Deprivation of maternal care has long-lasting consequences for the hypothalamic-pituitary-adrenal axis of zebra finches

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1729, 2012, Pages 759-766

  Banerjee, Sunayana B ^a   Arterbery, Adam S ^a   Fergus, Daniel J ^a   Adkins Regan, Elizabeth ^a  

^a Cornell University ^*  (United States)

Author keywords

Corticosterone; Glucocorticoid receptor; Maternal deprivation; Mineralocorticoid receptor; Stress; Zebra finch

Indexed keywords

LIFE HISTORY TRAIT; MATERNAL CARE; MITOCHONDRIAL DNA; PASSERINE; PATERNAL CARE;

AVES; MAMMALIA; TAENIOPYGIA GUTTATA;

EID: 84855673930     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.1265     Document Type: Article

References (45)

1. Lightman, S. L. 2008 The neuroendocrinology of stress: a never ending story. J. Neuroendocrinol. 20, 880-884. (doi:10.1111/j.1365-2826.2008.01711.x)
2. McEwen, B. S. et al. 1995 Stress and the brain: a paradoxical role for adrenal steroids. Vitam. Horm. 51, 371-402. (doi:10.1016/S0083-6729(08)61045-6)
3. McEwen, B. S. 2008 Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators. Eur. J. Pharmacol. 583, 174-185. (doi:10.1016/j.ejphar.2007.11.071)
4. Plotsky, P. M., Owens, M. J. & Nemeroff, C. B. 1998 Psychoneuroendocrinology of depression-hypothalamicpituitary- adrenal axis. Psychiatr. Clin. North Am. 21, 293-307. (doi:10.1016/S0193-953X(05)70006-X)
5. Sapolsky, R. M., Romero, L. M. & Munck, A. U. 2000 How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21, 55-89. (doi:10.1210/er.21.1.55)
6. De Kloet, E. R. 1991 Brain corticosteroid receptor balance and homeostatic control. Front. Neuroendocrinol. 12, 95-164. (doi:10.1016/S0079-6123(08)62132-9)
7. De Kloet, E. R., Karst, H. & Joels, M. 2008 Corticosteroid hormones in the central stress response: quick-and-slow. Front. Neuroendocrinol. 29, 268-272. (doi:10.1016/j.yfrne.2007.10.002)
8. De Kloet, E. R., Joels, M. & Holsboer, F. 2005 Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 6, 463-475. (doi:10.1038/nrn1683)
9. De Kloet, E. R. 2000 Stress in the brain. Eur. J. Pharmacol. 405, 187-198. (doi:10.1016/S0014-2999(00)00552-5)
10. Veenema, A. H. 2009 Early life stress, the development of aggression and neuroendocrine and neurobiological correlates: what can we learn from animal models? Front. Neuroendocrinol. 30, 497-518. (doi:10.1016/j.yfrne.2009.03.003)
11. Levine, S. 2000 Influence of psychological variables on the activity of the hypothalamic-pituitary-adrenal axis. Eur. J. Pharmacol. 405, 149-160. (doi:10.1016/S0014-2999(00)00548-3)
12. Lippmann, M., Bress, A., Nemeroff, C. B., Plotsky, P. M. & Monteggia, L. M. 2007 Long-term behavioural and molecular alterations associated with maternal separation in rats. Eur. J. Neurosci. 25, 3091-3098. (doi:10.1111/j.1460-9568.2007.05522.x)
13. Daniels, W. M. U., Pietersen, C. Y., Carstens, M. E. & Stein, D. J. 2004 Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metab. Brain Dis. 19, 3-14. (doi:10.1023/B:MEBR.0000027412.19664.b3)
14. Meaney, M. J., Diorio, J., Francis, D., Widdowson, J., LaPlante, P., Caldji, C., Sharma, S., Seckl, J. R. & Plotsky, P. M. 1996 Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev. Neurosci. 18, 49-72. (doi:10.1159/000111395)
15. 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. Mol. Brain Res. 18, 195-200. (doi:10.1016/0169-328X(93)90189-V)
16. Meaney, M. J. 2001 Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 24, 1161-1192. (doi:10.1146/annurev.neuro.24.1.1161)
17. Francis, D. D. & Meaney, M. J. 1999 Maternal care and the development of stress responses. Curr. Opin. Neurobiol. 9, 128-134. (doi:10.1016/S0959-4388(99)80016-6)
18. Anisman, H., Zaharia, M. D., Meaney, M. J. & Merali, Z. 1998 Doearly-life events permanently alter behavioral and hormonal responses to stressors? Int. J. Dev. Neurosci. 16, 149-164. (doi:10.1016/S0736-5748(98)00025-2)
19. Zann, R. A. 1996 The zebra finch: a synthesis of field and laboratory studies. Oxford, UK: Oxford University Press.
20. Rensel, M. A., Wilcoxen, T. E. & Schoech, S. J. 2010 The influence of nest attendance and provisioning on nestling stress physiology in the Florida scrub-jay. Horm. Behav. 57, 162-168. (doi:10.1016/j.yhbeh.2009.10.009)
21. Sapolsky, R. M. & Meaney, M. J. 1986 Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res. 396, 64-76. (doi:10.1016/0165-0173(86)90010-X)
22. Rensel, M. A., Boughton, R. K. & Schoech, S. J. 2010 Development of the adrenal stress response in the Florida scrub-jay (Aphelocoma coerulescens). Gen. Comp. Endocrinol. 165, 255-261. (doi:10.1016/j.ygcen.2009.07.002)
23. S Sims, C. G. & Holberton, R. L. 2000 Development of the corticosterone stress response in young Northern Mockingbirds (Mimus polyglottos). Gen. Comp. Endocrinol. 119, 193-201. (doi:10.1006/gcen.2000.7506)
24. Wada, H., Hahn, T. P. & Breuner, C. W. 2007 Development of stress reactivity in white-crowned sparrow nestlings: total corticosterone response increases with age, while free corticosterone response remains low. Gen. Comp. Endocrinol. 150, 405-413. (doi:10.1016/j.ygcen.2006.10.002)
25. Wada, H., Salvante, K. G., Wagner, E., Williams, T. D. & Breuner, C. W. 2009 Ontogeny and individual variation in the adrenocortical response of zebra finch (Taeniopygia guttata) nestlings. Physiol. Biochem. Zool. 82, 325-331. (doi:10.1086/599320)
26. Dickens, M., Romero, L. M., Cyr, N. E., Dunn, I. C. & Meddle, S. L. 2009 Chronic stress alters glucocorticoid receptor and mineralocorticoid receptor mRNA expression in the European starling (Sturnus vulgaris) brain. J. Neuroendocrinol. 21, 832-840. (doi:10.1111/j.1365-2826.2009.01908.x)
27. Hodgson, Z. G., Meddle, S. L., Roberts, M. L., Buchanan, K. L., Evans, M. R., Metzdorf, R., Gahr, M. & Healy, S. D. 2007 Spatial ability is impaired and hippocampal mineralocorticoid receptor mRNA expression reduced in zebra finches (Taeniopygia guttata) selected for acute high corticosterone response to stress. Proc. R. Soc. B 274, 239-245. (doi:10.1098/rspb.2006.3704)
28. Makino, S., Hashimoto, K. & Gold, P. W. 2002 Multiple feedback mechanisms activating corticotropin-releasing hormone system in the brain during stress. Pharmacol. Biochem. Behav. 73, 147-158. (doi:10.1016/S0091-3057(02)00791-8)
29. Sapolsky, R. M., Zolamorgan, S. & Squire, L. R. 1991 Inhibition of glucocorticoid secretion by the hippocampal formation in the primate. J. Neurosci. 11, 3695-3704.
30. Jacobson, L. & Sapolsky, R. 1991 The role of the hippocampus in feedback-regulation of the hypothalamicpituitary- adrenocortical axis. Endocr. Rev. 12, 118-134. (doi:10.1210/edrv-12-2-118)
31. Kitraki, E., Karandrea, D. & Kittas, C. 1999 Long-lasting effects of stress on glucocorticoid receptor gene expression in the rat brain. Neuroendocrinology 69, 331-338. (doi:10.1159/000054435)
32. Herman, J. P., Ostrander, M. M., Mueller, N. K. & Figueiredo, H. 2005 Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog. Neuropsychopharmacol. Biol. Psychol. 29, 1201-1213. (doi:10.1016/j.pnpbp.2005.08.006)
33. Wada, H. & Breuner, C.W. 2010 Developmental changes in neural corticosteroid receptor binding capacity in altricial nestlings. Dev. Neurobiol. 70, 853-861. (doi:10.1002/ dneu.20819)
34. Oitzl, M. S., Champagne, D. L., van der Veen, R. & De Kloet, E. R. 2010 Brain development under stress: hypotheses of glucocorticoid actions revisited. Neurosci. Biobehav. Rev. 34, 853-866. (doi:10.1016/j.neubiorev.2009.07.006)
35. De Kloet, E. R., Vreugdenhil, E., Oitzl, M. S. & Joels, M. 1998 Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 19, 269-301. (doi:10.1210/er.19.3.269)
36. Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M. & Meaney, M. J. 2004 Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847-854. (doi:10.1038/nn1276)
37. Champagne, F. A., Francis, D. D., Mar, A. & Meaney, M. J. 2003 Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol. Behav. 79, 359-371. (doi:10.1016/S0031-9384(03)00149-5)
38. Champagne, F. A. & Curley, J. P. 2009 Epigenetic mechanisms mediating the long-term effects of maternal care on development. Neurosci. Biobehav. Rev. 33, 593-600. (doi:10.1016/j.neubiorev.2007.10.009)
39. Szyf, M., Weaver, I. C. G., Champagne, F. A., Diorio, J. & Meaney, M. J. 2005 Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat. Front. Neuroendocrinol. 26, 139-162. (doi:10.1016/j.yfrne.2005.10.002)
40. Romero, L.M. & Wikelski, M. 2010 Stress physiology as a predictor of survival in Galapagos marine iguanas. Proc. R. Soc. B 277, 3157-3162. (doi:10.1098/rspb.2010.0678)
41. Champagne, D. L., Bagot, R. C., van Hasselt, F., Ramakers, G., Meaney, M. J., De Kloet, E. R., Joëls, M. & Krugers, H. 2008 Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J. Neurosci. 28, 6037-6045. (doi:10.1523/JNEUROSCI.0526-08.2008)
42. Zhang, T. Y. et al. 2006 Maternal programming of defensive responses through sustained effects on gene expression. Biol. Psychol. 73, 72-89. (doi:10.1016/j.biopsycho.2006.01.009)
43. Zhang, T. Y. & Meaney, M. J. 2010 Epigenetics and the environmental regulation of the genome and its function. Annu. Rev. Psychol. 61, 439-466. (doi:10.1146/annurev.psych.60.110707.163625)
44. Meaney, M. J., Szyf, M. & Seckl, J. R. 2007 Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends Mol. Med. 13, 269-277. (doi:10.1016/j.molmed.2007.05.003)
45. Cameron, N. M., Champagne, F. A., Fish, C., Ozaki-Kuroda, K. & Meaney, M. J. 2005 The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care. Neurosci. Biobehav. Rev. 29, 843-865. (doi:10.1016/j.neubiorev.2005.03.022)