Hostname: page-component-7c8c6479df-p566r Total loading time: 0 Render date: 2024-03-18T16:58:43.133Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  12 May 2005

W. THOMAS BOYCE
Affiliation:
University of California, Berkeley
BRUCE J. ELLIS
Affiliation:
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. 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 research on which this paper was based was supported 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 Division 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 influenced 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.

Type
Research Article
Copyright
© 2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adler, L. E., Pang, K., Gerhardt, G., & Rose, G. M. (1988). Modulation of the gating of auditory evoked potentials by norepinephrine: Pharmacological evidence obtained using a selective neurotoxin. Biological Psychiatry 24, 179190.Google Scholar
Adler, P. S., & Ditto, B. (1998). Psychophysiological effects of interviews about emotional events on offspring of hypertensives and normotensives. International Journal of Psychophysiology 28, 263271.Google Scholar
Alkon, A., Goldstein, L. H., Smider, N., Essex, M., Kupfer, D., & Boyce, W. T. (2003). Developmental and contextual influences on autonomic reactivity in young children. Developmental Psychobiology 42, 6478.Google Scholar
Allen, M. T., & Matthews, K. A. (1997). Hemodynamic responses to laboratory stressors in children and adolescents: The influences of age, race, and gender. Psychophysiology 34, 329339. [erratum p. 730]Google Scholar
Aron, E. N., & Aron, A. (1997). Sensory-processing sensitivity and its relation to introversion and emotionality. Journal of Personality and Social Psychology 73, 345368.Google Scholar
Asendorpf, J. B., & Meier, G. H. (1993). Personality effects on children's speech in everyday life: Sociability-mediated exposure and shyness-mediated reactivity to social situations. Journal of Personality and Social Psychology 64, 10721083.Google Scholar
Aston–Jones, G., Rajkowski, J., Kubiak, P., Valentino, R. J., & Shipley, M. T. (1996). Role of the locus coeruleus in emotional activation. Progress in Brain Research 107, 379402.Google Scholar
Bartels, M., de Geus, E. J., Kirschbaum, C., Sluyter, F., & Boomsma, D. I. (2003). Heritability of daytime cortisol levels in children. Behavior Genetics 33, 421433.Google Scholar
Bateson, P. P. G., Mendl, M., & Feaver, J. (1990). Play in the domestic cat is enhanced by rationing of the mother during lactation. Animal Behaviour 40, 514525.Google Scholar
Bauer, A. S. (2002). Concurrent sympathetic and adrenocortical activity as correlates of behavior in middle childhood. Unpublished master's thesis, University of California, Berkeley.
Belsky, J. (1997). Variation in susceptibility to environmental influence: An evolutionary argument. Psychological Inquiry 8, 182186.Google Scholar
Belsky, J. (2000). Conditional and alternative reproductive strategies: Individual differences in susceptiblity to rearing experiences. In J. L. Rodgers, D. C. Rowe, & W. B. Miller (Eds.), Genetic influences on human fertility and sexuality: Theoretical and empirical contributions from the biological and behavioral sciences (pp. 127145). Boston: Kluwer Academic.
Belsky, J. (2005). Differential susceptibility to rearing influence: An evolutionary hypothesis and some evidence. In B. J. Ellis & D. F. Bjorklund (Eds.), Origins of the social mind: Evolutionary psychology and child development (pp. 139163). New York: Guilford Press.
Belsky, J., Hsieh, K., & Crnic, K. (1998). Mothering, fathering, and infant negativity as antecedents of boys' externalizing problems and inhibition at age 3: Differential susceptibility to rearing influence? Development and Psychopathology 10, 301319.Google Scholar
Belsky, J., Steinberg, L., & Draper, P. (1991). Childhood experience, interpersonal development, and reproductive strategy: An evolutionary theory of socialization. Child Development 62, 647670.Google Scholar
Benediktsson, R., Lindsay, R. S., Noble, J., Seckl, J. R., & Edwards, C. R. (1993). Glucocorticoid exposure in utero: New model for adult hypertension. Lancet 341(8841), 339341.Google Scholar
Bentley, P. J. (1998). Comparative vertebrate endocrinology. Cambridge: Cambridge University Press.
Bergman, P., & Escalona, S. K. (1949). Unusual sensitivities in very young children. Pschoanalytic Studies of the Child 4, 333352.Google Scholar
Bernard, C. (1878). Les phenomenes de la vie. Paris: Baillière.
Blair, C. (2002). Early intervention for low birth weight preterm infants: The role of negative emotionality in the specification of effects. Development and Psychopathology 14, 311332.Google Scholar
Bloom, F. E., & Kupfer, D. J. (1995). Psychopharmacology (4th ed.). New York: Raven Press.
Boutros, N. N., Torello, M. W., Barker, B. A., Tueting, P. A., Wu, S. C., & Nasrallah, H. A. (1995). The P50 evoked potential component and mismatch detection in normal volunteers: Implications for the study of sensory gating. Psychiatry Research 57, 8388.Google Scholar
Boyce, W. T. (1996). Biobehavioral reactivity and injuries in children and adolescents. In M. H. Bornstein & J. Genevro (Eds.), Child development and behavioral pediatrics: Toward understanding children and health. Mahwah, NJ: Erlbaum.
Boyce, W. T., Champoux, M., Suomi, S. J., & Gunnar, M. R. (1995). Salivary cortisol in nursery-reared rhesus monkeys: Reactivity to peer interactions and altered circadian activity. Developmental Psychobiology 28, 257267.Google Scholar
Boyce, W. T., Chesney, M., Alkon–Leonard, A., Tschann, J., Adams, S., Chesterman, B., Cohen, F., Kaiser, P., Folkman, S., & Wara, D. (1995). Psychobiologic reactivity to stress and childhood respiratory illnesses: Results of two prospective studies. Psychosomatic Medicine 57, 411422.Google Scholar
Boyce, W. T., O'Neill–Wagner, P., Price, C. S., Haines, M., & Suomi, S. J. (1998). Crowding stress and violent injuries among behaviorally inhibited rhesus macaques. Health Psychology 17, 285289.Google Scholar
Boyce, W. T., Quas, J., Alkon, A., Smider, N., Essex, M., & Kupfer, D. J. (2001). Autonomic reactivity and psychopathology in middle childhood. British Journal of Psychiatry 179, 144150.Google Scholar
Braff, D. L., & Geyer, M. A. (1990). Sensorimotor gating and schizophrenia. Human and animal model studies. Archives of General Psychiatry 47, 181188.Google Scholar
Bremner, J. D., & Vermetten, E. (2001). Stress and development: Behavioral and biological consequences. Development and Psychopathology 13, 473489.Google Scholar
Bullock, W. A., & Gilliland, K. (1993). Eysenck's arousal theory of introversion–extraversion: A converging measures investigation. Journal of Personality and Social Psychology 64, 113123.Google Scholar
Busjahn, A., Faulhaber, H. D., Viken, R. J., Rose, R. J., & Luft, F. C. (1996). Genetic influences on blood pressure with the cold-pressor test: A twin study. Journal of Hypertension 14(10), 11951199.Google Scholar
Byrne, G., & Suomi, S. J. (2002). Cortisol reactivity and its relation to homecage behavior and personality ratings in tufted capuchin (Cebus apella) juveniles from birth to six years of age. Psychoneuroendocrinology, 27(1–2), 139154.Google Scholar
Cacioppo, J. T., Berntson, G. G., Malarkey, W. B., Kiecolt–Glaser, J. K., Sheridan, J. F., Poehlmann, K. M., Burleson, M. H., Ernst, J. M., Hawkley, L. C., & Glaser, R. (1998). Autonomic, neuroendocrine, and immune responses to psychological stress: The reactivity hypothesis. Annals of the New York Academy of Sciences 840, 664673.Google Scholar
Cacioppo, J. T., Berntson, G. G., Sheridan, J. F., & McClintock, M. K. (2000). Multilevel integrative analyses of human behavior: Social neuroscience and the complementing nature of social and biological approaches. Psychological Bulletin 126, 829843.Google Scholar
Calkins, S. D., & Fox, N. A. (1992). The relations among infant temperament, security of attachment, and behavioral inhibition at twenty-four months. Child Development 63, 14561472.Google Scholar
Calkins, S. D., Fox, N. A., & Marshall, T. R. (1996). Behavioral and physiological antecedents of inhibited and uninhibited behavior. Child Development 67, 523540.Google Scholar
Campbell, J. B., & Hawley, C. W. (1982). Study habits and Eysenck's theory of extraversion–introversion. Journal of Research in Personality 16, 139146.Google Scholar
Cannon, W. B. (1929). Bodily changes in pain, hunger, fear and rage. New York: Appleton.
Carlson, M., & Earls, F. (1997). Psychological and neuroendocrinological sequelae of early social deprivation in institutionalized children in Romania. Annals of the New York Academy of Sciences 807, 419428.Google Scholar
Carter, C. S. (1998). Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology 23, 779818.Google Scholar
Castellanos, F. X., Fine, E. J., Kaysen, D., Marsh, W. L., Rapoport, J. L., & Hallett, M. (1996). Sensorimotor gating in boys with Tourette's syndrome and ADHD: Preliminary results. Biological Psychiatry 39, 3341.Google Scholar
Champagne, F., & Meaney, M. J. (2001). Like mother, like daughter: Evidence for non-genomic transmission of parental behavior and stress responsivity. Progress in Brain Research 133, 287302.Google Scholar
Champoux, M., Higley, J. D., & Suomi, S. J. (1997). Behavioral and physiological characteristics of Indian and Chinese–Indian hybrid rhesus macaque infants. Developmental Psychobiology 31, 4963.Google Scholar
Champoux, M., Hwang, L., Lang, O., & Levine, S. (2001). Feeding demand conditions and plasma cortisol in socially-housed squirrel monkey mother–infant dyads. Psychoneuroendocrinology 26, 461477.Google Scholar
Champoux, M., & Suomi, S. J. (1994). Behavioral and adrenocortical responses of rhesus macaque mothers to infant separation in an unfamiliar environment. Primates 35, 191202.Google Scholar
Cheng, L. S., Carmelli, D., Hunt, S. C., & Williams, R. R. (1997). Segregation analysis of cardiovascular reactivity to laboratory stressors. Genetic Epidemiology 14, 3549.Google Scholar
Chesterman, E., Boyce, W. T., & Winkleby, M. A. (1989). Psychosocial predictors of maternal and infant health: A “sense of permanence” as a mediating variable (Abstract). Paper presented at the Society of Behavioral Medicine Annual Meeting, San Francisco.
Chisholm, J. S. (1999). Death, hope and sex: Steps to an evolutionary ecology of mind and morality. New York: Cambridge University Press.
Chrousos, G. P. (1998). Stressors, stress, and neuroendocrine integration of the adaptive response. The 1997 Hans Selye Memorial Lecture. Annals of the New York Academy of Sciences 851, 311335.Google Scholar
Comings, D. E., Muhleman, D., Johnson, J. P., & MacMurray, J. P. (2002). Parent–daughter transmission of the androgen receptor gene as an explanation of the effect of father absence on age of menarche. Child Development 73, 10461051.Google Scholar
Coplan, J. D., Andrews, M. W., Rosenblum, L. A., Owens, M. J., Friedman, S., Gorman, J. M., & Nemeroff, C. B. (1996). Persistent elevations of cerebrospinal fluid concentrations of corticotropin-releasing factor in adult nonhuman primates exposed to early-life stressors: Implications for the pathophysiology of mood and anxiety disorders. Proceedings of the National Academy of Sciences of the United States of America 93, 16191623.Google Scholar
Cratty, M. S., Ward, H. E., Johnson, E. A., Azzaro, A. J., & Birkle, D. L. (1995). Prenatal stress increases corticotropin-releasing factor (CRF) content and release in rat amygdala minces. Brain Research 675, 297302.Google Scholar
Crawford, C. B., & Anderson, J. L. (1989). Sociobiology: An environmentalist discipline? American Psychologist 44, 14491459.Google Scholar
Dallman, M. F., Akana, S. F., Cascio, C. S., Darlington, D. N., Jacobson, L., & Levin, N. (1987). Regulation of ACTH secretion: Variations on a theme of B. Recent Progress in Hormone Research 43, 113173.Google Scholar
Davidson, R. J., & Irwin, W. (1999). The functional neuroanatomy of emotion and affective style. Trends in Cognitive Sciences 3, 1121.Google Scholar
Davidson, R. J., Jackson, D. C., & Kalin, N. H. (2000). Emotion, plasticity, context, and regulation: Perspectives from affective neuroscience. Psychological Bulletin 126, 890909.Google Scholar
Davis, C., Cowles, M., & Kohn, P. (1984). Behavioural and physiological aspects of the augmenting-reducing dimension. Personality and Individual Differences 5, 683691.Google Scholar
Davis, E., Donzella, B., Krueger, W. K., & Gunnar, M. R. (1999). The start of a new school year: Individual differences in salivary cortisol response in relation to child temperament. Developmental Psychobiology 35, 188196.Google Scholar
Deater–Deckard, K., & Dodge, K. (1997). Spare the rod, spoil the authors: Emerging themes in research on parenting. Psychological Inquiry 8, 230235.Google Scholar
De Bellis, M. D., Baum, A. S., Birmaher, B., Keshavan, M. S., Eccard, C. H., Boring, A. M., Jenkins, F. J., & Ryan, N. D. (1999). A.E. Bennett Research Award. Developmental traumatology. Part I: Biological stress systems. Biological Psychiatry 45, 12591270.Google Scholar
de Haan, M., Gunnar, M. R., Tout, K., Hart, J., & Stansbury, K. (1998). Familiar and novel contexts yield different associations between cortisol and behavior among 2-year-olds. Developmental Psychobiology 31, 93101.Google Scholar
Dhabhar, F. S., McEwen, B. S., & Spencer, R. L. (1993). Stress response, adrenal steroid receptor levels and corticosteroid-binding globulin levels—A comparison between Sprague–Dawley, Fischer 344 and Lewis rats. Brain Research, 616(1–2), 8998.Google Scholar
Doughty, D., & Rodgers, J. L. (2000). Behavior genetic modeling of menarche in U.S. females. In J. L. Rodgers, D. C. Rowe, & W. B. Miller (Eds.), Genetic influences on human fertility and sexuality: Theoretical and empirical contributions from the biological and behavioral sciences. Boston: Kluwer Academic.
Draper, P., & Harpending, H. (1982). Father absence and reproductive strategy: An evolutionary perspective. Journal of Anthropological Research 38, 255273.Google Scholar
Draper, P., & Harpending, H. (1988). A sociobiological perspective on the development of human reproductive strategies. In K. B. MacDonald (Ed.), Sociobiological perspectives on human development (pp. 340372). New York: Springer–Verlag.
Dubos, R. J. (1965). Man adapting. New Haven, CT: Yale University Press.
Dunn, A. J., & Berridge, C. W. (1990). Physiological and behavioral responses to corticotropin-releasing factor administration: Is CRF a mediator of anxiety or stress responses? Brain Research Reviews 15, 71100.Google Scholar
Ekman, P., Levenson, R. W., & Friesen, W. V. (1983). Autonomic nervous system activity distinguishes among emotions. Science 221(4616), 12081210.Google Scholar
Elenkov, I. J., & Chrousos, G. P. (1999). Stress hormones, Th1/Th2 patterns, pro/anti-inflammatory cytokines and susceptibility to disease. Trends in Endocrinology and Metabolism 10, 359368.Google Scholar
Eliasz, A. (1987). Temperament-contingent cognitive orientation toward various aspects of reality. In J. Strelau & J. H. Eysenck (Eds.), Personality dimensions and arousal. Perspectives on individual differences (pp. 197212). New York: Plenum Press.
Ellis, B. J. (2004). Timing of pubertal maturation in girls: An integrated life history approach. Psychological Bulletin 130, 920958.Google Scholar
Ellis, B. J., Bates, J. E., Dodge, K. A., Fergusson, D., Horwood, J., Pettit, G. S., & Woodward, L. (2003). Does early father absence place daughters at special risk for early sexual activity and teenage pregnancy? Child Development 74, 801821.Google Scholar
Ellis, B. J., & Garber, J. (2000). Psychosocial antecedents of variation in girls' pubertal timing: Maternal depression, stepfather presence, and marital and family stress. Child Development 71, 485501.Google Scholar
Ellis, B. J., & Ketelaar, T. (2000). On the natural selection of alternative models: Evaluation of explanations in evolutionary psychology. Psychological Inquiry 11, 5668.Google Scholar
Ellis, B. J., McFadyen–Ketchum, S., Dodge, K. A., Pettit, G. S., & Bates, J. E. (1999). Quality of early family relationships and individual differences in the timing of pubertal maturation in girls: A longitudinal test of an evolutionary model. Journal of Personality & Social Psychology 77, 387401.Google Scholar
Essex, M. J., Klein, M. H., Cho, E., & Kalin, N. H. (2002). Maternal stress beginning in infancy may sensitize children to later stress exposure: Effects on cortisol and behavior. Biological Psychiatry 52, 776784.Google Scholar
Eysenck, H. J. (1967). The biological basis of personality. Springfield, IL: Charles C. Thomas.
Eysenck, H. J., & Eysenck, M. W. (1985). Personality and individual differences: A natural science approach. New York: Plenum Press.
Feldman, R., Greenbaum, C., & Yirmiya, N. (1999). Mother–infant affect synchrony as an antecedent of the emergence of self-control. Developmental Psychology 35, 223231.Google Scholar
Fernald, L. C., & Grantham–McGregor, S. M. (1998). Stress response in school-age children who have been growth retarded since early childhood. American Journal of Clinical Nutrition 68, 691698.Google Scholar
Fox, N. A. (1991). If it's not left, it's right: Electroencephalograph asymmetry and the development of emotion. American Psychologist 46, 863872.Google Scholar
Fox, N. A., & Card, J. A. (1999). Psychophysiological measures in the study of attachment. In J. Cassidy & P. R. Shaver (Eds.), Handbook of attachment: Theory, research, and clinical applications (pp. 226245). New York: Guilford Press.
Fox, N. A., Henderson, H. A., Rubin, K. H., Calkins, S. D., & Schmidt, L. A. (2001). Continuity and discontinuity of behavioral inhibition and exuberance: Psychophysiological and behavioral influences across the first four years of life. Child Development 72, 121.Google Scholar
Fox, N. A., Rubin, K. H., Calkins, S. D., Marshall, T. R., Coplan, R. J., Porges, S. W., Long, J. M., & Stewart, S. (1995). Frontal activation asymmetry and social competence at four years of age. Child Development 66, 17701784.CrossRefGoogle Scholar
Gangestad, S. W., & Simpson, J. A. (2000). The evolution of human mating: Trade-offs and strategic pluralism. Behavioral and Brain Sciences 23, 573644.CrossRefGoogle Scholar
Gannon, L., Banks, J., Shelton, D., & Luchetta, T. (1989). The mediating effects of psychophysiological reactivity and recovery on the relationship between environmental stress and illness. Journal of Psychosomatic Medicine 33, 167175.CrossRefGoogle Scholar
Geen, R. (1984). Preferred stimulation levels in introverts and extraverts: Effects on arousal and performance. Journal of Personality and Social Psychology 46, 13031312.CrossRefGoogle Scholar
Goenjian, A. K., Yehuda, R., Pynoos, R. S., Steinberg, A. M., Tashjian, M., Yang, R. K., Najarian, L. M., & Fairbanks, L. A. (1996). Basal cortisol, dexamethasone suppression of cortisol, and MHPG in adolescents after the 1988 earthquake in Armenia. American Journal of Psychiatry 153, 929934.Google Scholar
Gold, P. W., & Chrousos, G. P. (1999). The endocrinology of melancholic and atypical depression: Relation to neurocircuitry and somatic consequences. Proceedings of the Association of American Physicians 111, 2234.CrossRefGoogle Scholar
Gold, P. W., & Chrousos, G. P. (2002). Organization of the stress system and its dysregulation in melancholic and atypical depression: High vs low CRH/NE states. Molecular Psychiatry 7, 254275.CrossRefGoogle Scholar
Gold, P. W., Goodwin, F. K., & Chrousos, G. P. (1988). Clinical and biochemical manifestations of depression. Relation to the neurobiology of stress (1). New England Journal of Medicine 319, 348353.Google Scholar
Gray, J. A. (1982). The neuropsychology of anxiety: An enquiry into the functions of the septo-hippocampal system. New York: Clarendon/Oxford University Press.
Gray, J. A. (1990). Brain systems that mediate both emotion and cognition. Cognition and Emotion 4, 269288.CrossRefGoogle Scholar
Greene, E. (1989). A diet-induced developmental polymorphism in a caterpillar. Science 243, 643646.CrossRefGoogle Scholar
Greene, E. (1996). Effect of light quality and larval diet on morph induction in the polymorphic caterpillar Nemoria arizonaria (Lepidoptera: Geometridae). Biological Journal of the Linnean Society 58, 277285.Google Scholar
Gross, M. R. (1996). Alternative reproductive strategies and tactics: Diversity within sexes. Trends in Ecology & Evolution 11, 9298.CrossRefGoogle Scholar
Gunnar, M. R. (1994). Psychoendocrine studies of temperament and stress in early childhood: Expanding current models. In J. E. Bates & T. D. Wachs (Eds.), Temperament: Individual differences at the interface of biology and behavior (pp. 175198). Washington, DC: American Psychological Association.
Gunnar, M. R., Morison, S. J., Chisholm, K., & Schuder, M. (2001). Salivary cortisol levels in children adopted from Romanian orphanages. Development and Psychopathology 13, 611628.CrossRefGoogle Scholar
Gunnar, M. R., & Vazquez, D. M. (2001). Low cortisol and a flattening of expected daytime rhythm: Potential indices of risk in human development. Development and Psychopathology 13, 515538.CrossRefGoogle Scholar
Habib, K. E., Gold, P. W., & Chrousos, G. P. (2001). Neuroendocrinology of stress. Neuroendocrinology 30, 695728.CrossRefGoogle Scholar
Harlow, H. F., Harlow, M. K., & Suomi, S. J. (1971). From thought to therapy: Lessons from a primate laboratory. American Scientist 59, 538549.Google Scholar
Heilig, M., Koob, G. F., Ekman, R., & Britton, K. T. (1994). Corticotropin-releasing factor and neuropeptide Y: Role in emotional integration. Trends in Neurosciences 17, 8085.CrossRefGoogle Scholar
Heim, C., Ehlert, U., & Hellhammer, D. H. (2000). The potential role of hypocortisolism in the pathophysiology of stress-related bodily disorders. Psychoneuroendocrinology 25, 135.Google Scholar
Heim, C., & Nemeroff, C. B. (1999). The impact of early adverse experiences on brain systems involved in the pathophysiology of anxiety and affective disorders. Biological Psychiatry 46, 15091522.CrossRefGoogle Scholar
Heim, C., Newport, D. J., Heit, S., Graham, Y. P., Wilcox, M., Bonsall, R., Miller, A. H., & Nemeroff, C. B. (2000). Pituitary–adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. Journal of the American Medical Association 284, 592597.CrossRefGoogle Scholar
Hertsgaard, L., Gunnar, M. R., Erickson, M. F., & Nachmias, M. (1995). Adrenocortical responses to the strange situation in infants with disorganized/disoriented attachment relationships. Child Development 66, 11001106.CrossRefGoogle Scholar
Higley, J. D., & Linnoila, M. (1997). Low central nervous system serotonergic activity is traitlike and correlates with impulsive behavior. A nonhuman primate model investigating genetic and environmental influences on neurotransmission. Annals of the New York Academy of Sciences 836, 3956.Google Scholar
Higley, J. D., Thompson, W. W., Champoux, M., Goldman, D., Hasert, M. F., Kraemer, G. W., Scanlan, J. M., Suomi, S. J., & Linnoila, M. (1993). Paternal and maternal genetic and environmental contributions to cerebrospinal fluid monoamine metabolites in rhesus monkeys (Macaca mulatta). Archives of General Psychiatry 50, 615623.CrossRefGoogle Scholar
Hofer, M. A. (1994). Early relationships as regulators of infant physiology and behavior. Acta Paediatrica Supplement 397, 918.CrossRefGoogle Scholar
Holsboer, F., Lauer, C. J., Schreiber, W., & Krieg, J. C. (1995). Altered hypothalamic–pituitary–adrenocortical regulation in healthy subjects at high familial risk for affective disorders. Neuroendocrinology 62, 340347.Google Scholar
Hrdy, S. B. (1999). Mother nature: Maternal instincts and how they shape the human species. New York: Ballantine Books.
Introini–Collison, I. B., Dalmaz, C., & McGaugh, J. L. (1996). Amygdala beta-noradrenergic influences on memory storage involve cholinergic activation. Neurobiology, Learning and Memory 65, 5764.CrossRefGoogle Scholar
Issa, A. M., Rowe, W., Gauthier, S., & Meaney, M. J. (1990). Hypothalamic–pituitary–adrenal activity in aged, cognitively impaired and cognitively unimpaired rats. Journal of Neuroscience 10, 32473254.Google Scholar
Johnson, M. R., & Adler, L. E. (1993). Transient impairment in P50 auditory sensory gating induced by a cold-pressor test. Biological Psychiatry 33, 380387.CrossRefGoogle Scholar
Jones, B., Leeton, J., McLeod, I., & Wood, C. (1972). Factors influencing the age of menarche in a lower socioeconomic group in Melbourne. Medical Journal of Australia 2, 533535.Google Scholar
Kagan, J. (1994). Galen's prophecy. New York: Basic Books.
Kagan, J. (1997). Conceptualizing psychopathology: The importance of developmental profiles. Development and Psychopathology 9, 114.CrossRefGoogle Scholar
Kagan, J., Reznick, J. S., & Snidman, N. (1987). The physiology and psychology of behavioral inhibition in young children. Child Development 58, 14591473.CrossRefGoogle Scholar
Kagan, J., Reznick, J. S., & Snidman, N. (1988). Biological bases of childhood shyness. Science 240, 167171.CrossRefGoogle Scholar
Kagan, J., Snidman, N., Zentner, M., & Peterson, E. (1999). Infant temperament and anxious symptoms in school age children. Development and Psychopathology 11, 209224.CrossRefGoogle Scholar
Ketelaar, T., & Ellis, B. J. (2000). Are evolutionary explainations unfalsifiable? Evolutionary psychology and the Lakatosian philosophy of science. Psychological Inquiry 11, 121.Google Scholar
Klonowicz, T. (1987). Reactivity and the control of arousal. In J. Strelau & J. H. Eysenck (Eds.), Personality dimensions and arousal. Perspectives on individual differences (pp. 183196). New York: Plenum Press.
Kochanska, G. (1993). Toward a synthesis of parental socialization and child temperament in early development of conscience. Child Development 64, 325347.CrossRefGoogle Scholar
Kochanska, G. (1997). Multiple pathways to conscience for children with different temperaments: From toddlerhood to age 5. Developmental Psychology 33, 228240.CrossRefGoogle Scholar
Kohn, P. M. (1991). Reactivity and anxiety in the laboratory and beyond. In J. Strelau & A. Angleitner (Eds.), Explorations in temperament: International perspectives on theory and measurement. London: Plenum Press.
Kohn, P. M., Hunt, R. W., Cowles, M. P., & Davis, C. A. (1986). Factor structure and construct validity of the Vando Reducer–Augmenter Scale. Personality and Individual Differences 7, 5764.CrossRefGoogle Scholar
Laban, O., Dimitrijevic, M., von Hoersten, S., Markovic, B. M., & Jankovic, B. D. (1995). Experimental allergic encephalomyelitis in adult DA rats subjected to neonatal handling or gentling. Brain Research 676, 133140.CrossRefGoogle Scholar
Lacey, J. I. (1959). Psychophysiological approaches to the evaluation of psychotherapeutic process and outcome. In E. A. Rubinstein & M. B. Parloff (Eds.), Research in psychotherapy (pp. 161196). Washington, DC: American Psychological Association.
Lakatos, I. (1970). Falsificationism and the methodology of scientific research programmes. In I. Lakatos & A. Musgrave (Eds.), Criticism and the growth of knowledge (pp. 91196). Cambridge: Cambridge University Press.
Lakatos, I. (1978). The Methodology of scientific research programmes: Philosophical papers (Vol. 1). Cambridge: Cambridge University Press.CrossRef
Lemne, C. E. (1998). Increased blood pressure reactivity in children of borderline hypertensive fathers. Journal of Hypertension 16, 12431248.CrossRefGoogle Scholar
Lewis, M., & Ramsay, D. S. (1997). Stress reactivity and self-recognition. Child Development 68, 621629.CrossRefGoogle Scholar
Liang, S. W., Jemerin, J. J., Tschann, J. M., Irwin, C. E., Wara, D. W., & Boyce, W. T. (1995). Life events, cardiovascular reactivity, and risk behavior in adolescent boys. Pediatrics 96, 11011105.Google Scholar
Linnoila, M., Virkkunen, M., George, T., Eckardt, M., Higley, J. D., Nielsen, D., Goldman, D. (1994). Serotonin, violent behavior and alcohol. Experientia Supplement 71, 155163.CrossRefGoogle Scholar
Liu, D., & Meaney, M. J. (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic–pituitary–adrenal responses to stress. Science 277, 16591662.CrossRefGoogle Scholar
Lubach, G. R., Coe, C. L., & Ershler, W. B. (1995). Effects of early rearing environment on immune responses of infant rhesus monkeys. Brain Behavior and Immunity 9, 3146.CrossRefGoogle Scholar
Lupien, S. J., King, S., Meaney, M. J., & McEwen, B. S. (2000). Child's stress hormone levels correlate with mother's socioeconomic status and depressive state. Biological Psychiatry 48, 976980.CrossRefGoogle Scholar
Luthar, S. S., Doernberger, C. H., & Zigler, E. (1993). Resilience is not a unidimensional construct: Insights from a prospective study of inner-city adolescents. Development and Psychopathology 5, 703717.CrossRefGoogle Scholar
Lynch, J. W., Everson, S. A., Kaplan, G. A., Salonen, R., & Salonen, J. T. (1998). Does low socioeconomic status potentiate the effects of heightened cardiovascular responses to stress on the progression of carotid atherosclerosis? American Journal of Public Health 88, 389394.Google Scholar
Lyons, D. M., Wang, O. J., Lindley, S. E., Levine, S., Kalin, N. H., & Schatzberg, A. F. (1999). Separation induced changes in squirrel monkey hypothalamic–pituitary–adrenal physiology resemble aspects of hypercortisolism in humans. Psychoneuroendocrinology 24, 131142.CrossRefGoogle Scholar
Lyons, D. M., Yang, C., Sawyer–Glover, A. M., Moseley, M. E., & Schatzberg, A. F. (2001). Early life stress and inherited variation in monkey hippocampal volumes. Archives of General Psychiatry 58, 11451151.CrossRefGoogle Scholar
MacDonald, K. (1995). Evolution, the five-factor model, and levels of personality. Journal of Personality 63, 525567.CrossRefGoogle Scholar
Martin, R. E., Sackett, G. P., Gunderson, V. M., & Goodlin–Jones, B. L. (1988). Auditory evoked heart rate responses in pigtailed macaques (Macaca nemestrina) raised in isolation. Developmental Psychobiology 21, 251260.CrossRefGoogle Scholar
Masten, A. S. (2001). Ordinary magic: Resilience processes in development. American Psychologist 56, 227238.CrossRefGoogle Scholar
Matthews, K. A. (1986). Summary, conclusions and implications. In K. A. Matthews, S. M. Weiss, & T. Detre (Eds.), Handbood of stress, reactivity and cardiovascular disease. New York: Wiley–Interscience.
Matthews, K. A., Manuck, S. B., Stoney, C. M., Rakaczky, C. J., McCann, B. S., Saab, P. G., Woodall, K. L., Block, D. R., Visintainer, P. F., & Engebretson, T. O. (1988). Familial aggregation of blood pressure and heart rate responses during behavioral stress. Psychosomatic Medicine 50, 341352.CrossRefGoogle Scholar
McCormick, D. A., & Bal, T. (1994). Sensory gating mechanisms of the thalamus. Current Opinion in Neurobiology 4, 550556.CrossRefGoogle Scholar
McEwen, B. S. (1998). Protective and damaging effects of stress mediators. New England Journal of Medicine 338, 171179.CrossRefGoogle Scholar
McEwen, B. S., & Stellar, E. (1993). Stress and the individual. Mechanisms leading to disease. Archives of Internal Medicine 153, 20932101.CrossRefGoogle Scholar
Mealey, L. (1995). The sociobiology of sociopathy: An integrated evolutionary model. Behavioral and Brain Sciences 18, 523599.CrossRefGoogle Scholar
Mealey, L. (2000). Sex differences: Development and evolutionary strategies. San Diego, CA: Academic Press.
Mealey, L. (2001). Kinship: The tie that binds (disciplines). In H. Holcomb (Ed.), Conceptual challenges in evolutionary psychology. New York: Kluwer Academic.
Meaney, M. J. (2001). Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annual Review of Neuroscience 24, 11611192.CrossRefGoogle Scholar
Meyer, J. S., & Bowman, R. E. (1972). Rearing experience, stress and adrenocorticosteroids in the rhesus monkey. Physiology & Behavior 8, 339343.CrossRefGoogle Scholar
Meyer, S. E., Chrousos, G. P., & Gold, P. W. (2001). Major depression and the stress system: A life span perspective. Development and Psychopathology 13, 565580.CrossRefGoogle Scholar
Moffitt, T. E., Caspi, A., Belsky, J., & Silva, P. A. (1992). Childhood experience and the onset of menarche: A test of a sociobiological model. Child Development 63, 4758.CrossRefGoogle Scholar
Munck, A., Guyre, P. M., & Holbrook, N. J. (1984). Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocrine Reviews 5, 2543.CrossRefGoogle Scholar
Musante, L., Treiber, F. A., Kapuku, G., Moore, D., Davis, H., & Strong, W. B. (2000). The effects of life events on cardiovascular reactivity to behavioral stressors as a function of socioeconomic status, ethnicity, and sex. Psychosomatic Medicine 62, 760767.CrossRefGoogle Scholar
Nachmias, M., Gunnar, M. R., Mangelsdorf, S., Parritz, R. H., & Buss, K. (1996). Behavioral inhibition and stress reactivity: The moderating role of attachment security. Child Development 67, 508522.CrossRefGoogle Scholar
Neiss, R. (1988). Reconceptualizing arousal: Psychobiological states in motor performance. Psychological Bulletin 103, 345366.CrossRefGoogle Scholar
Nesse, R. M., & Young, E. A. (2000). Evolutionary origins and functions of the stress response. In G. Fink (Ed.), Encyclopedia of stress (Vol. 2, pp. 7984). New York: Academic Press.
Neylan, T. C., Fletcher, D. J., Lenoci, M., McCallin, K., Weiss, D. S., Schoenfeld, F. B., Marmar, C. R., & Fein, G. (1999). Sensory gating in chronic posttraumatic stress disorder: Reduced auditory P50 suppression in combat veterans. Biological Psychiatry 46, 16561664.CrossRefGoogle Scholar
Owens, M. J., & Nemeroff, C. B. (1991). Physiology and pharmacology of corticotropin-releasing factor. Pharmacological Reviews 43, 425473.Google Scholar
Patterson, C. M., & Newman, J. P. (1993). Reflectivity and learning from aversive events: Toward a psychological mechanism for the syndromes of disinhibition. Psychological Review 100, 716736.CrossRefGoogle Scholar
Perry, B. (1994). Neurobiological sequelae of childhood trauma: PTSD in children. In M. Murburg (Ed.), Catecholamine function in post-traumatic stresss disorder: Emerging concepts (pp. 233255). Washington, DC: American Psychiatric Press.
Plotsky, P. M., & Meaney, M. J. (1993). Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Molecular Brain Research 18, 195200.CrossRefGoogle Scholar
Quas, J. A., Bauer, A. M., & Boyce, W. T. (2004). Physiological reactivity, social support, and memory in early childhood. Child Development. 75(3) 797814CrossRefGoogle Scholar
Quas, J. A., Hong, M., Alkon, A., & Boyce, W. T. (2000). Dissociations between psychobiologic reactivity and emotional expression in children. Developmental Psychobiology 37, 153175.3.0.CO;2-Y>CrossRefGoogle Scholar
Raine, A., Venables, P. H., & Mednick, S. A. (1997). Low resting heart rate at age 3 years predisposes to aggression at age 11 years: Evidence from the Mauritius Child Health Project. Journal of the American Academy of Child and Adolescent Psychiatry 36, 14571464.CrossRefGoogle Scholar
Reis, D. J., & Golanov, E. V. (1997). Autonomic and vasomotor regulation. International Review of Neurobiology 41, 121149.CrossRefGoogle Scholar
Reznick, J. S., Kagan, J., Snidman, N., Gersten, M., Baak, K., & Rosenberg, A. (1986). Inhibited and uninhibited children: A follow-up study. Child Development 57, 660680.CrossRefGoogle Scholar
Rolls, E. T. (1999). The brain and emotion. Oxford: Oxford University Press.
Sanchez, M. M., Ladd, C. O., & Plotsky, P. M. (2001). Early adverse experience as a developmental risk factor for later psychopathology: Evidence from rodent and primate models. Development and Psychopathology 13, 419449.CrossRefGoogle Scholar
Sapolsky, R. M. (1990). Adrenocortical function, social rank, and personality among wild baboons. Biological Psychiatry 28, 862885.CrossRefGoogle Scholar
Sapolsky, R. M. (1996). Why stress is bad for your brain. Science 273, 749750.CrossRefGoogle Scholar
Sapolsky, R. M., Romero, L. M., & Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21, 5589.Google Scholar
Sapolsky, R. M., & Share, L. J. (1994). Rank-related differences in cardiovascular function among wild baboons: Role of sensitivity to glucocorticoids. American Journal of Primatology 32, 261275.CrossRefGoogle Scholar
Scarpa, A., & Raine, A. (1997). Psychophysiology of anger and violent behavior. Psychiatric Clinics of North America 20, 375394.CrossRefGoogle Scholar
Schlichting, C. D., & Pigliucci, M. (1998). Phenotypic evolution: A reaction norm perspective. Sunderland, MA: Sinauer Associates.
Schmidt, L. A., Fox, N. A., Schulkin, J., & Gold, P. W. (1999). Behavioral and psychophysiological correlates of self-presentation in temperamentally shy children. Developmental Psychobiology 35, 119135.3.0.CO;2-G>CrossRefGoogle Scholar
Selye, H. (1950). Stress: The physiology and pathology of exposure to stress. Montreal: Acta Medical Publishers.
Shannon, C., Champoux, M., & Suomi, S. J. (1998). Rearing condition and plasma cortisol in rhesus monkey infants. American Journal of Primatology 46, 311321.3.0.CO;2-L>CrossRefGoogle Scholar
Shimamura, A. P. (2000). The role of the prefrontal cortex in dynamic filtering. Psychobiology 28, 207218.Google Scholar
Slobodkin, L., & Rapoport, A. (1974). An optimal strategy of evolution. Quarterly Review of Biology 49, 181200.CrossRefGoogle Scholar
Smith, G. W., Aubry, J. M., Dellu, F., Contarino, A., Bilezikjian, L. M., Gold, L. H., Chen, R., Marchuk, Y., Hauser, C., Bentley, C. A., Sawchenko, P. E., Koob, G. F., Vale, W., & Lee K. F. (1998). Corticotropin releasing factor receptor 1-deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development. Neuron 20, 10931102.CrossRefGoogle Scholar
Snidman, N., Kagan, J., Riordan, L., & Shannon, D. C. (1995). Cardiac function and behavioral reactivity during infancy. Psychophysiology 32, 199207.CrossRefGoogle Scholar
Stein, M. B., Yehuda, R., Koverola, C., & Hanna, C. (1997). Enhanced dexamethasone suppression of plasma cortisol in adult women traumatized by childhood sexual abuse. Biological Psychiatry 42, 680686.CrossRefGoogle Scholar
Stevens, K. E., Bullock, A. E., & Collins, A. C. (2001). Chronic corticosterone treatment alters sensory gating in C3H mice. Pharmacology Biochemistry and Behavior 69, 359366.CrossRefGoogle Scholar
Stevenson–Hinde, J., & Marshall, P. J. (1999). Behavioral inhibition, heart period, and respiratory sinus arrhythmia: An attachment perspective. Child Development 70, 805816.CrossRefGoogle Scholar
Strelau, J. (1983). Temperament personality activity. New York: Academic Press.
Strelau, J., & Eysenck, H. J. (1987). Personality dimensions and arousal. New York: Plenum Press.CrossRef
Suomi, S. J. (1987a). Individual differences in rhesus monkey behavioral and adrenocortical responses to social challenge: Correlations with measures of heart rate variability. Paper presented at the Heart Rate Variability and Social Behavior: Behavioral and Biological Correlates Conference, Baltimore, MD.
Suomi, S. J. (1987b). Genetic and maternal contributions to individual differences in Rhesus monkey biobehavioral development. In N. Krasnagor (Ed.), Psychobiological aspects of behavioral development (pp. 397419). New York: Academic Press.
Suomi, S. J. (1997). Early determinants of behaviour: Evidence from primate studies. British Medical Bulletin 53, 170184.CrossRefGoogle Scholar
Surbey, M. K. (1990). Family composition, stress, and the timing of human menarche. In T. E. Ziegler (Ed.), Socioendocrinology of primate reproduction. Monographs in primatology (pp. 1132). New York: Wiley–Liss.
Taub, J. M. (1998). Eysenck's descriptive and biological theory of personality: A review of construct validity. International Journal of Neuroscience 94, 145197.CrossRefGoogle Scholar
Turkheimer, E., & Gottesman, I. I. (1991). Individual differences and the canalization of human behavior. Developmental Psychology 27, 1822.CrossRefGoogle Scholar
Turner, J. R., & Hewitt, J. K. (1992). Twin studies of cardiovascular response to psychological challenge: A review and suggested future directions. Annals of Behavioral Medicine 14, 1220.Google Scholar
Valentino, R. J., Curtis, A. L., Page, M. E., Pavcovich, L. A., & Florin–Lechner, S. M. (1998). Activation of the locus ceruleus brain noradrenergic system during stress: Circuitry, consequences, and regulation. Advances in Pharmacology 42, 781784.Google Scholar
van der Saag, P. T., Caldenhoven, E., & van de Stolpe, A. (1996). Molecular mechanisms of steroid action: A novel type of cross-talk between glucocorticoids and NF-kappa B transcription factors. European Respiratory Journal, Supplement 22, 146s153s.Google Scholar
Vazquez, D. M., Watson, S. J., & Lopez, J. F. (2000, July). Failure to terminate stress responses in children with psychosocial dwarfism: A mechanism for growth failure. Paper presented at the International Conference of Infant Studies, Brighton, UK.
Viau, V. (2002). Functional cross-talk between the hypothalamic–pituitary–gonadal and –adrenal axes. Journal of Neuroendocrinology 14, 506513.CrossRefGoogle Scholar
von Bertalanffy, L. (1968). General system theory: Foundations, development, applications. New York: George Braziller.
Waddington, C. H. (1966). Principles of development and differentiation. New York: MacMillan.
Waldo, M., Myles–Worsley, M., Madison, A., Byerley, W., & Freedman, R. (1995). Sensory gating deficits in parents of schizophrenics. American Journal of Medical Genetics 60, 506511.CrossRefGoogle Scholar
Ward, H. E., Johnson, E. A., Salm, A. K., & Birkle, D. L. (2000). Effects of prenatal stress on defensive withdrawal behavior and corticotropin releasing factor systems in rat brain. Physiology & Behavior 70, 359366.CrossRefGoogle Scholar
White, B. P., Gunnar, M. R., Larson, M. C., Donzella, B., & Barr, R. G. (2000). Behavioral and physiological responsivity and patterns of sleep and daily salivary cortisol in infants with and without colic. Child Development 71, 862877.CrossRefGoogle Scholar
Willemsen–Swinkels, S. H., Bakermans–Kranenburg, M. J., Buitelaar, J. K., van, I. M. H., & van Engeland, H. (2000). Insecure and disorganised attachment in children with a pervasive developmental disorder: Relationship with social interaction and heart rate. Journal of Child Psychology and Psychiatry and Allied Disciplines 41, 759767.CrossRefGoogle Scholar
Worthman, C. M., Angold, A., & Costello, E. J. (1998). Stress, reactivity and psychiatric risk in adolescents. Paper presented at the Biennial Meeting of the Society for Research on Adolescence, San Diego, CA, February 26–28.
Yehuda, R. (2002). Post-traumatic stress disorder. New England Journal of Medicine 346, 108114.CrossRefGoogle Scholar
Yehuda, R., Halligan, S. L., & Bierer, L. M. (2001). Relationship of parental trauma exposure and PTSD to PTSD, depressive and anxiety disorders in offspring. Journal of Psychiatric Research 35, 261270.CrossRefGoogle Scholar
Yehuda, R., Halligan, S. L., & Grossman, R. (2001). Childhood trauma and risk for PTSD: Relationship to intergenerational effects of trauma, parental PTSD, and cortisol excretion. Development and Psychopathology 13, 733753.CrossRefGoogle Scholar
Yehuda, R., McFarlane, A. C., & Shalev, A. Y. (1998). Predicting the development of posttraumatic stress disorder from the acute response to a traumatic event. Biological Psychiatry 44, 13051313.CrossRefGoogle Scholar
Yerkes, R. M., & Dodson, J. D. (1908). The relation of strength of stimulus to rapidity of habit formation. Journal of Comparative Neurology and Psychology 18, 459482.CrossRefGoogle Scholar
Zaharia, M. D., Kulczycki, J., Shanks, N., Meaney, M. J., & Anisman, H. (1996). The effects of early postnatal stimulation on Morris water-maze acquisition in adult mice: Genetic and maternal factors. Psychopharmacology (Berlin) 128, 227239.CrossRefGoogle Scholar
Zuckerman, M. (1984). Sensation seeking: A comparative approach to a human trait. Behavioral and Brain Sciences 7, 413471.CrossRefGoogle Scholar