Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-22T18:18:58.831Z Has data issue: false hasContentIssue false

Maternal responsiveness moderates the relationship between allostatic load and working memory

Published online by Cambridge University Press:  15 July 2011

Stacey N. Doan*
Affiliation:
Boston University
Gary W. Evans
Affiliation:
Cornell University
*
Address correspondence and reprint requests to: Stacey N. Doan, Department of Psychology, Boston University, 64 Cummington Street, Boston, MA 02215; E-mail: [email protected].

Abstract

A substantial amount of research has demonstrated the deleterious effects of chronic stress on memory. However, much less is known about protective factors. In the current study we test the role of maternal responsiveness in buffering the effects of childhood allostatic load on subsequent adolescent working memory. Allostatic load is a marker of cumulative stress on the body that is caused by mobilization of multiple physiological systems in response to chronic environmental demands. Results of the study suggest that allostatic load negatively affects working memory, but that this effect is significantly attenuated in children with responsive mothers.

Type
Articles
Copyright
Copyright © Cambridge University Press 2011

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

Aiken, L., & West, S. (1991). Multiple regression: Testing and interpreting interactions. Los Angeles: Sage.Google Scholar
Baddeley, A. D. (2003). Working memory: Looking back and looking forward. Nature Reviews Neuroscience, 4, 829839.CrossRefGoogle ScholarPubMed
Belsky, J., Crnic, K., & Woodsworth, S. (1995). Personality and parenting: Exploring the mediating role of transient mood and daily hassles. Journal of Personality, 63, 905929.CrossRefGoogle ScholarPubMed
Bornstein, M. H. (1989). Maternal responsiveness characteristics and consequences. San Francisco, CA: Jossey–Bass.Google Scholar
Bradley, R. H., Caldwell, B. M., & Rock, S. L. (1990). Home environment classification system: A model for assessing the home environments of development children. Early Education and Development, 1, 238265.CrossRefGoogle Scholar
Bradley, R. H., Whiteside, L., Mundform, D., Casey, P., Kelleher, K., & Pope, S. (1994). Early indications of resilience and their relation to experiences in the home environments of low birthweight, premature children living in poverty. Child Development, 65, 346360.CrossRefGoogle ScholarPubMed
Buss, C., Wolf, O. T., Witt, J., & Hellhammer, D. H. (2004). Autobiographic memory impairment following acute cortisol administration. Psychoneuroendocrinology, 29, 10931096.CrossRefGoogle ScholarPubMed
Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P., & Meaney, M. (1998). Maternal care during infancy regulates the development of neural systems mediating the expression of behavioral fearlessness in adulthood in the rat. Proceedings of the National Academy of Sciences of the United States of America, 95, 53355340.CrossRefGoogle Scholar
Cicchetti, D., & Curtis, W. J. (2007). A multilevel approach to resilience. Development and Psychopathology, 19, 627955.CrossRefGoogle Scholar
Cicchetti, D., & Tucker, D. (1994). Development and self-regulatory structures of the mind. Development and Psychopathology, 6, 533549.CrossRefGoogle Scholar
Contreras, L. N.Hane, S., & Tyrrell, J. B. (1986). Urinary cortisol in the assessment of pituitary–adrenal function: Utility of 24-hour and spot determinations. Journal of Clinical Endocrinological Metabolism, 62, 876969.CrossRefGoogle ScholarPubMed
Curtis, W. J., & Cicchetti, D. (2003). Moving research on resilience into the 21st century: Theoretical and methodological considerations in examining the biological contributors to resilience. Development and Psychopathology, 15, 773810.CrossRefGoogle ScholarPubMed
de Quervain, D. J., Roozendaal, B., Nitsch, R. M., McGaugh, J. L., & Hock, C. (2000). Acute cortisone administration impairs retrieval of long-term declarative memory in humans. Nature Neuroscience, 3, 313314.CrossRefGoogle ScholarPubMed
Elzinga, B. M., Bakker, A., & Brenner, J. D. (2005). Stress-indcued coritsol elevations are associated with imparied delayed, but not immediate recall. Psychiatry Research, 134, 211223.CrossRefGoogle Scholar
Elzinga, B. M., & Roelofs, K. (2005). Cortisol-induced impairments of working memory require acute sympathetic activation. Behavioral Neuroscience, 119, 98103.CrossRefGoogle ScholarPubMed
Evans, G. W. (2003). A multimethodological analysis of cumulative risk and allostatic load among rural children. Developmental Psychology, 39, 924933.CrossRefGoogle ScholarPubMed
Evans, G. W., Kim, P., Ting, A., Tesher, H., & Shannis, D. (2007). Cumulative risk, maternal responsiveness, and allostatic load among young adolescents. Developmental Psychology, 43, 341351.CrossRefGoogle ScholarPubMed
Evans, G. W., & Shamberg, M. (2009). Childhood poverty, chronic stress and adult working memory. Proceedings of the National Academy of Sciences of the United States of America, 106, 65456549.CrossRefGoogle ScholarPubMed
Farah, M., Betancourt, L., Shera, D., Savage, J., Gianetta, J., Brodksy, N., et al. (2008). Environmental stimulation, parental nurturance and cognitive development in humans. Developmental Science, 11, 793801.CrossRefGoogle ScholarPubMed
Farah, M. J., Shera, D. M., Savage, J. H., Betancourt, L., Gianetta, J. M., Brodsky, N. L., et al. (2006). Childhood poverty, specific associations with neurocognitive development. Brain Research, 1110, 166174.CrossRefGoogle ScholarPubMed
Feldman, R., & Masalha, S. (2007). The role of culture in moderating the links between early ecological risk and young children's adaptation. Development and Psychopathology, 19, 121.CrossRefGoogle ScholarPubMed
Fish, E., Shahroky, D., Bagot, R., Caldji, C., Bredy, T., Szyf, M., et al. (2004). Epigenetic programming of stress responses through variations in maternal care. Annuals of the New York Academy of Sciences, 1036, 167180.CrossRefGoogle ScholarPubMed
Fivush, R., Haden, C. A., & Reese, E. (2006). Elaborating on elaborations: The role of maternal reminiscing style in cognitive and socioemotional development. Child Development, 77, 15681588.CrossRefGoogle ScholarPubMed
Francis, D., & Meaney, M. (1999). Maternal care and the development of stress responses. Current Opinion in Neurobiology, 9, 128134.CrossRefGoogle ScholarPubMed
Fuster, J. M. (1980). The prefrontal cortex. New York: Raven.Google Scholar
Fuster, J. M. (2000). The prefrontal cortex of the primate: A synopsis. Psychobiology, 28, 125131.CrossRefGoogle Scholar
Gramezy, N. (1985). Stress-resistant children: The search for protective factors. In Stevenson, J. E. (Ed.), Recent research in developmental psychopathology. Journal of Child Psychology and Psychiatry (Book Suppl. 4, pp. 213233). Oxford: Pergamon Press.Google Scholar
Kagan, J. (2001). Biological constraint, cultural variety, and psychological structures. Annals of the New York Academy of Sciences, 935, 177190.CrossRefGoogle ScholarPubMed
Kamarck, T., Jennings, R., Debski, T., Glicksman-Weis, E. Johnson, P., Eddy, M., et al. (1992). Reliable measures of behaviorally evoked cardiovascular reactivity from a PC-based test battery. Psychophysiology, 29, 1728.CrossRefGoogle ScholarPubMed
Kubzansky, L. D., Kawachi, I., & Sparrow, D. (1999). Socioeconomic status, hostility, and risk factor clustering in the normative aging study: Any help from the concept of allostatic load? Annals of Behavioral Medicine, 21, 330338.CrossRefGoogle ScholarPubMed
Kulhmann, S., Piel, M., & Wolf, O. T. (2005). Impaired memory retreival after psychosocial stress in healthy young men. Journal of Neuroscience, 25, 29772982.CrossRefGoogle Scholar
Larkina, M., Güler, O. E., Kleinknecht, E., & Bauer, P. (2008). Maternal provision of structure in a deliberate memory task in relation to their preschool children's recall. Journal of Experimental Child Psychology, 100, 235251.CrossRefGoogle Scholar
Laucht, M., Esser, G., & Schmidt, M. H. (2001). Differential development of infants at risk for psychopathology: The moderating role of early maternal responsivity. Developmental Medicine and Child Neurology, 43, 292300.CrossRefGoogle ScholarPubMed
Liu, D., Diorio, J., Day, J., Francis, D., & Meaney, M. (2000). Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nature Neuroscience, 3, 799805.CrossRefGoogle ScholarPubMed
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., et al. (1997). Maternal care, hippocampal glucorticoid receptors, and hypothalamic–pituitary–adrenal responses to stress. Science, 277, 1659.CrossRefGoogle Scholar
Lupien, S. J., & Lepage, M. (2001). Stress, memory, and the hippocampus: Can't live with it, can't live without it. Behavioral Brain Research, 127, 137158.CrossRefGoogle Scholar
Lupien, S. J., Maheu, F., Tu, M., Fiocco, A., & Schramek, T. E. (2007). The effects of stress and stress hormones on human cognition: Implications for the field of brain and cognition. Brain and Cognition, 65, 209237.CrossRefGoogle ScholarPubMed
Luthar, S. S. (2006). Resilience in development: A synthesis of research across five decades. In Cicchetti, D. & Cohen, D. J. (Eds.), Developmental Psychopathology: Risk, disorder, and adaptation (pp. 740795). New York: Wiley.Google Scholar
Luthar, S. S., Cicchetti, D., & Becker, B. (2000). The construct of resilience: A critical evaluation and guidelines for future work. Child Development, 71, 543562.CrossRefGoogle ScholarPubMed
Masten, A. (2001). Ordinary magic: Resilience processes in development. American Psychologist, 56, 227238.CrossRefGoogle ScholarPubMed
McEwen, B. S. (1998). Stress, adaptation and disease. Allostasis and allostatic load. Annals of the New York Academy of Sciences, 840, 3344.CrossRefGoogle ScholarPubMed
McEwen, B. S. (1999). Stress and hippocampal plasticity. Annual Review of Neuroscience, 22, 105122.CrossRefGoogle ScholarPubMed
McEwen, B. S. (2000). Allostasis and allostatic load: Implications for neuropsychopharmacology. Neuropsychopharmacology, 22, 108124.CrossRefGoogle ScholarPubMed
McEwen, B. S., Conrad, C. D., Kuroda, Y., Frankfurt, M., Margarinos, A. M., & McKittrick, C. (1997). Prevention of stress-indeced morphological and cognitive consequences. European Neuropsychopharmacology, 7(Suppl. 3), S323S328.CrossRefGoogle ScholarPubMed
McEwen, B. S., & Gianaros, P. J. (2010). Central role of the brain in stress and adaptation, links to socioeconomic status, health and disease. Annual of the New York Academy of Sciences, 1186, 190222.CrossRefGoogle ScholarPubMed
McEwen, B. S., Weiss, J. M., & Schwarz, L. S. (1968). Selective retention of corticosterone by limbic structures in rat brain. Nature, 220, 911912.CrossRefGoogle ScholarPubMed
Meaney, M. J., & Szyf, M. (2005). Maternal care as a model for experience-dependent chromatin plasticity? Trends in Neurosciences, 28, 456463.CrossRefGoogle Scholar
Mizoguchi, K., Yuzurihara, M., Ishige, A., Sasaki, H., Chui, D., & Tabira, T. (1992). Chronic stress induces impairment of spatial working memory because of prefrontal dopaminergic dysfunction. Journal of Neuroscience, 20, 15681574.CrossRefGoogle Scholar
Muller, N. G., & Knight, R. T. (2006). The functional neuroanatomy of working memory: Contributions of human brain lesion studies. Neuroscience, 139, 5158.CrossRefGoogle ScholarPubMed
Oei, N. Y., Everaerd, W. T., Elzinga, B. M., van Well, S., & Bermond, B. (2006). Psychosocial stress impairs working memory at high loads: An association with cortisol levels and memory retrieval. Stress, 9, 133141.CrossRefGoogle ScholarPubMed
Petrides, M. (2000). The role of the mid-dorsolateral prefrontal cortex in working memory. Experimental Brain Research, 133, 4454.CrossRefGoogle ScholarPubMed
Riggin, R., & Kissinger, P. (1977). Determination of catecholamines in urine by reverse phase liquid chromatography with electrochemical detection. Analytic Chemistry, 49, 21092111.CrossRefGoogle ScholarPubMed
Sandi, C., Loscertales, M., & Guaza, C. (1998). Experience-dependent faciliatating effect of corticosterone on spatial memory formation in the water maze. European Journal of Neuroscience, 9, 637642.CrossRefGoogle Scholar
Sandi, C., & Pinelo-Nava, M. T. (2007). Stress and memory: Behavioral effects and neurobiological mechanisms. Neural Plasticity, 2007, 78970.CrossRefGoogle ScholarPubMed
Sapolsky, R. (1996). Why stress is bad for your brain. Science, 273, 749750.CrossRefGoogle ScholarPubMed
Schoofs, D., Preuss, D., & Wolf, O. T. (2008). Psychosocial stress induces working memory impairments in an n-back paradigm. Psychoneuroendocrinology, 33, 643653.CrossRefGoogle Scholar
Selden, N. R., Cole, B. J., Everitt, B. J., & Robbins, T. W. (1990). Damage to ceruleo-cortical noradrenergic projections impairs locally cued but enhances spatially cued water maze acquisition. Behavioral Brain Research, 39, 2951.CrossRefGoogle ScholarPubMed
Smeets, T., Jelicic, M., & Merckelbach, H. (2006). The effect of acute stress on memory depends on word valence. International Journal of Psychophysiology, 62, 3037.CrossRefGoogle ScholarPubMed
Tamis-LeMonda, C. S., Bornstein, M. H., & Baumwell, L. (2001). Maternal responsiveness and children's achievement of language milestones. Child Development, 72, 748767.CrossRefGoogle ScholarPubMed
Tops, M., van der Pompe, G., Wijers, A. A., Den Boer, J. A., Meijman, T. F., & Korf, J. (2004). Free recall of pleasant words from recency positions is especially sensitive to acute administration of cortisol. Psychoneuroendocrinology, 29, 327338.CrossRefGoogle ScholarPubMed
Wang, Q., & Ross, M. (2007). Culture and memory. In Kitayama, H. & Cohen, D. (Eds.), Handbook of cultural psychology (pp. 645667). New York: Guilford Press.Google Scholar
Werner, E. E., Bierman, J. M., & French, F. E. (1971). Children of Kauai. Honolulu: University of Hawaii Press.Google Scholar
Werner, E. E., & Smith, R. S. (1977). Kauai's children come of age. Honolulu: University of Hawaii Press.Google Scholar
Werner, E. E., & Smith, R. S. (1982). Vulnerable but invincible: A study of resilient children. New York: McGraw–Hill.Google Scholar
Williams, B. M., Luo, Y., Ward, C., Redd, K., Gibson, R., Kuczaj, S. A., et al. (2001). Environmental enrichment: Effects on spatial memory and hippocampal CREB immunoreactivity. Physiology & Behavior, 73, 649658.CrossRefGoogle ScholarPubMed
Wolkowitz, O. M., Reus, V. I., Weingartner, H., Thompson, K., Breier, A., Doran, A., et al. (1990). Cognitive effects of corticosteroids. American Journal of Psychiatry, 137, 12971303.Google Scholar
Yang, J., Hou, C., Ma, N., Liu, J., Zhang, Y., Zhou, J., et al. (2007). Enriched environmental treatment restores impaired hippocampal synaptic plasticity and cognitive deficits induced by prenatal chronic stress. Neurobiology of Learning and Memory, 87, 257263.CrossRefGoogle ScholarPubMed
Young, A. H., Sahakain, B. J., Robbins, T. W., & Cowen, P. J. (1999). The effects of chronic administation of hydrocortisone on cognitive function in normal male volunteers. Psychopharmacology (Berlin), 145, 260266.CrossRefGoogle Scholar