Abstract
Evidence from animal research has demonstrated the effect of early maternal care on the offspring’s endocrine and behavioral stress response in adulthood. The present prospective study investigates, in humans, the long-term impact of maternal responsiveness and stimulation during early mother–child interaction on adrenocorticotropic hormone (ACTH) and cortisol response to a psychosocial laboratory stressor in adulthood. The data are from an epidemiological cohort study of the long-term outcome of early risk factors assessed at birth. At age 3 months, mothers and infants were videotaped during a 10-min standardized nursing and playing situation and evaluated by trained raters for maternal stimulation and infant and maternal responsiveness. At age 19 years, 270 participants (146 females, 124 males) completed the Trier Social Stress Test. The results indicated that less maternal stimulation during early interaction at age 3 months predicted diminished plasma ACTH and cortisol increase in response to acute psychosocial stress in male, but not female offspring. In contrast, maternal responsiveness was found to be unrelated to hypothalamic–pituitary–adrenal (HPA) reactivity. In accordance with the findings from animal research, the present study provides prospective evidence in humans of a long-term association between early maternal interaction behavior and the offspring’s hormonal stress response in young adulthood, suggesting that poor maternal stimulation in early infancy may result in reduced HPA axis reactivity to an acute psychosocial stressor in males.
Similar content being viewed by others
References
Ainsworth MD, Blehar M, Waters E, Wall S (1978) Patterns of attachment. Erlbaum, Hillsdale
Albers EM, Riksen-Walraven JM, Sweep FC et al (2008) Maternal behavior predicts infant cortisol recovery from a mild everyday stressor. J Child Psychol Psychiatry 49:97–103
Bardi M, Bode AE, Ramirez SM et al (2005) Maternal care and development of stress responses in baboons. Am J Primatol 66:263–278
Beck AT, Steer RA (1987) Beck Depression Inventory (BDI). The Psychological Corporation Inc., San Antonio
Bowlby J (1982) Attachment and loss: attachment. Hogarth Press, London
Boyce WT, Chesterman E (1990) Life events, social support, and cardiovascular reactivity in adolescence. J Dev Behav Pediatr 11:105–111
Boyce WT, Ellis BJ (2005) Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Dev Psychopathol 17:271–301
Brazelton TB, Kosolowski B, Main M (1974) The origins of reciprocity: the early mother–infant interaction. In: Lewis M, Rosenblum L (eds) The effect of the infant on its caretaker. Raven, New York, pp 49–76
Buchmann AF, Kopf D, Westphal S et al (2010) The impact of early parental child-rearing behavior on young adults’ cardiometabolic risk profile: a prospective study. Psychosom Med 72:156–162
Burke HM, Davis MC, Otte C et al (2005) Depression and cortisol responses to psychological stress: a meta-analysis. Psychoneuroendocrinology 30:846–856
Caldji C, Tannenbaum B, Sharma S et al (1998) Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci USA 95:5335–5340
Campbell SB, Matestic P, von Stauffenberg C, Mohan R, Kirchner T (2007) Trajectories of maternal depressive symptoms, maternal sensitivity, and children’s functioning at school entry. Dev Psychol 43:1202–1215
Carpenter LL, Carvalho JP, Tyrka AR et al (2007) Decreased adrenocorticotropic hormone and cortisol responses to stress in healthy adults reporting significant childhood maltreatment. Biol Psychiatry 62:1080–1087
Cerezo MA, Pons-Salvador G, Trenado RM (2008) Mother–infant interaction and children’s socio-emotional development with high- and low-risk mothers. Infant Behav Dev 31:578–589
Coe CL, Glass JC, Wiener SG et al (1983) Behavioral, but not physiological, adaptation to repeated separation in mother and infant primates. Psychoneuroendocrinology 8:401–409
Cohn JF, Campbell SB, Matias R (1990) Face-to-face interactions of postpartum depressed and nondepressed mother–infant pairs at 2 months. Dev Psychol 26:15–23
Elzinga BM, Roelofs K, Tollenaar MS et al (2008) Diminished cortisol responses to psychosocial stress associated with lifetime adverse events a study among healthy young subjects. Psychoneuroendocrinology 33:227–237
Essex MJ, Klein MH, Cho E et al (2002) Maternal stress beginning in infancy may sensitize children to later stress exposure: effects on cortisol and behavior. Biol Psychiatry 52:776–784
Fairchild G, van Goozen SH, Stollery SJ et al (2008) Cortisol diurnal rhythm and stress reactivity in male adolescents with early-onset or adolescence-onset conduct disorder. Biol Psychiatry 64:599–606
Field T (1990) Infancy. Harvard University Press, Cambridge
Field T, Healy B, Goldstein S et al (1988) Infants of depressed mothers show “depressed” behavior even with nondepressed adults. Child Dev 59:1569–1579
Francis DD, Champagne FA, Liu D et al (1999) Maternal care, gene expression, and the development of individual differences in stress reactivity. Ann N Y Acad Sci 896:66–84
Fries E, Hesse J, Hellhammer J et al (2005) A new view on hypocortisolism. Psychoneuroendocrinology 30:1010–1016
Garmezy N (1991) Resilience in children’s adaptation to negative life events and stressed environments. Pediatr Ann 20(459–460):463–466
Gunnar MR, Donzella B (2002) Social regulation of the cortisol levels in early human development. Psychoneuroendocrinology 27:199–220
Gunnar MR, Fisher PA (2006) Bringing basic research on early experience and stress neurobiology to bear on preventive interventions for neglected and maltreated children. Dev Psychopathol 18:651–677
Gunnar MR, Frenn K, Wewerka SS et al (2009) Moderate versus severe early life stress: associations with stress reactivity and regulation in 10-12-year-old children. Psychoneuroendocrinology 34:62–75
Haley DW, Stansbury K (2003) Infant stress and parent responsiveness: regulation of physiology and behavior during still-face and reunion. Child Dev 74:1534–1546
Halligan SL, Herbert J, Goodyer IM et al (2004) Exposure to postnatal depression predicts elevated cortisol in adolescent offspring. Biol Psychiatry 55:376–381
Handa RJ, Burgess LH, Kerr JE et al (1994) Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Horm Behav 28:464–476
Hautzinger M, Bailer M, Worall H et al (1994) Beck-Depressions-Inventar (BDI) [in German]. Hans Huber, Bern
Heim C, Ehlert U, Hellhammer DH (2000) The potential role of hypocortisolism in the pathophysiology of stress-related bodily disorders. Psychoneuroendocrinology 25:1–35
Heim C, Plotsky PM, Nemeroff CB (2004) Importance of studying the contributions of early adverse experience to neurobiological findings in depression. Neuropsychopharmacology 29:641–648
Heim C, Newport DJ, Mletzko T et al (2008) The link between childhood trauma and depression: insights from HPA axis studies in humans. Psychoneuroendocrinology 33:693–710
Houshyar H, Galigniana MD, Pratt WB et al (2001) Differential responsivity of the hypothalamic-pituitary-adrenal axis to glucocorticoid negative-feedback and corticotropin releasing hormone in rats undergoing morphine withdrawal: possible mechanisms involved in facilitated and attenuated stress responses. J Neuroendocrinol 13:875–886
Jörg M, Dinter R, Rose F et al (1994) Kategoriensystem zur Mikroanalyse der frühen Mutter-Kind-Interaktion. Z Kinder- Jugendpsychiat 22:97–106
Kajantie E, Phillips DI (2006) The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology 31:151–178
Kaufman J, Yang BZ, Douglas-Palumberi H et al (2004) Social supports and serotonin transporter gene moderate depression in maltreated children. Proc Natl Acad Sci USA 101:17316–17321
Kirschbaum C, Pirke KM, Hellhammer DH (1993a) The ‘Trier Social Stress Test’—a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 28:76–81
Kirschbaum C, Strasburger CJ, Langkrar J (1993b) Attenuated cortisol response to psychological stress but not to CRH or ergometry in young habitual smokers. Pharmacol Biochem Behav 44:527–531
Kochanska G, Murray KT, Harlan ET (2000) Effortful control in early childhood: continuity and change, antecedents, and implications for social development. Dev Psychol 36:220–232
Kudielka BM, Kirschbaum C (2005) Sex differences in HPA axis responses to stress: a review. Biol Psychiatry 69:113–132
Ladd CO, Thrivikraman KV, Huot RL et al (2005) Differential neuroendocrine responses to chronic variable stress in adult Long Evans rats exposed to handling-maternal separation as neonates. Psychoneuroendocrinology 30:520–533
Laucht M, Esser G, Schmidt MH (1997) Developmental outcome of infants born with biological and psychosocial risks. J Child Psychol Psychiatry 38:843–853
Laucht M, Esser G, Baving L et al (2000) Behavioral sequelae of perinatal insults and early family adversity at 8 years of age. J Am Acad Child Adolesc Psychiatry 39:1229–1237
Laucht M, Esser G, Schmidt MH (2001) Differential development of infants at risk for psychopathology: the moderating role of early maternal responsivity. Dev Med Child Neurol 43:292–300
Levine S, Mody T (2003) The long-term psychobiological consequences of intermittent postnatal separation in the squirrel monkey. Neurosci Biobehav Rev 27:83–89
Liu D, Diorio J, Tannenbaum B et al (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277:1659–1662
Lyons DM, Parker KJ (2007) Stress inoculation-induced indications of resilience in monkeys. J Trauma Stress 20:423–433
Matthews SG (2002) Early programming of the hypothalamo-pituitary-adrenal axis. Trends Endocrinol Metab 13:373–380
McGowan PO, Sasaki A, D’Alessio AC et al (2009) Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 12:342–348
Meaney MJ, Szyf M (2005) Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome. Dialogues Clin Neurosci 7:103–123
Menard JL, Hakvoort RM (2007) Variations of maternal care alter offspring levels of behavioral defensiveness in adulthood: evidence for a threshold model. Behav Brain Res 176:302–313
Müller R, Abbet JP (1991) Changing trends in the consumption of legal and illegal drugs by 11-16-year-old adolescent pupils. Findings from a study conducted under the auspices of the WHO Europe. Swiss Professional Service for Alcohol Problems, Lausanne
Murray L, Halligan SL, Goodyer I et al (2010) Disturbances in early parenting of depressed mothers and cortisol secretion in offspring: a preliminary study. J Affect Disord 122:218–223
Nachmias M, Gunnar M, Mangelsdorf S et al (1996) Behavioral inhibition and stress reactivity: the moderating role of attachment security. Child Dev 67:508–522
Ostrander MM, Ulrich-Lai YM, Choi DC et al (2006) Hypoactivity of the hypothalamo-pituitary-adrenocortical axis during recovery from chronic variable stress. Endocrinology 147:2008–2017
Pajer K, Gardner W, Rubin RT et al (2001) Decreased cortisol levels in adolescent girls with conduct disorder. Arch Gen Psychiatry 58:297–302
Parker KJ, Buckmaster CL, Schatzberg AF et al (2004) Prospective investigation of stress inoculation in young monkeys. Arch Gen Psychiatry 61:933–941
Parker KJ, Buckmaster CL, Sundlass K et al (2006) Maternal mediation, stress inoculation, and the development of neuroendocrine stress resistance in primates. Proc Natl Acad Sci USA 103:3000–3005
Popma A, Jansen LM, Vermeiren R et al (2006) Hypothalamus pituitary adrenal axis and autonomic activity during stress in delinquent male adolescents and controls. Psychoneuroendocrinology 31:948–957
Priebe K, Romeo RD, Francis DD et al (2005) Maternal influences on adult stress and anxiety-like behavior in C57BL/6J and BALB/cJ mice: a cross-fostering study. Dev Psychobiol 47:398–407
Pruessner JC, Kirschbaum C, Meinlschmid G et al (2003) Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology 28:916–931
Pruessner JC, Champagne F, Meaney MJ et al (2004) Dopamine release in response to a psychological stress in humans and its relationship to early life maternal care: a positron emission tomography study using [11C]raclopride. J Neurosci 24:2825–2831
Pryce CR, Ruedi-Bettschen D, Dettling AC et al (2005) Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research. Neurosci Biobehav Rev 29:649–674
Rhodes ME, Rubin RT (1999) Functional sex differences (‘sexual diergism’) of central nervous system cholinergic systems, vasopressin, and hypothalamic-pituitary-adrenal axis activity in mammals: a selective review. Brain Res Brain Res Rev 30:135–152
Roelofs K, Elzinga BM, Rotteveel M (2005) The effects of stress-induced cortisol responses on approach-avoidance behavior. Psychoneuroendocrinology 30:665–677
Roelofs K, Bakvis P, Hermans EJ et al (2007) The effects of social stress and cortisol responses on the preconscious selective attention to social threat. Biol Psychol 75:1–7
Rutter M (1993) Resilience: some conceptual considerations. J Adolesc Health 14:626–631
Rutter M, Quinton D (1977) Psychiatric disorder—ecological factors and concepts of causation. In: McGurk M (ed) Ecological factors in human development. North Holland, Amsterdam, pp 173–187
Saltzman W, Hogan BK, Abbott DH (2006) Diminished cortisol levels in subordinate female marmosets are associated with altered central drive to the hypothalamic-pituitary-adrenal axis. Biol Psychiatry 60:843–849
Sanchez MM, Noble PM, Lyon CK et al (2005) Alterations in diurnal cortisol rhythm and acoustic startle response in nonhuman primates with adverse rearing. Biol Psychiatry 57:373–381
Schmid B (2009) Einfluss der frühen Mutter-Kind-Interaktion auf die Depressivität und Stressreaktivität im jungen Erwachsenenalter unter Berücksichtigung moderierender genetischer Faktoren. Unpublished doctoral thesis, University of Heidelberg
Schmid B, Blomeyer D, Buchmann AF et al (2011) Quality of early mother–child interaction associated with depressive psychopathology in the offspring: a prospective study from infancy to adulthood. J Psychiatr Res 45:1387–1394
Smeekens S, Riksen-Walraven JM, van Bakel HJ (2007) Multiple determinants of externalizing behavior in 5-year-olds: a longitudinal model. J Abnorm Child Psychol 35:347–361
Spangler G, Schieche M (1998) Emotional and adrenocortical responses of infants to the strange situation: the differential function of emotional expression. Int J Behav Dev 22:681–706
Spangler G, Schieche M, Ilg U et al (1994) Maternal sensitivity as an external organizer for biobehavioral regulation in infancy. Dev Psychobiol 27:425–437
Stams GJ, Juffer F, van Ijzendoorn MH (2002) Maternal sensitivity, infant attachment, and temperament in early childhood predict adjustment in middle childhood: the case of adopted children and their biologically unrelated parents. Dev Psychol 38:806–821
Swaab DF, Bao AM, Lucassen PJ (2005) The stress system in the human brain in depression and neurodegeneration. Ageing Res Rev 4:141–194
Tronick EZ, Cohn JF (1989) Infant-mother face-to-face interaction: age and gender differences in coordination and the occurrence of miscoordination. Child Dev 60:85–92
Tronick ED, Als H, Brazelton TB (1977) Mutuality in mother–infant interaction. J Commun 27:74–79
van Goozen SH, Matthys W, Cohen-Kettenis PT et al (1998) Salivary cortisol and cardiovascular activity during stress in oppositional-defiant disorder boys and normal controls. Biol Psychiatry 43:531–539
Weaver IC, Meaney MJ, Szyf M (2006) Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc Natl Acad Sci USA 103:3480–3485
Wittchen HU, Zaudig M, Fydrich T (1997) Structured clinical interview for DSM-IV Axis I and II—SCID. Hogrefe, Göttingen
Young EA, Altemus M (2004) Puberty, ovarian steroids, and stress. Ann N Y Acad Sci 1021:124–133
Acknowledgments
This study was supported by multiple grants from the Deutsche Forschungsgemeinschaft (DFG), the Federal Ministry for Education and Research as part of the ‘Baden-Wuerttemberg Consortium for Addiction Research’ and the ‘National Genome Research Network’.
Conflict of interest
Dr. Banaschewski served in an advisory or consultancy role for Bristol Myers-Sqibb, Desitin, Lilly, Medice, Novartis, Pfizer, Shire, UCB and Viforpharma. He received conference attendance support and conference support or received speaker’s fees from Lilly, Janssen McNeil, Medice, Novartis, Shire, UCB. He is/has been involved in clinical trials conducted by Lilly, Shire and Novartis. The present work is unrelated to the above grants and relationships. All other authors declare that they have no conflicts of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Schmid, B., Buchmann, A.F., Trautmann-Villalba, P. et al. Maternal stimulation in infancy predicts hypothalamic–pituitary–adrenal axis reactivity in young men. J Neural Transm 120, 1247–1257 (2013). https://doi.org/10.1007/s00702-013-0970-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00702-013-0970-8