Effects of denial of reward through maternal contact in the neonatal period on adult hypothalamic-pituitary-adrenal axis function in the rat

Psychoneuroendocrinology

Volumn 38, Issue 6, 2013, Pages 830-841

  Diamantopoulou, Anastasia ^a   Raftogianni, Androniki ^a   Stamatakis, Antonios ^a   Oitzl, Melly S ^b   Stylianopoulou, Fotini ^a  

^a UNIVERSITY OF ATHENS   (Greece)

^b LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Coping style; CRH R1; Early life experience; GR; MR; Stress hormones

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; GLUCOCORTICOID RECEPTOR; MESSENGER RNA;

ADULT ANIMAL; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CENTRAL NUCLEUS (AMYGDALA); CONTROLLED STUDY; COPING BEHAVIOR; CORTICOSTERONE BLOOD LEVEL; EXPERIENCE; FEMALE; FORCED SWIMMING TEST; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; HORMONE ACTION; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MALE; MATERNAL DEPRIVATION; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RAT; STRESS;

ADAPTATION, PSYCHOLOGICAL; ADRENOCORTICOTROPIC HORMONE; AMYGDALA; ANIMALS; ANIMALS, NEWBORN; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; FEMALE; HIPPOCAMPUS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MATERNAL DEPRIVATION; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PITUITARY-ADRENAL SYSTEM; RATS; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; RECEPTORS, GLUCOCORTICOID; REWARD; STRESS, PSYCHOLOGICAL;

EID: 84877068432     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2012.09.007     Document Type: Article

References (58)

1. Aisa B., Tordera R., Lasheras B., Del Río J., Ramírez M.J. Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 2007, 32:256-266.
2. Avishai-Eliner, Eghbal-Ahmadi M., Tabachnik E., Brunson K.L., Baram T.Z. Down-regulation of hypothalamic corticotropin-releasing hormone messenger ribonucleic acid (mRNA) precedes early-life experience-induced changes in hippocampal glucocorticoid receptor mRNA. Endocrinology 2001, 142:89-97.
3. Avishai-Eliner S., Gilles E.E., Eghbal-Ahmadi M., Bar-El Y., Baram T.Z. Altered regulation of gene and protein expression of hypothalamic-pituitary-adrenal axis components in an immature rat model of chronic stress. J. Neuroendocrinol. 2001, 13:799-807.
4. Baek S.B., Bahn G., Moon S.J., Lee J., Kim K.H., Ko I.G., Kim S.E., Sung Y.H., Kim B.K., Kim T.S., Kim C.J., Shin M.S. The phosphodiesterase type-5 inhibitor, tadalafil, improves depressive symptoms, ameliorates memory impairment, as well as suppresses apoptosis and enhances cell proliferation in the hippocampus of maternal-separated rat pups. Neurosci. Lett. 2011, 488:26-30.
5. Beaulieu S., Pelletier G., Vaudry H., Barden N. Influence of the central nucleus of the amygdala on the content of corticotropin-releasing factor in the median eminence. Neuroendocrinology 1989, 49:255-261.
6. Bilang-Bleuel A., Ulbricht S., Chandramohan Y., De Carli S., Droste S.K., Reul J.M. Psychological stress increases histone H3 phosphorylation in adult dentate gyrus granule neurons: involvement in a glucocorticoid receptor-dependent behavioural response. Eur. J. Neurosci. 2005, 22:1691-1700.
7. Brunson K.L., Avishai-Eliner S., Hatalski C.G., Baram T.Z. Neurobiology of the stress response early in life: evolution of a concept and the role of corticotropin releasing hormone. Mol. Psychiatry 2001, 6:647-656.
8. Champagne F.A., Francis D.D., Mar A., Meaney M.J. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol. Behav. 2003, 79:359-371.
9. Connor T.J., Kelly J.P., Leonard B.E. Forced swim test-induced neurochemical endocrine, and immune changes in the rat. Pharmacol. Biochem. Behav. 1997, 58:961-967.
10. Daskalakis N.P., Claessens S.E., Laboyrie J.J., Enthoven L., Oitzl M.S., Champagne D.L., de Kloet E.R. The newborn rat's stress system readily habituates to repeated and prolonged maternal separation, while continuing to respond to stressors in context dependent fashion. Horm. Behav. 2011, 60:165-176.
11. Dayas C.V., Buller K.M., Crane J.W., Xu Y., Day T.A. Stressor categorization: acute physical and psychological stressors elicit distinctive recruitment patterns in the amygdala and in medullary noradrenergic cell groups. Eur. J. Neurosci. 2001, 14:1143-1152.
12. de Kloet E.R., Joëls M., Holsboer F. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 2005, 6:463-475.
13. de Quervain D.J., Aerni A., Schelling G., Roozendaal B. Glucocorticoids and the regulation of memory in health and disease. Front. Neuroendocrinol. 2009, 30:358-370.
14. Diamantopoulou A., Stamatakis A., Panagiotaropoulos T., Stylianopoulou F. Reward or its denial during the neonatal period affects adult spatial memory and hippocampal phosphorylated cAMP response element-binding protein levels of both the neonatal and adult rat. Neuroscience 2011, 181:89-99.
15. Diamantopoulou A., Raftogianni A., Stamatakis A., Alikaridis F., Oitzl M.S., Stylianopoulou F. Denial of reward in the neonate shapes sociability and serotonergic activity in the adult rat. PLoS One 2012, 7(3):e33793.
16. Ebner K., Bosch O.J., Krömer S.A., Singewald N., Neumann I.D. Release of oxytocin in the rat central amygdala modulates stress-coping behavior and the release of excitatory amino acids. Neuropsychopharmacology 2005, 30:223-230.
17. Fenoglio K.A., Chen Y., Baram T.Z. Neuroplasticity of the hypothalamic-pituitary-adrenal axis early in life requires recurrent recruitment of stress-regulating brain regions. J. Neurosci. 2006, 26:2434-2442.
18. Francis D.D., Chen Y., Baram T.Z. Environmental enrichment reverses the effects of maternal separation on stress reactivity. J. Neurosci. 2002, 22:7840-7843.
19. Gomez-Sanchez C.E., de Rodriguez A.F., Romero D.G., Estess J., Warden M.P., Gomez-Sanchez M.T., Gomez-Sanchez E.P. Development of a panel of monoclonal antibodies against the mineralocorticoid receptor. Endocrinology 2006, 147:1343-1348.
20. Heim C., Nemeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry 2001, 49:1023-1039.
21. Heim C., Shugart M., Craighead W.E., Nemeroff C.B. Neurobiological and psychiatric consequences of child abuse and neglect. Dev. Psychobiol. 2010, 52:671-690.
22. Herman J.P., Cullinan W.E. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci. 1997, 20:78-84.
23. Herman J.P., Ostrander M.M., Mueller N.K., Figueiredo H. Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog. Neuropsychopharmacol. Biol. Psychiatry 2005, 29:1201-1213.
24. Jiang Y.Q., Kawashima H., Iwasaki Y., Uchida K., Sugimoto K., Itoi K. Differential effects of forced swim-stress on the corticotropin-releasing hormone and vasopressin gene transcription in the parvocellular division of the paraventricular nucleus of rat hypothalamus. Neurosci. Lett. 2004, 358:201-204.
25. Kaufman J., Yang B.Z., Douglas-Palumberi H., Houshyar S., Lipschitz D., Krystal J.H., Gelernter J. Social supports and serotonin transporter gene moderate depression in maltreated children. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:17316-17321.
26. Kitraki E., Kremmyda O., Youlatos D., Alexis M.N., Kittas C. Gender-dependent alterations in corticosteroid receptor status and spatial performance following 21 days of restraint stress. Neuroscience 2004, 125:47-55.
27. Kozlovsky N., Zohar J., Kaplan Z., Cohen H. Microinfusion of a corticotrophin-releasing hormone receptor 1 antisense oligodeoxynucleotide into the dorsal hippocampus attenuates stress responses at specific times after stress exposure. J. Neuroendocrinol. 2012, 24:489-503.
28. Ladd C.O., Owens M.J., Nemeroff C.B. Persistent changes in corticotropin-releasing factor neuronal systems induced by maternal deprivation. Endocrinology 1996, 137:1212-1218.
29. Ladd C.O., Huot R.L., Thrivikraman K.V., Nemeroff C.B., Meaney M.J., Plotsky P.M. Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog. Brain Res. 2000, 122:81-103.
30. Ladd C.O., Huot R.L., Thrivikraman K.V., Nemeroff C.B., Plotsky P.M. Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo-pituitary-adrenal axis following neonatal maternal separation. Biol. Psychiatry 2004, 55:367-375.
31. Ladd C.O., Thrivikraman K.V., Huot R.L., Plotsky P.M. Differential neuroendocrine responses to chronic variable stress in adult Long Evans rats exposed to handling-maternal separation as neonates. Psychoneuroendocrinology 2005, 30:520-533.
32. Lajud N., Roque A., Cajero M., Gutiérrez-Ospina G., Torner L. Periodic maternal separation decreases hippocampal neurogenesis without affecting basal corticosterone during the stress hyporesponsive period, but alters HPA axis and coping behavior in adulthood. Psychoneuroendocrinology 2011, 37:410-420.
33. Lehmann J., Feldon J. Long-term biobehavioral effects of maternal separation in the rat: consistent or confusing?. Rev. Neurosci. 2000, 11:383-408.
34. Levine S. Influence of psychological variables on the activity of the hypothalamic-pituitary-adrenal axis. Eur. J. Pharmacol. 2000, 405:149-160.
35. Levine S., Stanton M.E., Gutierrez Y.R. Maternal modulation of pituitary-adrenal activity during ontogeny. Advances in experimental medicine and biology. Adv. Exp. Med. Biol. 1988, 245:295-310.
36. Liu D., Caldji C., Sharma S., Plotsky P.M., Meaney M.J. Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinepherine release in the hypothalamic paraventricular nucleus. J. Neuroendocrinol. 2000, 12:5-12.
37. Marti J., Armario A. Effects of diazepam and desipramine in the forced swimming test: influence of previous experience with the situation. Eur. J. Pharmacol. 1993, 236:295-299.
38. Meaney M.J., Bhatnagar S., Diorio J., Larocque S., Francis D., O'Donnell D., Shanks N., Sharma S., Smythe J., Viau V. Molecular basis for the development of individual differences in the hypothalamic-pituitary-adrenal stress response. Cell. Mol. Neurobiol. 1993, 13:321-347.
39. Meaney M.J., Diorio J., Francis D., Widdowson J., LaPlante P., Caldji C., Sharma S., Seckl J.R., Plotsky P.M. Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev. Neurosci. 1996, 18:49-72.
40. O'Malley D., Dinan T.G., Cryan J.F. Neonatal maternal separation in the rat impacts on the stress responsivity of central corticotropin-releasing factor receptors in adulthood. Psychopharmacology (Berl.) 2011, 214:221-229.
41. Oitzl M.S., Champagne D.L., van der Veen R., de Kloet E.R. Brain development under stress: hypotheses of glucocorticoid actions revisited. Neurosci. Biobehav. Rev. 2010, 34:853-866.
42. Panagiotaropoulos T., Diamantopoulou A., Stamatakis A., Dimitropoulou M., Stylianopoulou F. Learning of a T-maze by rat pups when contact with the mother is either permitted or denied. Neurobiol. Learn. Mem. 2009, 91:2-12.
43. Paxinos G., Wattson C. The Rat Brain in Stereotaxic Coordinates 2005, Elsevier, Amsterdam. 5th edition.
44. Plotsky P.M., Meaney M.J. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res. Mol. Brain Res. 1993, 18:195-200.
45. Plotsky P.M., Thrivikraman K.V., Nemeroff C.B., Caldji C., Sharma S., Meaney M.J. Long-term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring. Neuropsychopharmacology 2005, 30:2192-2204.
46. Porsolt R.D., Le Pichon M., Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977, 266:730-732.
47. Reul J.M., Holsboer F. On the role of corticotropin-releasing hormone receptors in anxiety and depression. Dialogues Clin. Neurosci. 2002, 4:31-46.
48. Ruedi-Bettschen D., Zhang W., Russig H., Ferger B., Weston A., Pedersen E.M., Feldon J., Pryce C.R. Early deprivation leads to altered behavioural, autonomic and endocrine responses to environmental challenge in adult Fischer rats. Eur. J. Neurosci. 2006, 24:2879-28793.
49. Smith G.W., Aubry J.M., Dellu F., Contarino A., Bilezikjian L.M., Gold L.H., Chen R., Marchuk Y., Hauser C., Bentley C.A., Sawchenko P.E., Koob G.F., Vale W., Lee K.F. Corticotropin releasing factor receptor 1-deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development. Neuron 1998, 20:1093-1102.
50. Smotherman W.P. Mother-infant interaction and the modulation of pituitary-adrenal activity in rat pups after early stimulation. Dev. Psychobiol. 1983, 16:169-176.
51. Stamatakis A., Pondiki S., Kitraki E., Diamantopoulou A., Panagiotaropoulos T., Raftogianni A., Stylianopoulou F. Effect of neonatal handling on adult rat spatial learning and memory following acute stress. Stress 2008, 11:148-159.
52. Sutanto W., Rosenfeld P., de Kloet E.R., Levine S. Long-term effects of neonatal maternal deprivation and ACTH on hippocampal mineralocorticoid and glucocorticoid receptors. Brain Res. Dev Brain Res. 1996, 92:156-163.
53. Veenema A.H., Blume A., Niederle D., Buwalda B., Neumann I.D. Effects of early life stress on adult male aggression and hypothalamic vasopressin and serotonin. Eur. J. Neurosci. 2006, 24:1711-1720.
54. Weaver I.C., Diorio J., Seckl J.R., Szyf M., Meaney M.J. Early environmental regulation of hippocampal glucocorticoid receptor gene expression: characterization of intracellular mediators and potential genomic target sites. Ann. N.Y. Acad. Sci. 2004, 1024:182-212.
55. Weinberg J., Levine S. Early handling influences on behavioral and physiological responses during active avoidance. Dev. Psychobiol. 1977, 10:161-169.
56. Wigger A., Neumann I.D. Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol. Behav. 1999, 66:293-302.
57. Workel J.O., Oitzl M.S., Fluttert M., Lesscher H., Karssen A., de Kloet E.R. Differential and age-dependent effects of maternal deprivation on the hypothalamic-pituitary-adrenal axis of brown Norway rats from youth to senescence. J. Neuroendocrinol. 2001, 13:569-580.
58. Zobel A.W., Nickel T., Künzel H.E., Ackl N., Sonntag A., Ising M., Holsboer F. Effects of the high-affinity corticotropin-releasing hormone receptor 1 antagonist R121919 in major depression: the first 20 patients treated. J. Psychiatr. Res. 2000, 34:171-181.