Skip to main content

Maternal responsiveness moderates the relationship between allostatic load and working memory

  • Stacey N. Doan (a1) and Gary W. Evans (a2)

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.

Corresponding author
Address correspondence and reprint requests to: Stacey N. Doan, Department of Psychology, Boston University, 64 Cummington Street, Boston, MA 02215; E-mail:
Hide All
Aiken, L., & West, S. (1991). Multiple regression: Testing and interpreting interactions. Los Angeles: Sage.
Baddeley, A. D. (2003). Working memory: Looking back and looking forward. Nature Reviews Neuroscience, 4, 829839.
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.
Bornstein, M. H. (1989). Maternal responsiveness characteristics and consequences. San Francisco, CA: Jossey–Bass.
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.
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.
Buss, C., Wolf, O. T., Witt, J., & Hellhammer, D. H. (2004). Autobiographic memory impairment following acute cortisol administration. Psychoneuroendocrinology, 29, 10931096.
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.
Cicchetti, D., & Curtis, W. J. (2007). A multilevel approach to resilience. Development and Psychopathology, 19, 627955.
Cicchetti, D., & Tucker, D. (1994). Development and self-regulatory structures of the mind. Development and Psychopathology, 6, 533549.
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.
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.
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.
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.
Elzinga, B. M., & Roelofs, K. (2005). Cortisol-induced impairments of working memory require acute sympathetic activation. Behavioral Neuroscience, 119, 98103.
Evans, G. W. (2003). A multimethodological analysis of cumulative risk and allostatic load among rural children. Developmental Psychology, 39, 924933.
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.
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.
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.
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.
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.
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.
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.
Francis, D., & Meaney, M. (1999). Maternal care and the development of stress responses. Current Opinion in Neurobiology, 9, 128134.
Fuster, J. M. (1980). The prefrontal cortex. New York: Raven.
Fuster, J. M. (2000). The prefrontal cortex of the primate: A synopsis. Psychobiology, 28, 125131.
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.
Kagan, J. (2001). Biological constraint, cultural variety, and psychological structures. Annals of the New York Academy of Sciences, 935, 177190.
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.
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.
Kulhmann, S., Piel, M., & Wolf, O. T. (2005). Impaired memory retreival after psychosocial stress in healthy young men. Journal of Neuroscience, 25, 29772982.
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.
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.
Liu, D., Diorio, J., Day, J., Francis, D., & Meaney, M. (2000). Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nature Neuroscience, 3, 799805.
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.
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.
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.
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.
Luthar, S. S., Cicchetti, D., & Becker, B. (2000). The construct of resilience: A critical evaluation and guidelines for future work. Child Development, 71, 543562.
Masten, A. (2001). Ordinary magic: Resilience processes in development. American Psychologist, 56, 227238.
McEwen, B. S. (1998). Stress, adaptation and disease. Allostasis and allostatic load. Annals of the New York Academy of Sciences, 840, 3344.
McEwen, B. S. (1999). Stress and hippocampal plasticity. Annual Review of Neuroscience, 22, 105122.
McEwen, B. S. (2000). Allostasis and allostatic load: Implications for neuropsychopharmacology. Neuropsychopharmacology, 22, 108124.
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.
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.
McEwen, B. S., Weiss, J. M., & Schwarz, L. S. (1968). Selective retention of corticosterone by limbic structures in rat brain. Nature, 220, 911912.
Meaney, M. J., & Szyf, M. (2005). Maternal care as a model for experience-dependent chromatin plasticity? Trends in Neurosciences, 28, 456463.
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.
Muller, N. G., & Knight, R. T. (2006). The functional neuroanatomy of working memory: Contributions of human brain lesion studies. Neuroscience, 139, 5158.
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.
Petrides, M. (2000). The role of the mid-dorsolateral prefrontal cortex in working memory. Experimental Brain Research, 133, 4454.
Riggin, R., & Kissinger, P. (1977). Determination of catecholamines in urine by reverse phase liquid chromatography with electrochemical detection. Analytic Chemistry, 49, 21092111.
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.
Sandi, C., & Pinelo-Nava, M. T. (2007). Stress and memory: Behavioral effects and neurobiological mechanisms. Neural Plasticity, 2007, 78970.
Sapolsky, R. (1996). Why stress is bad for your brain. Science, 273, 749750.
Schoofs, D., Preuss, D., & Wolf, O. T. (2008). Psychosocial stress induces working memory impairments in an n-back paradigm. Psychoneuroendocrinology, 33, 643653.
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.
Smeets, T., Jelicic, M., & Merckelbach, H. (2006). The effect of acute stress on memory depends on word valence. International Journal of Psychophysiology, 62, 3037.
Tamis-LeMonda, C. S., Bornstein, M. H., & Baumwell, L. (2001). Maternal responsiveness and children's achievement of language milestones. Child Development, 72, 748767.
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.
Wang, Q., & Ross, M. (2007). Culture and memory. In Kitayama, H. & Cohen, D. (Eds.), Handbook of cultural psychology (pp. 645667). New York: Guilford Press.
Werner, E. E., Bierman, J. M., & French, F. E. (1971). Children of Kauai. Honolulu: University of Hawaii Press.
Werner, E. E., & Smith, R. S. (1977). Kauai's children come of age. Honolulu: University of Hawaii Press.
Werner, E. E., & Smith, R. S. (1982). Vulnerable but invincible: A study of resilient children. New York: McGraw–Hill.
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.
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.
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.
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.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Development and Psychopathology
  • ISSN: 0954-5794
  • EISSN: 1469-2198
  • URL: /core/journals/development-and-psychopathology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Full text views

Total number of HTML views: 17
Total number of PDF views: 124 *
Loading metrics...

Abstract views

Total abstract views: 488 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 18th June 2018. This data will be updated every 24 hours.