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Biological sensitivity to context: II. Empirical explorations of an evolutionary–developmental theory

Published online by Cambridge University Press:  12 May 2005

BRUCE J. ELLIS ,
MARILYN J. ESSEX  and
W. THOMAS BOYCE
BRUCE J. ELLIS
Affiliation:
University of Arizona
MARILYN J. ESSEX
Affiliation:
University of Wisconsin
W. THOMAS BOYCE
Affiliation:
University of California, Berkeley
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Abstract

In two studies comprising 249 children and their families, the authors utilized secondary, exploratory data analyses to examine Boyce and Ellis' (this issue) evolutionary–developmental theory of biological sensitivity to context. The theory proposes that individual differences in stress reactivity constitute variation in susceptibility to environmental influence, both positive and negative, and that early childhood exposures to either highly protective or acutely stressful environments result in heightened reactivity. In Study 1, 127 3- to 5-year old children were concurrently assessed on levels of support/adversity in home and preschool environments and on cardiovascular reactivity to laboratory challenges. In Study 2, 122 children were prospectively assessed on familial stress in both infancy and preschool and on autonomic and adrenocortical reactivity to laboratory challenges at age 7. In both studies, a disproportionate number of children in supportive, low stress environments displayed high autonomic reactivity. Conversely, in Study 2, a relatively high proportion of children in very stressful environments showed evidence of heightened sympathetic and adrenocortical reactivity. Consistent with the evolutionary–developmental theory, the exploratory analyses also generated the testable hypothesis that relations between levels of childhood support/adversity and the magnitude of stress reactivity are curvilinear, with children from moderately stressful environments displaying the lowest reactivity levels in both studies.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 the National Institute of Mental Health (R01-MH44340 and P50-MH53524). We thank Jay Belsky and David Bjorklund for comments on an earlier draft of this paper.

Type
Research Article
Information
Development and Psychopathology , Volume 17 , Issue 2 , June 2005 , pp. 303 - 328
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Abidin, R. R. (1986). Parenting Stress Index (2nd ed.). Charlottesville, VA: Pediatric Psychology Press.
Ablow, J. C., Measelle, J. R., Kraemer, H. C., Harrington, R., Luby, J., Smider, N., Dierker, L., Clark, V., Dubicka, B, Heffelfinger, A., Essex. M. J., &Kupfer, D. J. (1999). The MacArthur Three-City Outcome Study: Evaluating multi-informant measures of young children's symptomatology. Journal of the American Academy of Child and Adolescent Psychiatry 38, 1580–1590.CrossRefGoogle 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, 64–78.CrossRefGoogle 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, 329–339. [Erratum p. 730]CrossRefGoogle Scholar
Anisman, H., Zaharia, M. D., Meaney, M. J., & Merali, Z. (1998). Do early-life events permanently alter behavioral and hormonal responses to stressors? International Journal of Developmental Neuroscience 16, 149–164.Google Scholar
Barnett, R. C., & Marshall, N. L. (1989). Preliminary manual for the role-quality scales. Unpublished manuscript, Wellesley College, Center for Research on Women.
Barr, C. S., Newman, T. K., Becker, M. L., Parker, C. C., Champoux, M., Lesch, K. P., Goldman, D., Suomi, S. J., & Higley, J. D. (2003). The utility of the non-human primate model for studying gene by environment interactions in behavioral research. Genes, Brain, and Behavior 2, 336–340.CrossRefGoogle Scholar
Barr, C. S., Newman, T. K., Lindell, S., Shannon, C., Champoux, M., Lesch, K. P., Suomi, S. J., Goldman, D., & Higley, J. D. (2004). Interaction between serotonin transporter gene variation and rearing condition in alcohol preference and consumption in female primates. Archives of General Psychiatry 61, 1146–1152.CrossRefGoogle Scholar
Bauer, A. M., Quas, J. A., & Boyce, W. T. (2002). Concurrent sympathetic and adrenocortical activity as predictors of behavior in middle childhood. Unpublished manuscript.
Belsky, J., Steinberg, L., & Draper, P. (1991). Childhood experience, interpersonal development, and reproductive strategy: An evolutionary theory of socialization. Child Development 62, 647–670.CrossRefGoogle Scholar
Bennett, A. J., Lesch, K. P., Heils, A., Long, J. C., Lorenz, J. G., Shoaf, S. E., Champoux, M., Suomi, S. J., Linnoila, M. V., & Higley, J. D. (2002). Early experience and serotonin transporter gene variation interact to influence primate CNS function. Molecular Psychiatry 7, 118–122.CrossRefGoogle Scholar
Berntson, G. G., Quigley, K. S., Jang, J., & Boysen, S. T. (1990). A conceptual approach to artifact identification: Application to heart period data. Psychophysiology 27, 568–598.Google Scholar
Block, J. H. (1965). The Child-Rearing Practices Report (CRPR). Berkeley, CA: University of California, Institute of Human Development.
Boyce, W. T., Alkon, A., Tschann, J. M., Chesney, M. A., & Alpert, B. S. (1995). Dimensions of psychobiologic reactivity: Cardiovascular responses to laboratory stressors in preschool children. Annals of Behavioral Medicine 17, 315–323.CrossRefGoogle 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, 411–422.CrossRefGoogle Scholar
Boyce, W. T., & Ellis, B. J. (2005). Biological sensitivity to context: I. An evolutionary–developmental theory of the origins and functions of stress reactivity. Development and Psychopathology 17, 271–301.Google Scholar
Boyce, W. T., Essex, M., Woodward, H. R., Measelle, J. R., Ablow, J. C., & Kupfer, D. J. (2002). The confluence of mental, physical, social and academic difficulties in middle childhood: I. Exploring the “headwaters” of early life morbidities. Journal of the American Academy of Child and Adolescent Psychiatry 41, 580–587.CrossRefGoogle Scholar
Boyce, W. T., Jensen, E. W., & James, S. A. (1983). The Family Routines Inventory: Theoretical origins. Social Science & Medicine 17, 193–200.CrossRefGoogle 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, 285–289.CrossRefGoogle 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, 144–150.CrossRefGoogle Scholar
Brown, G. W., & Davidson, S. (1978). Social class, psychiatric disorder of mother, and accidents to children. Lancet February, 378–381.Google Scholar
Cacioppo, J. T., Berntson, G. G., Binkley, P. F., Quigley, K. S., Uchino, B. N., & Fieldstone, A. (1994). Autonomic cardiac control. II. Noninvasive indices and basal response as revealed by autonomic blockades. Psychophysiology 31, 586–598.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, 829–843.CrossRefGoogle Scholar
Cacioppo, J. T., Uchino, B. N., & Berntson, G. G. (1994). Individual differences in the autonomic origins of heart rate reactivity: The psychometrics of respiratory sinus arrhythmia and preejection period. Psychophysiology 31, 412–419.CrossRefGoogle Scholar
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, 419–428.CrossRefGoogle Scholar
Carlson, R. D. (1985). Gesell School Readiness Test. In D. Keyser & R. Sweetland (Eds.), Test critiques. Kansas City, MO: Test Corp of America.
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, 461–477.CrossRefGoogle Scholar
Chisholm, J. S. (1999). Death, hope and sex: Steps to an evolutionary ecology of mind and morality. New York: Cambridge University Press.CrossRef
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, 311–335.Google Scholar
Coddington, R. D. (1972). The significance of life events as etiologic factors in the diseases of children: II—A study of a normal population. Journal of Psychosomatic Research 16, 205–213.CrossRefGoogle 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, 1259–1270.Google Scholar
DeLongis, A., Coyne, J. C., Dakof, G., Folkman, S., & Lazarus, R. S. (1982). Relationship of daily hassles, uplifts, and major life events to health status. Health Psychology 1, 119–136.Google Scholar
DeLongis, A., Folkman, S., & Lazarus, R. S. (1988). The impact of daily stress on health and mood: Psychological and social resources as mediators. Journal of Personality and Social Psychology 54, 486–495.CrossRefGoogle Scholar
Eisenberg, N., Fabes, R. A., Bustamante, D., Mathy, R. M., Miller, P. A., & Lindholm, E. (1988). Differentiation of vicariously induced emotional reactions in children. Developmental Psychology 24, 237–246.CrossRefGoogle Scholar
Essex, M. J., Boyce, W. T., Goldstein, L. H., Armstrong, J. M., Kraemer, H. C., & Kupfer, D. J. (2002). The confluence of mental, physical, social, and academic difficulties in middle childhood: II. Developing the MacArthur Health & Behavior Questionnaire. Journal of the American Academy of Child and Adolescent Psychiatry 41, 588–603.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, 776–784.CrossRefGoogle Scholar
Ewart, C. K., & Kolodner, K. B. (1991). Social competence interview for assessing physiologic reactivity in adolescents. Psychosomatic Medicine 53, 289–304.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, 254–275.CrossRefGoogle Scholar
Gold, P. W., Goodwin, F. K., & Chrousos, G. P. (1988). Clinical and biochemical manifestations of depression. Relation to the neurobiology of stress. New England Journal of Medicine 319, 348–353.Google 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, 515–538.CrossRefGoogle Scholar
Halberstadt, A. G. (1986). Family socialization of emotional expression and non-verbal communication style and skills. Journal of Personality and Social Psychology 51, 827–836.CrossRefGoogle 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, 615–623.CrossRefGoogle Scholar
Hofer, M. A. (1994). Early relationships as regulators of infant physiology and behavior. Acta Paediatrica Supplement 397, 9–18.CrossRefGoogle Scholar
Hyde, J. S., Klein, M. H., Essex, M. J., & Clark, R. (1995). Maternity leave and women's mental health. Psychology of Women Quarterly 19, 257–285.CrossRefGoogle Scholar
Jensen, E., James, S., & Boyce, W. (1983). The Family Routines Inventory: Development and validation. Social Science & Medicine 17, 210–211.CrossRefGoogle Scholar
Kagan, J. (1994). Galen's prophecy. New York: Basic Books.
Kagan, J., Reznick, J. S., & Snidman, N. (1988). Biological bases of childhood shyness. Science 240, 167–171.CrossRefGoogle Scholar
Kamarck, T. W., Jennings, J. R., Debski, T. T., Glickman–Weiss, E., Johnson, P. S., Eddy, M. J., & Manuck, S. B. (1992). Reliable measures of behaviorally-evoked cardiovascular reactivity from a PC-based test battery: Results from student and community samples. Psychophysiology 29, 17–28.CrossRefGoogle Scholar
Kanner, A. D., Feldman, S. S., Weinberger, D. A., & Ford, M. E. (1987). Uplifts, hassles, and adaptational outcomes in preadolescents. Journal of Early Adolescence 7, 371–394.CrossRefGoogle Scholar
Kaufman, A. S., & Kaufman, N. L. (1983). Kaufman Assessment Battery for Children. Circle Pines, MN: American Guidance Service.
Kirschbaum, C., & Hellhammer, D. H. (1994). Salivary cortisol in psychoneuroendocrine research: Recent developments and applications. Psychoneuroendocrinology 19, 313–333.CrossRefGoogle Scholar
Kraemer, H. C. (1992). Evaluating medical tests: Objective and quantitative guidelines. Newbury Park, CA: Sage.
Manuck, S. B., Kasprowicz, A. L., & Muldoon, M. F. (1990). Behaviorally-evoked cardiovascular reactivity and hypertension: Conceptual issues and potential associations. Annals of Behavioral Medicine 12, 17–29.CrossRefGoogle Scholar
Matthews, K. A., Woodall, K. L., & Stoney, C. M. (1990). Changes in and stability of cardiovascular responses to behavioral stress: Results from a four-year longitudinal study of children. Child Development 61, 1134–1144.CrossRefGoogle Scholar
McEwen, B. S. (1998). Protective and damaging effects of stress mediators. New England Journal of Medicine 338, 171–179.CrossRefGoogle Scholar
McEwen, B. S. (2000). The neurobiology of stress: From serendipity to clinical relevance. Brain Research 886, 172–189.CrossRefGoogle Scholar
Meaney, M. J. (2001). Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annual Review of Neuroscience 24, 1161–1192.CrossRefGoogle Scholar
Monaghan, J. H., Robinson, J. O., & Dodge, J. A. (1979). The children's life events inventory. Journal of Psychosomatic Research 23, 63–68.CrossRefGoogle Scholar
Moos, R., Insel, P., & Humphrey, B. (1974). Family environment scale: Preliminary manual. Palo Alto, CA: Consulting Psychologists Press.
Murphy, J. K., Alpert, B. S., Willey, E. S., & Somes, G. W. (1988). Cardiovascular reactivity to psychological stress in healthy children. Psychophysiology 25, 144–152.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, 508–522.CrossRefGoogle Scholar
Park, M., & Menard, S. (1987). Accuracy of blood pressure measurement by the Dinamap monitor in infants and children. Pediatrics 79, 907–914.Google Scholar
Porges, S. W. (1995). Orienting in a defensive world: Mammalian modifications of our evolutionary heritage. A polyvagal theory. Psychophysiology 32, 301–318.Google Scholar
Radloff, L. S. (1977). The CES-D scale: A self-report depression scale for research in the general population. Applied Psychological Measurement 1, 385–401.CrossRefGoogle Scholar
Rubin, K. H. (1988). The Social Problem-Solving Test—Revised. Unpublished manuscript, University of Waterloo.
Sallis, J. F., Broyles, S. L., Nader, P. R., Buono, M. J., Abramson, I. S., Patterson, T. L., & Nelson, J. A. (1991). Blood pressure reactivity to exercise: Stability, determinants, family aggregation, and prediction. Journal of Developmental and Behavioral Pediatrics 12, 162–170.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, 55–89.Google Scholar
Sarason, I. G., Levine, H. M., Basham, R. B., & Sarason, B. R. (1983). Assessing social support: The Social Support Questionnaire. Journal of Personality and Social Psychology 44, 127–139.CrossRefGoogle Scholar
Spielberger, C. D. (1988). Manual for the State-Trait Anger Expression Inventory (STAXI). Odessa, FL: Psychological Assessment Resources.
Suomi, S. J. (1991). Early stress and adult emotional reactivity in rhesus monkeys. In G. R. Bock & J. Whelan (Eds.), The childhood environment and adult disease (pp. 171–188). Chichester: Wiley.
Suomi, S. J. (1997). Early determinants of behaviour: Evidence from primate studies. British Medical Bulletin 53, 170–184.CrossRefGoogle Scholar
Swets, J. A., & Pickett, R. M. (1982). Evaluation of diagnostic systems: Methods from signal detection theory. New York: Academic Press.
Tooby, J., & Cosmides, L. (1990). On the universality of human nature and the uniqueness of the individual: The role of genetics and adaptation. Journal of Personality 58, 17–67.CrossRefGoogle Scholar
Yehuda, R., Halligan, S. L., & Grossman, R. (2001). Childhood trauma and risk for PTSD: Relationship to intergenerational effects of trauma, parental posttraumatic stress disorder, and cortisol excretion. Development and Psychopathology 13, 733–753.CrossRefGoogle Scholar