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

February 2005
Development and Psychopathology 17(2):271-301

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PubMed

Authors:

University of Utah

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.

The relation between Eysenck's dimensions of extraversion and neuroticism and Gray's dimensions of impulsivity and anxiety.

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Biological sensitivity to context: I. An

evolutionary–developmental theory of the

origins and functions of stress reactivity

W. THOMAS BOYCE

and BRUCE J. ELLIS

University of California, Berkeley; and

University of Arizona

Abstract

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: boyce@socrates.berkeley.edu.

Development and Psychopathology 17 ~2005!, 271–301

Printed in the United States of America

DOI: 10.10170S0954579405050145

271

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

environment.

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,

1988!.

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

insects.

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

Phenotypes

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

capableofrecalibratingresponsesystemslater

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

parameters.

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

papersreviewedprovideevidenceforacentral

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

evidenceandthesefindingsthatthediscussion

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,

2000!.

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-

tion,

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–

Worsley,Madison,Byerley,&Freedman,1995!,

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-

troversionisassociatedwithgreaterbiological

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

investment.

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

environments.

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

history.

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

development

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

stressors.

2,3

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

explored.

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.

Conclusion

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.

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Biological sensitivity to context: I 301

Cortisol Reactivity as a Moderator in the Relationship Between Home Chaos and Conduct Problems: Gender-Specific Evidence from Chinese Preschoolers

Article

Full-text available

Apr 2025
APPL PSYCHOPHYS BIOF

This study aimed to explore the moderating role of cortisol stress reactivity in the relationship between home chaos and child conduct problems among Chinese preschoolers, and further reveal these moderating patterns in boys and girls. The researchers employed a longitudinal design, surveying 160 preschool-aged children (73 boys, 87 girls) and their parents at two separate time points annually. The findings revealed a positive correlation between home chaos and child conduct problems, with cortisol stress reactivity acting as a significant moderator. Further analysis showed that low cortisol reactivity amplified the association between home chaos and child conduct problems for both boys and girls, although the interaction between cortisol reactivity and home chaos reached statistical significance only for boys. These results highlight the importance of considering the interplay between individual physiological factors, such as cortisol reactivity, and environmental risks like home chaos, in understanding behavioral outcomes in young children and further underscore the necessity of tailored interventions that account for both biological and environmental influences on child development.

Supporting the mental health of forcibly displaced children

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Full-text available

Apr 2025

Close to 50 million children under 18 years of age are currently forcibly displaced from their homes because of armed conflict and other emergencies. Displaced children and adolescents are at increased risk of developing poor mental health. However, knowledge about how best to support their mental health and well-being is limited. In this Review, we consolidate knowledge on the prevalence of mental disorders in settings of forced displacement, discuss individual differences in response to war and displacement, and review existing mental health and psychosocial support approaches. Critical assessment of this literature indicates a substantial mental health burden among displaced children and supports a broad range of risk and resilience mechanisms. Although some specific mental health and psychosocial support interventions have positively influenced forcibly displaced children’s mental health, there is a need for more culturally and contextually relevant, accessible and evidence-based services that also address family and community factors during displacement. We discuss recommendations to ensure that these services are linked to strategies that target adverse conditions and structural barriers and strengthen the socio-ecological resources that contribute to children’s positive development and well-being.

Ratings of Students’ Stress: Initial Reliability and Validity Evidence for a Brief Stress and Resilience Assessment

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Full-text available

Apr 2025

Stress is a complex construct that is related to resilience and general health starting in childhood. Despite its importance for student health and well-being, there are few measures of stress designed for school-based applications. In this study, we developed and initially validated a Stress Indicators Scale using five samples of teachers, parents, and students (N = 3338). We also identified the five best items from the scale that could inform development of a brief version of the scale for broader applications in comprehensive universal screening. Using item response theory, reliability analyses, convergent/discriminant correlations, and item bias analyses evidence supported claims that both the full and brief version of the Stress Indicators Scale are psychometrically sound and hold promise to expand options for school-based stress and resilience assessment. Examination of generalization limitations for these findings and additional research to advance the interpretation and use of the Stress Indicators Scale as part of social emotional health screenings conclude the article.

The effectiveness of a parent emotion socialization intervention in Norway

Article

Full-text available

May 2025
J APPL DEV PSYCHOL

Introduction Parent emotion socialization (ES) interventions have been found effective in improving children's emotional and behavioral functioning but have not been widely tested in non-English speaking countries. The current study was an effectiveness trial of the Australian ES program, Tuning in to Kids, with Norwegian parents of kindergarten children. Method 261 parents were randomized into intervention or 12-month waitlist control. Parent questionnaires measured ES, parent functioning, child temperament, behavior and anxiety. Results Findings showed the program was effective in reducing child behavior problems and parent emotion dismissiveness, and increasing emotion coaching parenting. Exploratory moderation analyses found parents who self-reported having lower affect integration made greater changes. Children with higher temperamental shyness had lower anxiety at follow-up. Discussion Findings suggest the program was effective in improving ES and reducing child behavior problems when delivered by professionals in Norway. Anxiety, while unchanged for the total sample, improved for children with higher shyness.

Environmental Sensitivity in Children Is Associated With Emotion Recognition

Article

Full-text available

Apr 2025

Children differ significantly in their emotion recognition, which represents an important component of social competence. According to theory and initial empirical studies in adults, individual differences in the trait of environmental sensitivity have been associated with emotion recognition, but this has not been studied in highly sensitive children yet. Highly sensitive children are generally understood to perceive and process environmental stimuli, including social ones, more easily and deeply than other children. We hypothesized that highly sensitive children would perform better in an objective emotion recognition task and be rated as more socially competent compared to low sensitive children. Ninety-seven 7- to 9-year-old U.K. primary school children (47% girls) completed the Reading the Mind in the Eyes test’s child version on a computer one-on-one with a researcher during school hours on school premises. Teachers rated children’s sensitivity using the Highly Sensitive Child in School scale and also reported on children’s social competence. Children completed the Highly Sensitive Child scale. The data were collected in 2022. Teacher-reported sensitivity emerged as a significant predictor of the Reading the Mind in the Eyes test’s child version and social competence, while child-reported sensitivity was not associated with emotion recognition. Teacher-reported overstimulation of children was negatively associated with social competence. This study is the first to report links between children’s environmental sensitivity, emotion recognition skills, and social competence. Findings are consistent with theories on environmental sensitivity and highlight the potential benefits of high sensitivity but will need to be replicated in more ethnically diverse samples.

Associations Between Early Life Stress, Health Behaviors, and Risk-Taking in Adulthood: A Structural Equation Modeling Approach

Article

Full-text available

May 2025

Across various scientific fields, early life stress (ELS) has been associated with more detrimental health behavior, higher risk-taking as well as accelerated socio-sexual behaviors, and higher reproductive effort. Previous research has identified resource scarcity, unpredictability, harshness, neighborhood hazards, parental investment, and exposure to violence and aggression as crucial factors of ELS. This study used an online survey to collect responses from 371 adult US residents via MTurk (160 females, 210 males, one other gender; Mage=29.98). Retrospective and current self-report measures were used to build a structural equation model of early childhood environment, socio-sexual behavior, reproductive effort, and adult health- and risk-related behaviors. A second-order factor of ELS predicted lower behavioral investment in health and safety (β=-0.30, p<0.001), indicated by less preventative and more detrimental health behavior as well as higher risk-taking propensity. The model showed that these adult behavioral tendencies constitute a coordinated behavioral strategy that prioritizes short-term opportunities and rewards over investments in future health, well-being, and safety. Model fit was excellent (RMSEA=0.054 [90% CI=0.048; 0.059]; CFI=0.966; TLI=0.957). Results partly corroborate theory and part of the previous empirical evidence but also suggest that factors of ELS are highly interrelated. No reliable associations emerged between ELS and socio-sexual behaviors, reproductive effort, or between these outcomes and adult behavioral tendencies. The study’s insights have implications for the design of intervention and prevention programs, which could benefit from focusing on changing ultimate behavioral strategies that jeopardize future health and well-being, rather than individual health and risk-taking behaviors.

An organized camp and mental health: Moderating role of environmental sensitivity

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May 2025
J APPL DEV PSYCHOL

Social and Emotional Learning and Physical Health Outcomes Across the Lifespan: Little Progress & Big Potential

Article

Apr 2025

Mark T. Greenberg

Maternal Childhood Maltreatment, Development of Amygdala Volume, and Anxiety Symptoms in Offspring

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Apr 2025
J AM ACAD CHILD PSY

The relationship between psychological resilience and hair cortisol in adolescents: The influence of family and school environments

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PSYCHONEUROENDOCRINO

Emotion, Plasticity, Context, and Regulation: Perspectives From Affective Neuroscience

Article

Full-text available

Nov 2000

The authors present an overview of the neural bases of emotion. They underscore the role of the prefrontal cortex (PFC) and amygdala in 2 broad approach- and withdrawal-related emotion systems. Components and measures of affective style are identified. Emphasis is given to affective chronometry and a role for the PFC in this process is proposed. Plasticity in the central circuitry of emotion is considered, and implications of data showing experience-induced changes in the hippocampus for understanding psychopathology and stress-related symptoms are discussed. Two key forms of affective plasticity are described—context and regulation. A role for the hippocampus in context-dependent normal and dysfunctional emotional responding is proposed. Finally, implications of these data for understanding the impact on neural circuitry of interventions to promote positive affect and on mechanisms that govern health and disease are considered.

Mother–Infant Affect Synchrony as an Antecedent of the Emergence of Self-Control

Article

Full-text available

Jan 1999

This study examined relations between mother–infant affect synchrony and the emergence of children’s self-control. Mother–infant face-to-face play and infant difficult temperament were examined at 3 and 9 months. Maternal and infant affective states at play were coded in 0.25-s frames, and synchrony was computed with cross-correlation functions. Self-control, verbal IQ, and maternal warm discipline were assessed at 2 years. Maternal synchrony with infant affect at 3 months (infant-leads–mother-follows relation) and mutual synchrony at 9 months (cross-dependence between maternal and infant affect) were each related to self-control at 2 years when temperament, IQ, and maternal style were partialed. Infant temperament moderated the relations of synchrony and self-control, and closer associations were found between mutual synchrony and self-control for difficult infants. Shorter lags to maternal synchrony at 3 months were independently related to self-control. The mutual regulation of affect in infancy, as moderated by temperament, is proposed as an important contributor to the emergence of self-regulation.

Multiple Pathways to Conscience for Children With Different Temperaments: From Toddlerhood to Age 5

Article

Full-text available

Mar 1997

Grazyna Kochanska

This research extends longitudinally findings on child temperament as a moderator of the impact of socialization on conscience development, reported previously for contemporaneous data at toddler age. Children's temperament and maternal socialization at Time 1 (n = 103, aged 2–3 years) were considered predictors of future conscience, assessed using new observational and narrative measures. The moderation model was supported for predicting conscience at Time 2 (n = 99, age 4), and, to a lesser extent, at Time 3 (n = 90, age 5). For children fearful as toddlers, maternal gentle discipline, presumably capitalizing on the optimal level of anxious arousal, promoted conscience at Time 2. For children fearless as toddlers, perhaps insufficiently aroused by gentle discipline, alternative socialization mechanisms, presumably capitalizing on mother–child positive orientation (secure attachment, maternal responsiveness), promoted conscience at Times 2 and 3. Developmental interplay of temperament and socialization in emerging morality is discussed.

Reflectivity and Learning From Aversive Events: Toward a Psychological Mechanism for the Syndromes of Disinhibition

Article

Full-text available

Oct 1993

Gorenstein and Newman (1980) proposed that poorly modulated responding for reward is the common diathesis underlying disinhibited behavior in several traditionally distinct person categories: psychopathy, hysteria, early onset alcoholism, childhood hyperactivity, and nonpathological impulsivity (e.g., extraversion). The authors extend this proposal by theorizing a psychological mechanism that highlights relations among disinhibition, reflection, and failures to learn from aversive feedback. The hypothesized mechanism is presented as 4 generic stages of response modulation: the dominant response set, the reaction to an aversive event, the subsequent behavioral adaptation, and the immediate and long-term consequences of reflection, or the lack thereof. The mechanism has implications for disinhibited individuals' impulsivity and provides a point of departure to study factors responsible for similarities and differences among these syndromes.

Reconceptualizing Arousal: Psychobiological States in Motor Performance

Article

Full-text available

May 1988

Rob Neiss

This review of research dealing with psychologically induced arousal and motor performance focuses on the hypothesized inverted-∪ function relating arousal to performance. The inverted-∪ hypothesis is supported only in a weak and psychologically trivial fashion: Subjects with incentive will outperform either those with none or those responding to a serious and plausible threat; the arousal level of the first group will be intermediate to those of the other two. However, debilitating states (e.g., anxiety) can occur at arousal levels equal to that optimal for performance (the state of being “psyched up”). The concept of arousal cannot distinguish between these and other states (e.g., anger, sexuality, and fear) because it is an excessively broad physiological construct artificially severed from its psychological context. More useful research in human motor performance would investigate discrete psychobiological states, which include affect and cognition as well as physiology. Examination of profound individual differences in response to incentive and threat suggests that psychobiological states have their genesis in response expectancies and hypnotic-like self-inductions. The cognitive and affective components of these states are highly interactive and perhaps not profitably separated. Because performance anxiety is a central problem in the motor realm, it is carefully delineated and the test anxiety literature is scrutinized. Psychophysiological test batteries and other investigations in the area are described, and guidelines for future research are provided.

Personality Dimensions and Arousal

Book

Jan 1987

The functional neuroanatomy of emotion and affective style

Article

Jan 1999

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.

The Physiology and Pathology of Exposure to Stress

Article

Jan 1950

H. Selye

Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress

Article

Jan 2010
Adv Sci

Sensorimotor gating and the neurobiology of schizophrenia: Human and animal studies

Article

Jan 1989

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)

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

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