–341.
Bentley, P. J. ~1998!.Comparative vertebrate endocrinol-
ogy. Cambridge: Cambridge University Press.
Bergman, P., & Escalona, S. K. ~1949!. Unusual sensitiv-
ities in very young children. Pschoanalytic Studies of
the Child,4, 333–352.
Bernard, C. ~1878!.Les phenomenes de la vie. Paris:
Blair, C. ~2002!. Early intervention for low birth weight
preterm infants: The role of negative emotionality in
the specification of effects. Development and Psycho-
pathology,14, 311–332.
Bloom, F. E., & Kupfer, D. J. ~1995!.Psychopharmacol-
ogy ~4th ed.!. New York: Raven Press.
Boutros, N. N., Torello, M. W., Barker, B. A., Tueting,
P. A., Wu, S. C., & Nasrallah, H. A. ~1995!. The P50
evoked potential component and mismatch detection
in normal volunteers: Implications for the study of
sensory gating. Psychiatry Research,57, 83–88.
Boyce, W. T. ~1996!. Biobehavioral reactivity and inju-
ries in children and adolescents. In M. H. Bornstein &
J. Genevro ~Eds.!,Child development and behavioral
pediatrics: Toward understanding children and health.
Mahwah, NJ: Erlbaum.
Biological sensitivity to context: I 295
Boyce, W. T., Champoux, M., Suomi, S. J., & Gunnar,
M. R. ~1995!. Salivary cortisol in nursery-reared rhe-
sus monkeys: Reactivity to peer interactions and al-
tered circadian activity. Developmental Psychobiology,
28, 257–267.
Boyce, W. T., Chesney, M., Alkon–Leonard, A., Tschann,
J., Adams, S., Chesterman, B., Cohen, F., Kaiser, P.,
Folkman, S., & Wara, D. ~1995!. Psychobiologic re-
activity to stress and childhood respiratory illnesses:
Results of two prospective studies. Psychosomatic
Medicine,57, 411–422.
Boyce, W. T., O’Neill–Wagner, P., Price, C. S., Haines,
M., & Suomi, S. J. ~1998!. Crowding stress and vio-
lent injuries among behaviorally inhibited rhesus ma-
caques. Health Psychology,17, 285–289.
Boyce, W. T., Quas, J., Alkon, A., Smider, N., Essex, M.,
& Kupfer, D. J. ~2001!. Autonomic reactivity and psy-
chopathology in middle childhood. British Journal of
Psychiatry,179, 144–150.
Braff, D. L., & Geyer, M.A. ~1990!. Sensorimotor gating
and schizophrenia. Human and animal model studies.
Archives of General Psychiatry,47, 181–188.
Bremner, J. D., & Vermetten, E. ~2001!. Stress and devel-
opment: Behavioral and biological consequences. De-
velopment and Psychopathology,13, 473–489.
Bullock, W. A., & Gilliland, K. ~1993!. Eysenck’s arousal
theory of introversion–extraversion: A converging mea-
sures investigation. Journal of Personality and Social
Psychology,64, 113–123.
Busjahn, A., Faulhaber, H. D., Viken, R. J., Rose, R. J., &
Luft, F. C. ~1996!. Genetic influences on blood pres-
sure with the cold-pressor test: Atwin study. Journal
of Hypertension,14~10!, 1195–1199.
Byrne, G., & Suomi, S. J. ~2002!. Cortisol reactivity and
its relation to homecage behavior and personality rat-
ings in tufted capuchin ~Cebus apella!juveniles from
birth to six years of age. Psychoneuroendocrinology,
27~1–2!, 139–154.
Cacioppo, J. T., Berntson, G. G., Malarkey, W. B., Kiecolt–
Glaser, J. K., Sheridan, J. F., Poehlmann, K. M., Bur-
leson, M. H., Ernst, J. M., Hawkley, L. C., & Glaser,
R. ~1998!. Autonomic, neuroendocrine, and immune
responses to psychological stress: The reactivity hy-
pothesis. Annals of the New York Academy of Sci-
ences,840, 664– 673.
Cacioppo, J. T., Berntson, G. G., Sheridan, J. F., &
McClintock, M. K. ~2000!. Multilevel integrative
analyses of human behavior: Social neuroscience
and the complementing nature of social and bio-
logical approaches. Psychological Bulletin,126,
Calkins, S. D., & Fox, N. A. ~1992!. The relations among
infant temperament, security of attachment, and be-
havioral inhibition at twenty-four months. Child De-
velopment,63, 1456–1472.
Calkins, S. D., Fox, N. A., & Marshall, T. R. ~1996!.
Behavioral and physiological antecedents of inhibited
and uninhibited behavior. Child Development,67,
Campbell, J. B., & Hawley, C. W. ~1982!. Study habits
and Eysenck’s theory of extraversion–introversion.
Journal of Research in Personality,16, 139–146.
Cannon, W. B. ~1929!.Bodily changes in pain,hunger,
fear and rage. New York: Appleton.
Carlson, M., & Earls, F. ~1997!. Psychological and neuro-
endocrinological sequelae of early social deprivation
in institutionalized children in Romania. Annals of the
New YorkAcademy of Sciences,807, 419– 428.
Carter, C. S. ~1998!. Neuroendocrine perspectives on so-
cial attachment and love. Psychoneuroendocrinology,
23, 779–818.
Castellanos, F. X., Fine, E. J., Kaysen, D., Marsh, W. L.,
Rapoport, J. L., & Hallett, M. ~1996!. Sensorimotor
gating in boys with Tourette’s syndrome and ADHD:
Preliminary results. Biological Psychiatry,39, 33– 41.
Champagne, F., & Meaney, M. J. ~2001!. Like mother,
like daughter: Evidence for non-genomic transmis-
sion of parental behavior and stress responsivity.
Progress in Brain Research,133, 287–302.
Champoux, M., Higley, J. D., & Suomi, S. J. ~1997!.
Behavioral and physiological characteristics of Indian
and Chinese–Indian hybrid rhesus macaque infants.
Developmental Psychobiology,31, 49–63.
Champoux, M., Hwang, L., Lang, O., & Levine, S. ~2001!.
Feeding demand conditions and plasma cortisol in
socially-housed squirrel monkey mother–infant dy-
ads. Psychoneuroendocrinology,26, 461–477.
Champoux, M., & Suomi, S. J. ~1994!. Behavioral and
adrenocortical responses of rhesus macaque mothers
to infant separation in an unfamiliar environment. Pri-
mates,35, 191–202.
Cheng, L. S., Carmelli, D., Hunt, S. C., & Williams, R. R.
~1997!. Segregation analysis of cardiovascular reac-
tivity to laboratory stressors. Genetic Epidemiology,
14, 35–49.
Chesterman, E., Boyce, W. T., &Winkleby, M. A. ~1989!.
Psychosocial predictors of maternal and infant health:
A “sense of permanence” as a mediating variable
(Abstract). Paper presented at the Society of Behav-
ioral Medicine Annual Meeting, San Francisco.
Chisholm, J. S. ~1999!.Death, hope and sex: Steps to an
evolutionary ecology of mind and morality. New York:
Cambridge University Press.
Chrousos, G. P. ~1998!. Stressors, stress, and neuroendo-
crine integration of the adaptive response. The 1997
Hans Selye Memorial Lecture. Annals of the New
YorkAcademy of Sciences,851, 311–335.
Comings, D. E., Muhleman, D., Johnson, J. P., & Mac-
Murray, J. P. ~2002!. Parent–daughter transmission of
the androgen receptor gene as an explanation of the
effect of father absence on age of menarche. Child
Development,73, 1046–1051.
Coplan, J. D., Andrews, M. W., Rosenblum, L. A., Owens,
M. J., Friedman, S., Gorman, J. M., & Nemeroff, C. B.
~1996!. Persistent elevations of cerebrospinal fluid
concentrations of corticotropin-releasing factor in adult
nonhuman primates exposed to early-life stressors:
Implications for the pathophysiology of mood and
anxiety disorders. Proceedings of the National Acad-
emy of Sciences of the United States of America,93,
Cratty, M. S., Ward, H. E., Johnson, E. A., Azzaro,A. J.,
& Birkle, D. L. ~1995!. Prenatal stress increases corti-
cotropin-releasing factor ~CRF!content and release
in rat amygdala minces. Brain Research,675,
Crawford, C. B., & Anderson, J. L. ~1989!. Sociobiology:
An environmentalist discipline? American Psycholo-
gist,44, 1449–1459.
Dallman, M. F., Akana, S. F., Cascio, C. S., Darlington,
D. N., Jacobson, L., & Levin, N. ~1987!. Regulation
of ACTH secretion: Variations on a theme of B. Re-
cent Progress in Hormone Research,43, 113–173.
Davidson, R. J., & Irwin, W. ~1999!. The functional neuro-
anatomy of emotion and affective style. Trends in
Cognitive Sciences,3, 11–21.
296 W. T. Boyce and B. J. Ellis
Davidson, R. J., Jackson, D. C., & Kalin, N. H. ~2000!.
Emotion, plasticity, context, and regulation: Perspec-
tives from affective neuroscience. Psychological Bul-
letin,126, 890–909.
Davis, C., Cowles, M., & Kohn, P. ~1984!. Behavioural
and physiological aspects of the augmenting-reducing
dimension. Personality and Individual Differences,5,
Davis, E., Donzella, B., Krueger, W. K., & Gunnar, M. R.
~1999!. The start of a new school year: Individual
differences in salivary cortisol response in relation to
child temperament. Developmental Psychobiology,35,
Deater–Deckard, K., & Dodge, K. ~1997!. Spare the rod,
spoil the authors: Emerging themes in research on
parenting. Psychological Inquiry,8, 230–235.
De Bellis, M. D., Baum, A. S., Birmaher, B., Keshavan,
M. S., Eccard, C. H., Boring, A. M., Jenkins, F. J., &
Ryan, N. D. ~1999!. A.E. Bennett Research Award.
Developmental traumatology. Part I: Biological stress
systems. Biological Psychiatry,45, 1259–1270.
de Haan, M., Gunnar, M. R., Tout, K., Hart, J., & Stans-
bury, K. ~1998!. Familiar and novel contexts yield
different associations between cortisol and behavior
among 2-year-olds. Developmental Psychobiology,31,
Dhabhar, F. S., McEwen, B. S., & Spencer, R. L. ~1993!.
Stress response, adrenal steroid receptor levels and
corticosteroid-binding globulin levels—A compari-
son between Sprague–Dawley, Fischer 344 and Lewis
rats. Brain Research,616~1–2!, 89–98.
Doughty, D., & Rodgers, J. L. ~2000!. Behavior genetic
modeling of menarche in U.S. females. In J. L. Rod-
gers, D. C. Rowe, & W. B. Miller ~Eds.!,Genetic
influences on human fertility and sexuality: Theoreti-
cal and empirical contributions from the biological
and behavioral sciences. Boston: Kluwer Academic.
Draper, P., & Harpending, H. ~1982!. Father absence and
reproductive strategy: An evolutionary perspective.
Journal of Anthropological Research,38, 255–273.
Draper, P., & Harpending, H. ~1988!. A sociobiological
perspective on the development of human reproduc-
tive strategies. In K. B. MacDonald ~Ed.!,Sociobio-
logical perspectives on human development ~pp. 340–
372!. New York: Springer–Verlag.
Dubos, R. J. ~1965!.Man adapting. New Haven, CT: Yale
University Press.
Dunn, A. J., & Berridge, C. W. ~1990!. Physiological and
behavioral responses to corticotropin-releasing factor
administration: Is CRF a mediator of anxiety or stress
responses? Brain Research Reviews,15, 71–100.
Ekman, P., Levenson, R. W., & Friesen, W. V. ~1983!.
Autonomic nervous system activity distinguishes
among emotions. Science,221~4616!, 1208–1210.
Elenkov, I. J., & Chrousos, G. P. ~1999!. Stress hormones,
Th10Th2 patterns, pro0anti-inflammatory cytokines
and susceptibility to disease. Trends in Endocrinology
and Metabolism,10, 359–368.
Eliasz, A. ~1987!. Temperament-contingent cognitive ori-
entation toward various aspects of reality. In J. Strelau
& J. H. Eysenck ~Eds.!,Personality dimensions and
arousal. Perspectives on individual differences ~pp.
197–212!. New York: Plenum Press.
Ellis, B. J. ~2004!. Timing of pubertal maturation in girls:
An integrated life history approach. Psychological Bul-
letin,130, 920–958.
Ellis, B. J., Bates, J. E., Dodge, K. A., Fergusson, D.,
Horwood, J., Pettit, G. S., & Woodward, L. ~2003!.
Does early father absence place daughters at special
risk for early sexual activity and teenage pregnancy?
Child Development,74, 801–821.
Ellis, B. J., & Garber, J. ~2000!. Psychosocial antecedents
of variation in girls’ pubertal timing: Maternal depres-
sion, stepfather presence, and marital and family stress.
Child Development,71, 485–501.
Ellis, B. J., & Ketelaar, T. ~2000!. On the natural selection
of alternative models: Evaluation of explanations in
evolutionary psychology. Psychological Inquiry,11,
Ellis, B. J., McFadyen–Ketchum, S., Dodge, K. A., Pettit,
G. S., & Bates, J. E. ~1999!. Quality of early family
relationships and individual differences in the timing
of pubertal maturation in girls: A longitudinal test of
an evolutionary model. Journal of Personality & So-
cial Psychology,77, 387–401.
Essex, M. J., Klein, M. H., Cho, E., & Kalin, N. H.
~2002!. Maternal stress beginning in infancy may sen-
sitize children to later stress exposure: Effects on cor-
tisol and behavior. Biological Psychiatry,52, 776–784.
Eysenck, H. J. ~1967!.The biological basis of personal-
ity. Springfield, IL: Charles C. Thomas.
Eysenck, H. J., & Eysenck, M. W. ~1985!.Personality
and individual differences: A natural science ap-
proach. New York: Plenum Press.
Feldman, R., Greenbaum, C., & Yirmiya, N. ~1999!.
Mother–infant affect synchrony as an antecedent of
the emergence of self-control. Developmental Psychol-
ogy,35, 223–231.
Fernald, L. C., & Grantham–McGregor, S. M. ~1998!.
Stress response in school-age children who have been
growth retarded since early childhood. American Jour-
nal of Clinical Nutrition,68, 691–698.
Fox, N. A. ~1991!. If it’s not left, it’s right: Electroenceph-
alograph asymmetry and the development of emotion.
American Psychologist,46, 863–872.
Fox, N. A., & Card, J. A. ~1999!. Psychophysiological
measures in the study of attachment. In J. Cassidy &
P. R. Shaver ~Eds.!,Handbook of attachment: Theory,
research, and clinical applications ~pp. 226–245!. New
York: Guilford Press.
Fox,N. A., Henderson, H.A., Rubin, K. H.,Calkins, S. D.,
& Schmidt, L. A. ~2001!. Continuity and discontinuity
of behavioral inhibition and exuberance: Psychophys-
iologicaland behavioral influencesacross thefirst four
years of life. Child Development,72, 1–21.
Fox, N. A., Rubin, K. H., Calkins, S. D., Marshall, T. R.,
Coplan, R. J., Porges, S. W., Long, J. M., & Stewart,
S. ~1995!. Frontal activation asymmetry and social
competence at four years of age. Child Development,
66, 1770–1784.
Gangestad, S. W., & Simpson, J. A. ~2000!. The evolution
of human mating: Trade-offs and strategic pluralism.
Behavioral and Brain Sciences,23, 573–644.
Gannon, L., Banks, J., Shelton, D., & Luchetta, T. ~1989!.
The mediating effects of psychophysiological reactiv-
ity and recovery on the relationship between environ-
mental stress and illness. Journal of Psychosomatic
Medicine,33, 167–175.
Geen, R. ~1984!. Preferred stimulation levels in intro-
verts and extraverts: Effects on arousal and perfor-
mance. Journal of Personality and Social Psychology,
46, 1303–1312.
Goenjian, A. K., Yehuda, R., Pynoos, R. S., Steinberg,
A. M., Tashjian, M.,Yang, R. K., Najarian, L. M., &
Fairbanks, L. A. ~1996!. Basal cortisol, dexametha-
sone suppression of cortisol, and MHPG in adoles-
Biological sensitivity to context: I 297
cents after the 1988 earthquake in Armenia. American
Journal of Psychiatry,153, 929–934.
Gold, P. W., & Chrousos, G. P. ~1999!. The endocrinology
of melancholic and atypical depression: Relation to
neurocircuitry and somatic consequences. Proceed-
ings of the Association of American Physicians,111,
Gold, P. W., & Chrousos, G. P. ~2002!. Organization of
the stress system and its dysregulation in melancholic
and atypical depression: High vs low CRH0NE states.
Molecular Psychiatry,7, 254–275.
Gold, P. W., Goodwin, F. K., & Chrousos, G. P. ~1988!.
Clinical and biochemical manifestations of depres-
sion. Relation to the neurobiology of stress ~1!.New
England Journal of Medicine,319, 348–353.
Gray, J. A. ~1982!.Theneuropsychology of anxiety: Anen-
quiry into the functions of the septo-hippocampal sys-
tem. New York: Clarendon0Oxford University Press.
Gray, J. A. ~1990!. Brain systems that mediate both emo-
tion and cognition. Cognition and Emotion,4, 269–288.
Greene, E. ~1989!. A diet-induced developmental poly-
morphism in a caterpillar. Science,243, 643–646.
Greene, E. ~1996!. Effect of light quality and larval
diet on morph induction in the polymorphic caterpil-
lar Nemoria arizonaria ~Lepidoptera: Geometridae!.
Biological Journal of the Linnean Society,58,
Gross, M. R. ~1996!. Alternative reproductive strategies
and tactics: Diversity within sexes. Trends in Ecology
& Evolution,11, 92–98.
Gunnar, M. R. ~1994!. Psychoendocrine studies of tem-
perament and stress in early childhood: Expanding
current models. In J. E. Bates & T. D. Wachs ~Eds.!,
Temperament: Individual differences at the interface
of biology and behavior ~pp. 175–198!. Washington,
DC: American Psychological Association.
Gunnar, M. R., Morison, S. J., Chisholm, K., & Schuder,
M. ~2001!. Salivary cortisol levels in children adopted
from Romanian orphanages. Development and Psy-
chopathology,13, 611–628.
Gunnar, M. R., & Vazquez, D. M. ~2001!. Low cortisol
and a flattening of expected daytime rhythm: Poten-
tial indices of risk in human development. Develop-
ment and Psychopathology,13, 515–538.
Habib, K. E., Gold, P. W., & Chrousos, G. P. ~2001!.
Neuroendocrinology of stress. Neuroendocrinology,
30, 695–728.
Harlow, H. F., Harlow, M. K., & Suomi, S. J. ~1971!.
From thought to therapy: Lessons from a primate lab-
oratory. American Scientist,59, 538–549.
Heilig, M., Koob, G. F., Ekman, R., & Britton, K. T.
~1994!. Corticotropin-releasing factor and neuropep-
tide Y: Role in emotional integration. Trends in Neuro-
sciences,17, 80–85.
Heim, C., Ehlert, U., & Hellhammer, D. H. ~2000!. The
potential role of hypocortisolism in the pathophysiol-
ogy of stress-related bodily disorders. Psychoneuro-
endocrinology,25, 1–35.
Heim, C., & Nemeroff, C. B. ~1999!. The impact of early
adverse experiences on brain systems involved in the
pathophysiology of anxiety and affective disorders.
Biological Psychiatry,46, 1509–1522.
Heim, C., Newport, D. J., Heit, S., Graham,Y. P., Wilcox,
M., Bonsall, R., Miller, A. H., & Nemeroff, C. B.
~2000!. Pituitary–adrenal and autonomic responses to
stress in women after sexual and physical abuse in
childhood. Journal of the American Medical Associ-
ation,284, 592–597.
Hertsgaard, L., Gunnar, M. R., Erickson, M. F., & Nach-
mias, M. ~1995!. Adrenocortical responses to the
strange situation in infants with disorganized0
disoriented attachment relationships. Child Develop-
ment,66, 1100–1106.
Higley, J. D., & Linnoila, M. ~1997!. Low central nervous
system serotonergic activity is traitlike and correlates
with impulsive behavior.A nonhuman primate model
investigating genetic and environmental influences on
neurotransmission. Annals of the New York Academy
of Sciences,836, 39–56.
Higley, J. D., Thompson, W. W., Champoux, M., Gold-
man, D., Hasert, M. F., Kraemer, G. W., Scanlan,
J. M., Suomi, S. J., & Linnoila, M. ~1993!. Paternal
and maternal genetic and environmental contributions
to cerebrospinal fluid monoamine metabolites in rhe-
sus monkeys ~Macaca mulatta!.Archives of General
Psychiatry,50, 615–623.
Hofer, M. A. ~1994!. Early relationships as regulators of
infant physiology and behavior. Acta Paediatrica Sup-
plement,397, 9–18.
Holsboer, F., Lauer, C. J., Schreiber, W., & Krieg, J. C.
~1995!. Altered hypothalamic–pituitary–adrenocortical
regulation in healthy subjects at high familial risk for
affective disorders. Neuroendocrinology,62, 340–347.
Hrdy, S. B. ~1999!.Mother nature: Maternal instincts
and how they shape the human species. New York:
Ballantine Books.
Introini–Collison, I. B., Dalmaz, C., & McGaugh, J. L.
~1996!. Amygdala beta-noradrenergic influences on
memory storage involve cholinergic activation. Neuro-
biology, Learning and Memory,65, 57–64.
Issa, A. M., Rowe, W., Gauthier, S., & Meaney, M. J.
~1990!. Hypothalamic–pituitary–adrenal activity in
aged, cognitively impaired and cognitively unimpaired
rats. Journal of Neuroscience,10, 3247–3254.
Johnson, M. R., & Adler, L. E. ~1993!. Transient impair-
ment in P50 auditory sensory gating induced by a
cold-pressor test. Biological Psychiatry,33, 380–387.
Jones, B., Leeton, J., McLeod, I., & Wood, C. ~1972!.
Factors influencing the age of menarche in a lower
socioeconomic group in Melbourne. Medical Journal
of Australia,2, 533–535.
Kagan, J. ~1994!.Galen’s prophecy. New York: Basic
Kagan, J. ~1997!. Conceptualizing psychopathology: The
importance of developmental profiles. Development
and Psychopathology,9, 1–14.
Kagan, J., Reznick, J. S., & Snidman, N. ~1987!. The
physiology and psychology of behavioral inhibition
in young children. Child Development,58, 1459–1473.
Kagan, J., Reznick, J. S., & Snidman, N. ~1988!. Biolog-
ical bases of childhood shyness. Science,240, 167–171.
Kagan, J., Snidman, N., Zentner, M., & Peterson, E. ~1999!.
Infant temperament and anxious symptoms in school
age children. Development and Psychopathology,11,
Ketelaar, T., & Ellis, B. J. ~2000!. Are evolutionary ex-
plainations unfalsifiable? Evolutionary psychology and
the Lakatosian philosophy of science. Psychological
Inquiry,11, 1–21.
Klonowicz, T. ~1987!. Reactivity and the control of arousal.
In J. Strelau & J. H. Eysenck ~Eds.!,Personality di-
mensions and arousal. Perspectives on individual dif-
ferences ~pp. 183–196!. New York: Plenum Press.
Kochanska, G. ~1993!. Toward a synthesis of parental
socialization and child temperament in early develop-
ment of conscience. Child Development,64, 325–347.
298 W. T. Boyce and B. J. Ellis
Kochanska, G. ~1997!. Multiple pathways to conscience
for children with different temperaments: From tod-
dlerhood to age 5. Developmental Psychology,33,
Kohn, P. M. ~1991!. Reactivity and anxiety in the labora-
tory and beyond. In J. Strelau & A.Angleitner ~Eds.!,
Explorations in temperament: International perspec-
tives on theory and measurement. London: Plenum
Kohn, P. M., Hunt, R. W., Cowles, M. P., & Davis, C. A.
~1986!. Factor structure and construct validity of the
Vando Reducer–Augmenter Scale. Personality and In-
dividual Differences,7, 57–64.
Laban, O., Dimitrijevic, M., von Hoersten, S., Markovic,
B. M., & Jankovic, B. D. ~1995!. Experimental aller-
gic encephalomyelitis in adult DA rats subjected to
neonatal handling or gentling. Brain Research,676,
Lacey, J. I. ~1959!. Psychophysiological approaches to
the evaluation of psychotherapeutic process and out-
come. In E. A. Rubinstein & M. B. Parloff ~Eds.!,
Research in psychotherapy ~pp. 161–196!. Washing-
ton, DC: American Psychological Association.
Lakatos, I. ~1970!. Falsificationism and the methodology
of scientific research programmes. In I. Lakatos & A.
Musgrave ~Eds.!,Criticism and the growth of knowl-
edge ~pp. 91–196!. Cambridge: Cambridge Univer-
sity Press.
Lakatos, I. ~1978!.The Methodology of scientific re-
search programmes: Philosophical papers ~Vol. 1!.
Cambridge: Cambridge University Press.
Lemne, C. E. ~1998!. Increased blood pressure reactivity
in children of borderline hypertensive fathers. Jour-
nal of Hypertension,16, 1243–1248.
Lewis, M., & Ramsay, D. S. ~1997!. Stress reactivity and
self-recognition. Child Development,68, 621–629.
Liang, S. W., Jemerin, J. J., Tschann, J. M., Irwin, C. E.,
Wara, D. W., & Boyce, W. T. ~1995!. Life events,
cardiovascular reactivity, and risk behavior in adoles-
cent boys. Pediatrics,96, 1101–1105.
Linnoila, M., Virkkunen, M., George, T., Eckardt, M.,
Higley, J. D., Nielsen, D., Goldman, D. ~1994!. Sero-
tonin, violent behavior and alcohol. Experientia Sup-
plement,71, 155–163.
Liu, D., & Meaney M. J. ~1997!. Maternal care, hippo-
campal glucocorticoid receptors, and hypothalamic–
pituitary–adrenal responses to stress. Science,277,
Lubach, G. R., Coe, C. L., & Ershler, W. B. ~1995!.
Effects of early rearing environment on immune re-
sponses of infant rhesus monkeys. Brain Behavior
and Immunity,9, 31–46.
Lupien, S. J., King, S., Meaney, M. J., & McEwen, B. S.
~2000!. Child’s stress hormone levels correlate with
mother’s socioeconomic status and depressive state.
Biological Psychiatry,48, 976–980.
Luthar, S. S., Doernberger, C. H., & Zigler, E. ~1993!.
Resilience is not a unidimensional construct: Insights
from a prospective study of inner-city adolescents.
Development and Psychopathology,5, 703–717.
Lynch, J. W., Everson, S.A., Kaplan, G. A., Salonen, R.,
& Salonen, J. T. ~1998!. Does low socioeconomic
status potentiate the effects of heightened cardiovas-
cular responses to stress on the progression of carotid
atherosclerosis? American Journal of Public Health,
88, 389–394.
Lyons, D. M., Wang, O. J., Lindley, S. E., Levine, S.,
Kalin, N. H., & Schatzberg, A. F. ~1999!. Separation
induced changes in squirrel monkey hypothalamic–
pituitary–adrenal physiology resemble aspects of hy-
percortisolism in humans. Psychoneuroendocrinology,
24, 131–142.
Lyons, D. M., Yang, C., Sawyer–Glover, A. M., Moseley,
M. E., & Schatzberg, A. F. ~2001!. Early life stress
and inherited variation in monkey hippocampal vol-
umes. Archives of General Psychiatry,58, 1145–1151.
MacDonald, K. ~1995!. Evolution, the five-factor model,
and levels of personality. Journal of Personality,63,
Martin, R. E., Sackett, G. P., Gunderson, V. M., & Goodlin–
Jones, B. L. ~1988!. Auditory evoked heart rate re-
sponses in pigtailed macaques ~Macaca nemestrina!
raised in isolation. Developmental Psychobiology,21,
Masten, A. S. ~2001!. Ordinary magic: Resilience pro-
cesses in development. American Psychologist,56,
Matthews, K. A. ~1986!. Summary, conclusions and im-
plications. In K. A. Matthews, S. M. Weiss & T. Detre
~Eds.!,Handbood of stress, reactivity and cardiovas-
cular disease. New York: Wiley–Interscience.
Matthews, K. A., Manuck, S. B., Stoney, C. M., Rakac-
zky, C. J., McCann, B. S., Saab, P. G., Woodall, K. L.,
Block, D. R., Visintainer, P. F., & Engebretson, T. O.
~1988!. Familial aggregation of blood pressure and
heart rate responses during behavioral stress. Psycho-
somatic Medicine,50, 341–352.
McCormick, D. A., & Bal, T. ~1994!. Sensory gating
mechanisms of the thalamus. Current Opinion in
Neurobiology,4, 550–556.
McEwen, B. S. ~1998!. Protective and damaging effects
of stress mediators. New England Journal of Medi-
cine,338, 171–179.
McEwen, B. S., & Stellar, E. ~1993!. Stress and the indi-
vidual. Mechanisms leading to disease. Archives of
Internal Medicine,153, 2093–2101.
Mealey, L. ~1995!. The sociobiology of sociopathy: An
integrated evolutionary model. Behavioral and Brain
Sciences,18, 523–599.
Mealey, L. ~2000!.Sex differences: Development and evo-
lutionary strategies. San Diego, CA: Academic Press.
Mealey, L. ~2001!. Kinship: The tie that binds ~disci-
plines!. In H. Holcomb ~Ed.!,Conceptual challenges
in evolutionary psychology. New York: Kluwer
Meaney, M. J. ~2001!. Maternal care, gene expression,
and the transmission of individual differences in stress
reactivity across generations. Annual Review of Neuro-
science,24, 1161–1192.
Meyer, J. S., & Bowman, R. E. ~1972!. Rearing experi-
ence, stress and adrenocorticosteroids in the rhesus
monkey. Physiology & Behavior,8, 339–343.
Meyer, S. E., Chrousos, G. P., & Gold, P. W. ~2001!.
Major depression and the stress system: A life span
perspective. Development and Psychopathology,13,
Moffitt, T. E., Caspi, A., Belsky, J., & Silva, P. A. ~1992!.
Childhood experience and the onset of menarche: A
test of a sociobiological model. Child Development,
63, 47–58.
Munck, A., Guyre, P. M., & Holbrook, N. J. ~1984!. Phys-
iological functions of glucocorticoids in stress and
their relation to pharmacological actions. Endocrine
Reviews,5, 25–43.
Musante, L., Treiber, F. A., Kapuku, G., Moore, D., Da-
vis, H., & Strong, W. B. ~2000!. The effects of life
Biological sensitivity to context: I 299
events on cardiovascular reactivity to behavioral stress-
ors as a function of socioeconomic status, ethnicity,
and sex. Psychosomatic Medicine,62, 760–767.
Nachmias, M., Gunnar, M. R., Mangelsdorf, S., Parritz,
R. H., & Buss, K. ~1996!. Behavioral inhibition and
stress reactivity: The moderating role of attachment
security. Child Development,67, 508–522.
Neiss, R. ~1988!. Reconceptualizing arousal: Psychobio-
logical states in motor performance. Psychological
Bulletin,103, 345–366.
Nesse, R. M., & Young, E. A. ~2000!. Evolutionary ori-
gins and functions of the stress response. In G. Fink
~Ed.!,Encyclopedia of stress ~Vol. 2, pp. 79–84!. New
York: Academic Press.
Neylan, T. C., Fletcher, D. J., Lenoci, M., McCallin, K.,
Weiss, D. S., Schoenfeld, F. B., Marmar, C. R., &
Fein, G. ~1999!. Sensory gating in chronic posttrau-
matic stress disorder: Reduced auditory P50 suppres-
sion in combat veterans. Biological Psychiatry,46,
Owens, M. J., & Nemeroff, C. B. ~1991!. Physiology and
pharmacology of corticotropin-releasing factor. Phar-
macological Reviews,43, 425–473.
Patterson, C. M., & Newman, J. P. ~1993!. Reflectivity
and learning from aversive events: Toward a psycho-
logical mechanism for the syndromes of disinhibition.
Psychological Review,100, 716–736.
Perry, B. ~1994!. Neurobiological sequelae of childhood
trauma: PTSD in children. In M. Murburg ~Ed.!,Cat-
echolamine function in post-traumatic stresss disor-
der: Emerging concepts ~pp. 233–255!. Washington,
DC: American Psychiatric Press.
Plotsky, P. M., & Meaney, M. J. ~1993!. Early, postnatal
experience alters hypothalamic corticotropin-releasing
factor ~CRF!mRNA, median eminence CRF content
and stress-induced release in adult rats. Molecular
Brain Research,18, 195–200.
Quas, J. A., Bauer,A. M., & Boyce, W. T. ~2004!. Physi-
ological reactivity, social support, and memory in early
childhood. Child Development.
Quas, J. A., Hong, M.,Alkon, A., & Boyce, W. T. ~2000!.
Dissociations between psychobiologic reactivity and
emotional expression in children. Developmental Psy-
chobiology,37, 153–175.
Raine, A., Venables, P. H., & Mednick, S.A. ~1997!. Low
resting heart rate at age 3 years predisposes to aggres-
sionat age 11years: Evidence fromthe MauritiusChild
Health Project. Journal of the American Academy of
Child and Adolescent Psychiatry,36, 1457–1464.
Reis, D. J., & Golanov, E. V. ~1997!. Autonomic and
vasomotor regulation. International Review of Neuro-
biology,41, 121–149.
Reznick, J. S., Kagan, J., Snidman, N., Gersten, M., Baak,
K., & Rosenberg, A. ~1986!. Inhibited and uninhib-
ited children: A follow-up study. Child Development,
57, 660– 680.
Rolls, E. T. ~1999!.The brain and emotion. Oxford: Ox-
ford University Press.
Sanchez, M. M., Ladd, C. O., & Plotsky, P. M. ~2001!.
Early adverse experience as a developmental risk fac-
tor for later psychopathology: Evidence from rodent
and primate models. Development and Psychopathol-
ogy,13, 419–449.
Sapolsky, R. M. ~1990!. Adrenocortical function, social
rank, and personality among wild baboons. Biologi-
cal Psychiatry,28, 862–885.
Sapolsky, R. M. ~1996!. Why stress is bad for your brain.
Science,273, 749–750.
Sapolsky, R. M., Romero, L. M., & Munck,A. U. ~2000!.
How do glucocorticoids influence stress responses?
Integrating permissive, suppressive, stimulatory, and
preparative actions. Endocrine Reviews,21, 55–89.
Sapolsky, R. M., & Share, L. J. ~1994!. Rank-related dif-
ferences in cardiovascular function among wild ba-
boons: Role of sensitivity to glucocorticoids. American
Journal of Primatology,32, 261–275.
Scarpa, A., & Raine, A. ~1997!. Psychophysiology of
anger and violent behavior. Psychiatric Clinics of North
America,20, 375–394.
Schlichting, C. D., & Pigliucci, M. ~1998!.Phenotypic
evolution: A reaction norm perspective. Sunderland,
MA: Sinauer Associates.
Schmidt, L. A., Fox, N. A., Schulkin, J., & Gold, P. W.
~1999!. Behavioral and psychophysiological corre-
lates of self-presentation in temperamentally shy chil-
dren. Developmental Psychobiology,35, 119–135.
Selye, H. ~1950!.Stress: The physiology and pathology of
exposure to stress. Montreal:Acta Medical Publishers.
Shannon, C., Champoux, M., & Suomi, S. J. ~1998!. Rear-
ing condition and plasma cortisol in rhesus monkey
infants.AmericanJournal ofPrimatology,46,311–321.
Shimamura, A. P. ~2000!. The role of the prefrontal cor-
tex in dynamic filtering. Psychobiology,28, 207–218.
Slobodkin,L., &Rapoport,A.~1974!.An optimal strategy
ofevolution.Quarterly Review ofBiology,49,181–200.
Smith, G. W., Aubry, J. M., Dellu, F., Contarino, A.,
Bilezikjian, L. M., Gold, L. H., Chen, R., Marchuk,
Y., Hauser, C., Bentley, C. A., Sawchenko, P. E.,
Koob, G. F., Vale, W., & Lee K. F. ~1998!. Cortico-
tropin releasing factor receptor 1-deficient mice dis-
play decreased anxiety, impaired stress response, and
aberrant neuroendocrine development. Neuron,20,
Snidman, N., Kagan, J., Riordan, L., & Shannon, D. C.
~1995!. Cardiac function and behavioral reactivity dur-
ing infancy. Psychophysiology,32, 199–207.
Stein,M. B., Yehuda,R.,Koverola, C., &Hanna, C. ~1997!.
Enhanced dexamethasone suppression of plasma cor-
tisol in adult women traumatized by childhood sexual
abuse. Biological Psychiatry,42, 680– 686.
Stevens, K. E., Bullock, A. E., & Collins, A. C. ~2001!.
Chronic corticosterone treatment alters sensory gat-
ing in C3H mice. Pharmacology Biochemistry and
Behavior,69, 359–366.
Stevenson–Hinde, J., & Marshall, P. J. ~1999!. Behavioral
inhibition, heart period, and respiratory sinus arrhyth-
mia: An attachment perspective. Child Development,
70, 805–816.
Strelau, J. ~1983!.Temperament personality activity. New
York: Academic Press.
Strelau, J., & Eysenck, H. J. ~1987!.Personality dimen-
sions and arousal. New York: Plenum Press.
Suomi, S. J. ~1987a!.Individual differences in rhesus mon-
key behavioral and adrenocortical responses to so-
cial challenge: Correlations with measures of heart
rate variability. Paper presented at the Heart Rate
Variability and Social Behavior: Behavioral and Bio-
logical Correlates Conference, Baltimore, MD.
Suomi, S. J. ~1987b!. Genetic and maternal contributions
to individual differences in Rhesus monkey biobehav-
ioral development. In N. Krasnagor ~Ed.!,Psychobio-
logical aspects of behavioral development ~pp. 397–
419!. New York: Academic Press.
Suomi, S. J. ~1997!. Early determinants of behaviour:
Evidence from primate studies. British Medical Bul-
letin,53, 170–184.
300 W. T. Boyce and B. J. Ellis
Surbey, M. K. ~1990!. Family composition, stress, and
the timing of human menarche. In T. E. Ziegler~Ed.!,
Socioendocrinology of primate reproduction. Mono-
graphs in primatology ~pp. 11–32!. New York:
Taub, J. M. ~1998!. Eysenck’s descriptive and biological
theory of personality: A review of construct validity.
International Journal of Neuroscience,94, 145–197.
Turkheimer, E., & Gottesman, I. I. ~1991!. Individual
differences and the canalization of human behavior.
Developmental Psychology,27, 18–22.
Turner, J. R., & Hewitt, J. K. ~1992!. Twin studies of
cardiovascular response to psychological challenge:
A review and suggested future directions. Annals of
Behavioral Medicine,14, 12–20.
Valentino, R. J., Curtis, A. L., Page, M. E., Pavcovich, L.
A., & Florin–Lechner, S. M. ~1998!. Activation of the
locus ceruleus brain noradrenergic system during stress:
Circuitry, consequences, and regulation. Advances in
Pharmacology,42, 781–784.
van der Saag, P. T., Caldenhoven, E., & van de Stolpe,A.
~1996!. Molecular mechanisms of steroid action: A
novel type of cross-talk between glucocorticoids and
NF-kappa B transcription factors. European Respira-
tory Journal,Supplement 22, 146s–153s.
Vazquez, D. M., Watson, S. J., & Lopez, J. F. ~2000, July!.
Failure to terminate stress responses in children with
psychosocial dwarfism: A mechanism for growth fail-
ure. Paper presented at the International Conference
of Infant Studies, Brighton, UK.
Viau, V. ~2002!. Functional cross-talk between the
hypothalamic–pituitary–gonadal and –adrenal axes.
Journal of Neuroendocrinology,14, 506–513.
von Bertalanffy, L. ~1968!.General system theory: Foun-
dations,development,applications. New York: George
Waddington, C. H. ~1966!.Principles of development and
differentiation. New York: MacMillan.
Waldo, M., Myles–Worsley, M., Madison, A., Byerley,
W., & Freedman, R. ~1995!. Sensory gating deficits in
parents of schizophrenics. American Journal of Med-
ical Genetics,60, 506–511.
Ward, H. E., Johnson, E.A., Salm, A. K., & Birkle, D. L.
~2000!. Effects of prenatal stress on defensive with-
drawal behavior and corticotropin releasing factor sys-
tems in rat brain. Physiology & Behavior,70, 359–366.
White, B. P., Gunnar, M. R., Larson, M. C., Donzella, B.,
& Barr, R. G. ~2000!. Behavioral and physiological
responsivity and patterns of sleep and daily salivary
cortisol in infants with and without colic. Child De-
velopment,71, 862–877.
Willemsen–Swinkels, S. H., Bakermans–Kranenburg,
M. J., Buitelaar, J. K., van, I. M. H., & van Engeland,
H. ~2000!. Insecure and disorganised attachment in
children with a pervasive developmental disorder: Re-
lationship with social interaction and heart rate. Jour-
nal of Child Psychology and Psychiatry and Allied
Disciplines,41, 759–767.
Worthman, C. M., Angold, A., & Costello, E. J. ~1998!.
Stress,reactivity and psychiatric risk in adolescents.
Paper presented at the Biennial Meeting of the Soci-
ety for Research on Adolescence, San Diego, CA,
February 26–28.
Yehuda, R. ~2002!. Post-traumatic stress disorder. New
England Journal of Medicine,346, 108–114.
Yehuda, R., Halligan, S. L., & Bierer, L. M. ~2001!. Re-
lationship of parental trauma exposure and PTSD to
PTSD, depressive and anxiety disorders in offspring.
Journal of Psychiatric Research,35, 261–270.
Yehuda, R., Halligan, S. L., & Grossman, R. ~2001!. Child-
hood trauma and risk for PTSD: Relationship to inter-
generational effects of trauma, parental PTSD, and
cortisol excretion. Development and Psychopathol-
ogy,13, 733–753.
Yehuda, R., McFarlane, A. C., & Shalev, A. Y. ~1998!.
Predicting the development of posttraumatic stress
disorder from the acute response to a traumatic event.
Biological Psychiatry,44, 1305–1313.
Yerkes, R. M., & Dodson, J. D. ~1908!. The relation of
strength of stimulus to rapidity of habit formation.
Journal of Comparative Neurology and Psychology,
18, 459–482.
Zaharia, M. D., Kulczycki, J., Shanks, N., Meaney, M. J.,
& Anisman, H. ~1996!. The effects of early postnatal
stimulation on Morris water-maze acquisition in adult
mice: Genetic and maternal factors. Psychopharma-
cology (Berlin),128, 227–239.
Zuckerman, M. ~1984!. Sensation seeking: A compara-
tive approach to a human trait. Behavioral and Brain
Sciences,7, 413–471.
Biological sensitivity to context: I 301
... It is a concept that is superior to other theories used to explain individual differences in the ability to register and process environmental stimuli. It includes the Differential Susceptibility concept [7,8], the concept of Sensory Processing Sensitivity [9,10] as well as Biological Sensitivity to Context [11,12]. A common feature of the above-mentioned concepts is the view that both people and animals show diverse levels of sensitivity in response to supportive as well as to difficult, adverse environments, with some individuals being significantly more sensitive than others to the negative effects of adversity, stress and related difficulties of a psychological nature, but also "disproportionately susceptible to the beneficial effects of supportive and enriching experiences (or just the absence of adversity)" ( [8] p. 885). ...
... A common feature of the above-mentioned concepts is the view that both people and animals show diverse levels of sensitivity in response to supportive as well as to difficult, adverse environments, with some individuals being significantly more sensitive than others to the negative effects of adversity, stress and related difficulties of a psychological nature, but also "disproportionately susceptible to the beneficial effects of supportive and enriching experiences (or just the absence of adversity)" ( [8] p. 885). This means that the explanation for this phenomenon had been sought by conducting research concerning reactivity to the environment, both in terms of physiological mechanisms, reactivity to stress and phenotypic manifestations (e.g., [11,13]). ...
... In the subject literature, we find some reports that environmental sensitivity has a normal distribution in the population, and that about 20% of people are highly reactive to the environment (e.g., [11]). The results of several studies indicate the percentage of highly sensitive people in the population (i.a., [2,11,14,15,33]). ...
Full-text available
The research described herein is based on the assumptions of the sensory processing sensitivity concept and the meta framework for the concept of environmental sensitivity. The adopted theoretical framework shows that individuals differ in their sensitivity to the environment, with some being more sensitive than others. From the evolutionary perspective, it has also been assumed that sensory processing sensitivity follows a normal distribution in the population, with a minority being exceptionally or highly sensitive to environmental stimuli. We explored data from a sample of 928 young adolescents in two studies. The tool used to evaluate their sensitivity was the Highly Sensitive Child Scale, which in studies 1 and 2 had a three-factor structure. Latent class analysis was used for the interpretation of the data of the studied groups. The obtained results indicate the existence of three groups which differ significantly from each other according to the HSC result. Based on the obtained results, it may be assumed that young adolescents are divided into three groups characterized by different sensitivities and their percentage distribution is not in agreement with the research conducted to date. The acquired information has both a theoretical value and a practical applicability, prompting reflection about the different aspects of the study, such as cultural differences, changes related to the development stage and the characteristics of the evaluation tool itself. From the perspective of possible applications, the obtained results may provide important information (1) to decision-makers who plan support or intervention programs at various levels of prevention, (2) for practitioners to provide them with the means with which to consider sensitivity as an important factor in coping with difficulties through diversified and adequate support (3) that is broadly applicable in the face of an environmental crisis (pandemic, the changing structure of class groups which is related to the number of refugees).
... Moreover, it is worth noting that this concept is superior to other theories which attempt to explain individual differences in the ability to perceive and process environmental stimuli. The components of the Environmental Susceptibility theory include the Differential Susceptibility concept (Belsky 2005;Belsky and Pluess 2009), the Sensory Processing Sensitivity concept (Aron 2013;Aron and Aron 1997) and Biological Sensitivity to Context (Boyce and Ellis 2005;Shakiba et al. 2019). The common element of these assumptions is the view that there are differences in sensitivity to the environment among humans and animals, both positive and negative. ...
... An explanation for this fact was sought through research concerning reactivity to the environment, taking into account certain physiological mechanisms, reactivity to stress, but also phenotypic manifestations (e.g. Aron, Aron & Jagiellowicz, 2012;Boyce & Ellis, 2005). The sensory processing sensitivity (SPS) concept, which includes the latter, assumes that the aforementioned differences result from a temperamental trait, and that SPS is a manifestation of environmental sensitivity (Aron & Aron, 1997;Greven et al., 2019;Pluess, 2015). ...
... In addition, in children who may be described as highly sensitive, it has been observed that the stress they experience in the home and school environments has a significant effect upon the incidence with which they experience illnesses and various types of injuries. Children growing up in less stressful conditions, compared to their peers, experience injuries and suffer from illnesses significantly less often (Ellis, Boyce, 2005). Environmental sensitivity also provides them with the potential to make a fuller use of the opportunities arising from constructive influences. ...
... Este concepto queda englobado dentro del modelo de desarrollo de plasticidad fenotípica de Boyce y Ellis (2005). Estos investigadores explican que la sensibilidad biológica al contexto -"biological sensitivity to context" (BSC) -es la respuesta reactiva neurobiológica a una situación de estrés, que puede variar enormemente entre individuos. ...
... Argumentan que, dada una situación o entorno altamente estresante, esta característica hace que haya un incremento en la vigilancia ante los peligros y/o amenazas y en consecuencia aumente la competencia adaptativa. A su vez, en situaciones o entornos altamente protectores provoca un aumento de la susceptibilidad a los recursos sociales y el apoyo ambiental (Boyce y Ellis, 2005). Esta teoría apoya que los niños/as altamente reactivos -orquídeas como lo llaman dentro de esta perspectiva -se ven más favorecidos cuando se encuentran en un ambiente de apoyo y crianza. ...
Full-text available
Recopilación de estudios realizados por investigadores en formación a la sombra del Grupo de Investigación de Alto Rendimiento FERSE (Fundamentos de la Educación y Responsabilidad Social Educativa. Los estudios están vinculados a la línea de investigación preferente, no obstante, existen investigaciones que hacen aportaciones a diversas líneas.
... into potential resiliencies could be refined by measuring subjective impacts or severity of PTEs and minority stressors from a life history perspective (Boyce & Ellis, 2005). For example, Hequembourg and colleagues (2013) found that severity of adulthood and childhood sexual violence was significantly and positively associated with poorer outcomes such as risky drinking and revictimization. ...
... Evidence that shows that the same individual's factors (e.g., gene variations) predict both sensitivities to negative and positive aspects of the environment, may imply that the different models reflect the same propensity for sensitivity to the environment. However, the difference between these types of sensitivities (i.e., to a negative environment, a positive environment, or both) is shaped both by the presence of susceptibility factors and by early life experiences (36,37). According to this view, individuals who display a predisposition for sensitivity to the environment may eventually develop a biased sensitivity toward negative experience (i.e., diathesis-stress) or support (i.e., vantage sensitivity), according to their early development experiences. ...
Full-text available
Although the evidence for the genetic basis of attention-deficit/hyperactivity disorder (ADHD) is strong, environmental factors, such as the quality of parenting or the home environment, may moderate such genetic liability. The plausible negative effect of a low-quality home environment and negative parenting on child outcomes is well-established; however, the positive effect of a high-quality environment and positive parenting remained largely uninvestigated. Due to the presence of genetic, temperamental, or physiological factors, children who were traditionally considered at-risk for ADHD may be more sensitive to aspects of their environment compared to children who are not at such risk. Therefore, they would be more affected by their environmental experience, either for good or bad. Under supportive environmental conditions, such at-risk individuals might actually outperform their non-vulnerable peers, suggesting that these individual factors might be considered susceptibility factors rather than risk factors. Little is known regarding the positive effect of the environment in the ADHD literature, but it has been demonstrated in cognitive functions that are closely associated with ADHD, such as executive functions (EF). We review this literature and examine the extant empirical support for sensitivity to aspects of the home environment and parenting in the case of ADHD and EF. Moreover, we review factors that could help identify the specific aspects of the home environment and parenting that these children might be more susceptible to. Such knowledge could be valuable when designing preventive interventions and identifying those children that are especially sensitive and could benefit from such interventions. Recommendations for future studies are discussed as well.
... In this study, the exploration of the moderating effect of BDNF rs6265 on two environmental factors (physical activity, with an alleged protective effect, and childhood stress as a negative factor) in relation to the development of depressive symptoms allowed us to study the differential susceptibility of BDNF rs6265 alleles [77][78][79]. ...
Full-text available
Depression affects one in five persons at 18 years of age. Allele A of the brain-derived neurotrophic factor (BDNF) rs6265 is considered to be a risk factor for depression. Previous studies of the interaction between BDNF rs6265, early adversity, and/or physical activity have shown mixed results. In this study, we explored the relation between BDNF rs6265 polymorphism and childhood stress, as well as the moderating effect of physical activity in relation to depressive symptoms using binary logistic regressions and process models 1, 2 and 3 applied to data obtained at three times (waves 1, 2 and 3) from the Survey of Adolescent Life in Västmanland cohort study (SALVe). Results revealed that both childhood stress and physical activity had a moderation effect; physical activity in wave 1 with an R2 change = 0.006, p = 0.013, and the Johnson–Neyman regions of significance (RoS) below 1.259, p = 0.05 for 11.97%; childhood stress in wave 2 with the R2 change = 0.008, p = 0 002, and RoS below 1.561 with 26.71% and >4.515 with 18.20%; and a three-way interaction in wave 1 in genotype AA carriers. These results suggest that allele A is susceptible to physical activity (positive environment) and childhood stress (negative environment).
... Reaction to stress also depends on the childhood environment, and this explains, for instance, why psychosocial stress can have either an inhibiting or an accelerating effect on pubertal development (Ellis 2004). These strands of psychiatry and evolutionary literature on stress vulnerability suggest that the responses to parental death can be very diverse (Boyce and Ellis 2005). In the specific case of family life, we expect some individuals who experience early parental death to retreat from parenthood and others to embrace family life, while still others may show no specific reaction. ...
Full-text available
Death of a parent during childhood has become rare in developed countries but remains an important life course event that may have consequences for family formation. This paper describes the link between parental death before age 18 and fertility outcomes in adulthood. Using the large national 2011 French Family Survey (INSEE-INED), we focus on the 1946-66 birth cohorts, for whom we observe entire fertility histories. The sample includes 11,854 respondents who have lost at least one parent before age 18. We find a strong polarization of fertility behaviours among orphaned males, more pronounced for those coming from a disadvantaged background. More often childless, particularly when parental death occurred in adolescence, some seem to retreat from parenthood. But orphaned men and women who do become parents seem to embrace family life, by beginning childbearing earlier and having more children, especially when the deceased parent is of the same sex.
Research has shown that adolescents' substance use behavior is determined not only by individual characteristics but also by peer environments, and an emerging literature in social genomics has also found that individual genotypes moderate peer effects on egos' substance use. However, the previous literature on genetic by peer environment (GxPE) interaction effects is limited by the use of genetic measures with limited power and a lack of focus on causality. Based on a sample of about 4000 adolescents of European Ancestry from the National Longitudinal Study of Adolescent to Adult Health, this study utilizes polygenic scores to examine GxPE interactions between ego's genetics and peers' cigarette, alcohol, and marijuana use. The results show peers' cigarette and marijuana use positively affect ego's substance use, and peer effects are stronger when the ego is genetically predisposed to substance use. However, genetic propensities toward risk tolerance are found to weaken the peer effects on the ego's marijuana use. Overall, our findings provide new evidence for the existence of GxPE effects on adolescent substance use and reveal the multidimensional nature of GxPE effects.
Evolutionary psychology aims to understand the origins of the human mind, including disease. Several theories about the origins of disease have been proposed. One concerns a developmental mismatch—a mismatch might occur at the individual level between the environment experienced during childhood and the environment the adult finds herself in, possibly resulting in disease. A second theory concerns the idea of an evolutionary mismatch—humans are adapted to ancestral conditions so they might now experience a mismatch with their modern environment, possibly resulting in disease. A third theory—differential susceptibility—outlines how genetic and epigenetic differences influence the extent to which humans are susceptible to rearing, including positive and negative experiences. Because of these differences, some individuals are more prone to develop disease than others. We review empirical studies that substantiate these theories and argue that an overarching theory that integrates these three lines into one provides a more accurate understanding of disease from an evolutionary perspective.
Full-text available
W badaniach dotyczących rozwoju dzieci zwraca się szczególną uwagę na rolę warunków, w jakich przebiega ich rozwój, oraz na znaczenie adekwatnej stymulacji, której źródłem jest najbliższe otoczenie, zwłaszcza dom rodzinny, a kolejno – przedszkole i szkoła. Wyniki badań wskazują, że im dziecko jest młodsze, tym większą, nawet kluczową, rolę w jego rozwoju odgrywa odpowiednie oddziaływanie środowiskowe, a więc i jakość otoczenia. W tym kontekście nabiera znaczenia adekwatne wsparcie dzieci wykazujących swoistą reaktywność na bodźce zarówno wewnętrzne, jak i zewnętrzne. W odniesieniu do tych dzieci należy z baczną uwagą śledzić tworzenie warunków do ich rozwoju oraz przenikliwie oceniać jakość kontaktu wychowawczego, który wymaga zaangażowania przede wszystkim ze strony wychowawcy, ale również i dziecka. To osoba wychowawcy, nauczyciela czy opiekuna oraz jego umiejętności tworzą środowisko sprzyjające rozwojowi dziecka. Zgodnie z powyższą tezą projektowanie wsparcia dzieci wysoko wrażliwych nie polega na modyfikacji ich cech. Również świadoma praca z dzieckiem nie zakłada ingerencji w cechę, nie przewiduje uczynienia dziecka mniej wrażliwym czy przyjęcia cechy za trudność bądź problem, z którym należy sobie poradzić, ale opiera się na zapewnieniu warunków, w których dzieci wysoko wrażliwe będą miały równe szanse na rozwijanie swojego potencjału. Celem niniejszego opracowania jest uzasadnienie potrzeby wspierania dzieci wysoko wrażliwych w ich najbliższym otoczeniu oraz przedstawienie propozycji takich działań. Materiał składa się z pięciu części. W pierwszej – Cechy dziecka wysoko wrażliwego przedstawiono zagadnienie aspektów tzw. wysokiej wrażliwości rozumianej jako cechy, a także problem manifestowania się cechy w różnych sferach funkcjonowania dziecka. Kolejno, w drugiej części Potrzeba identyfikacji dzieci wysoko wrażliwych, podjęto temat nasilenia cechy. Trzecia część opracowania to Znaczenie środowiska dla rozwoju dzieci wysoko wrażliwych, w której omówiono właściwości środowiska zewnętrznego, takie jak hałas czy nadmiar bodźców, oraz kwestię jakości środowiska wychowawczego. W tym kontekście należy zaznaczyć, że w niesprzyjających warunkach dziecko wysoko wrażliwe doświadcza trudności w przystosowaniu się, natomiast przy optymalnym wsparciu rozwija swój potencjał (ang. Vantage Sensitivity), czyli wrażliwość dającą przewagę. Czwarta część zawiera prezentację tematu Wsparcie dzieci wysoko wrażliwych w systemie edukacji, co w praktyce oznacza optymalną dla nich postawę wychowawcy, wyrastającą z założeń psychologii humanistycznej. W części piątej, ostatniej, podjęto temat Pomoc dzieciom wysoko wrażliwym poprzez wsparcie rodziców i nauczycieli.
Recently, there has been a convergence in lesion and neuroimaging data in the identification of circuits underlying positive and negative emotion in the human brain. Emphasis is placed on the prefrontal cortex (PFC) and the amygdala as two key components of this circuitry. Emotion guides action and organizes behavior towards salient goals. To accomplish this, it is essential that the organism have a means of representing affect in the absence of immediate elicitors. It is proposed that the PFC plays a crucial role in affective working memory. The ventromedial sector of the PFC is most directly involved in the representation of elementary positive and negative emotional states while the dorsolateral PFC may be involved in the representation of the goal states towards which these elementary positive and negative states are directed. The amygdala has been consistently identified as playing a crucial role in both the perception of emotional cues and the production of emotional responses, with some evidence suggesting that it is particularly involved with fear-related negative affect. Individual differences in amygdala activation are implicated in dispositional affective styles and increased reactivity to negative incentives. The ventral striatum, anterior cingulate and insular cortex also provide unique contributions to emotional processing.
we currently believe that by translating attentional theories into testable hypotheses, we will be able to advance our understanding of schizophrenic psychopathology by using converging operations and new methodologies, we are now in a position to generate and test critical, operationally defined hypotheses this approach allows us to dissect both the information processing chain of events and the underlying neurobiological mechanisms that are disordered in schizophrenia (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Although most people will gradually recover from the psychological effects of a traumatic event, PTSD will develop in a substantial proportion. PTSD appears to represent a failure to recover from a nearly universal set of emotions and reactions and is typically manifested as distressing memories or nightmares related to the traumatic event, attempts to avoid reminders of the trauma, and a heightened state of physiological arousal. Studies of the biologic mechanisms of PTSD have delineated circumscribed alterations in brain regions, such as the amygdala and hippocampus, that are associated with fear and memory, as well as changes in hormonal, neurochemical, and physiological systems involved in coordinating the body's response to stress. The treatment of PTSD involves educating the patient about the nature of the disorder, providing a safe and supportive environment for discussing traumatic events and their impact, and relieving the distress associated with memories and reminders of the event. A variety of approaches, such as exposure therapy, cognitive therapy, and pharmacotherapy, have been found to be effective in the treatment of PTSD.
Posttraumatic stress disorder (PTSD) is a psychiatric condition that is directly precipitated by an event that threatens a person's life or physical integrity and that invokes a response of fear, helplessness, or horror. In recent years it has become clear that only a proportion of those exposed to fear-producing events develop or sustain PTSD. Thus, it seems that an important challenge is to elucidate aberrations in the normal fear response that might precipitate trauma-related psychiatric disorder. This paper summarizes the findings from recent studies that examined the acute and longer term biological response to traumatic stress in people appearing to the emergency room immediately following trauma exposure. In the aggregate, these studies have demonstrated increased heart rate and lower cortisol levels at the time of the traumatic event in those who have PTSD at a follow-up time compared to those who do not. In contrast, certain features associated with PTSD, such as intrusive symptoms and exaggerated startle responses, are only manifest weeks after the trauma. The findings suggest that the development of PTSD may be facilitated by an atypical biological response in the immediate aftermath of a traumatic event, which in turn leads to a maladaptive psychological state.
Environmental stressors and stable individual differences in human behavior have both been implicated etiologically in injuries. Because stress-related injuries are difficult to study experimentally in humans, the authors examined injury incidence in a troop of 21 male and 15 female free-ranging rhesus macaques (Macaca mulatta) before, during, and after a 6-month group confinement. Individual differences in behavioral inhibition to novelty were assessed, using multiple, quantified observations of behavior by 3 independent raters during 3 previous years. Incidence and severity of medically attended injuries were ascertained from veterinary records over a 2-year study period. A 5-fold increase in the incidence of injuries was documented during confinement stress, and an interaction was found between the stressor and behavioral inhibition in the prediction of injury incidence. Highly inhibited animals had significantly higher injury rates during confinement, compared with their uninhibited peers, but equal or lower rates in the low stress periods that preceded and followed confinement. Inhibited individuals appeared to have been specifically targeted for violence during the group stressor but were protected under normative, more predictable conditions.