Effect of increased maternal corticosterone during lactation on hippocampal corticosteroid receptors, stress response and learning in offspring in the early stages of life

Neuroscience

Volumn 79, Issue 4, 1997, Pages 1005-1012

  Casolini, P ^a   Cigliana, G ^b   Alema G S ^a   Ruggieri, V ^a   Angelucci, L ^a   Catalani, A ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b IRCCS SAN RAFFAELE PISANA   (Italy)

Author keywords

Corticosteroid receptors; Corticosterone; HPA axis; Lactation; Morris water maze; T maze

Indexed keywords

CORTICOSTEROID RECEPTOR; CORTICOSTERONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LACTATION; LEARNING; MAZE TEST; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; STRESS;

ANIMALS; CORTICOSTERONE; EMBRYONIC AND FETAL DEVELOPMENT; FEMALE; HIPPOCAMPUS; LACTATION; MATERNAL-FETAL EXCHANGE; MAZE LEARNING; PREGNANCY; RATS; RATS, WISTAR; RECEPTORS, STEROID; STRESS;

EID: 0030825439     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(96)00668-9     Document Type: Article

References (48)

1. Angelucci L., Patacchioli F. R., Bohus B. and de Kloet E. R. (1982) Serotonin innervation and glucocorticoid binding in the rat hippocampus: relevance to depression. In Typical and Atypical Antidepressants: Molecular Mechanisms (eds Costa E. and Racagni G.), pp. 365-370. Raven Press, New York.
2. Angelucci L., Patacchioli F. R., Scaccianoce S., Di Sciullo A., Cardillo A. and Maccari S. (1985) A model for later-life effects of perinatal drug exposure: maternal hormone mediation. Neurobehav. Toxicol. Teratol. 7, 511-517.
3. Beaumont K. and Fanestil D. (1983) Characterization of rat brain aldosterone receptors reveals high affinity for corticosterone. Neuroendocrinology 113, 2043-2051.
4. Bohn M. C. (1980) Granule cell genesis in the hippocampus of rats treated neonatally with hydrocortisone. Neuroscience 5, 2003-2012.
5. 2 agonist LY 171555 decreases the affinity of type II corticosteroid receptors in rat hippocampus and ventral striatum. Neuroscience 60, 939-943.
6. Casolini P., Piazza P. V., Kabbaj M., Leprat F., Angelucci L., Simon H., Le Moal M. and Maccari S. (1993) The mesolimbic dopaminergic system exerts an inhibitory influence on brain corticosteroid receptor affinities. Neuroscience 55, 429-434.
7. Castro C. A., Paylor R. and Rudy J. W. (1987) A developmental analysis of the learning and short-term memory processes mediating performance in conditional-spatial discrimination problems. Psychobiology 15, 308-316.
8. Catalani A., Marinelli M., Scaccianoce S., Nicolai R., Muscolo L. A. A., Porcu A., Korányi L., Piazza P. V. and Angelucci L. (1993) Progeny of mothers drinking corticosterone during lactation has lower stress-induced cortico-sterone secretion and better cognitive performance. Brain Res. 624, 209-215.
9. de Kloet E. R. (1991) Brain corticosteroid receptor balance and homeostatic control. Front. Neuroendocrinol. 12, 95-164.
10. Deminiére J. M., Piazza P. V., Guegan G., Abrous N., Maccari S., Le Moal M. and Simon H. (1992) Increased locomotor response to novelty and propensity to intravenous amphetamine self-administration in adult offspring of stressed mothers. Brain Res. 586, 135-139.
11. Denenberg V. H., Brumaghim J. T., Haltmeyer G. C. and Zarrow M. X. (1967) Increased adrenocortical activity in the neonatal rat following handling. Endocrinology 81, 1047.
12. Denenberg V. H., Ottinger D. R. and Stephen M. W. (1962) Effects of maternal factors upon growth and behavior of the rat. Child Dev. 33, 65-71.
13. Eck J. B. and Kuhn C. M. (1992) Effect of ether stress on growth hormone during development in the neonatal rat. Neuroendocrinology 56, 605-610.
14. Gould E., Woolley C. S. and McEwen B. S. (1990) Short-term glucocorticoid manipulations affect neuronal morphology and survival in the adult dentate gyrus. Neuroscience 37, 367-375.
15. Gould E., Woolley C. S. and McEwen B. S. (1991) The hippocampal formation: morphological changes induced by thyroid, gonadal and adrenal hormones. Psychoneuroendocrinology 16, 67-84.
16. Green R. J. and Stanton M. E. (1989) Differential ontogeny of working memory and reference memory in the rat. Behav. Neurosci. 103, 98-105.
17. Henning S. J. (1978) Plasma concentrations of total and free corticosterone during development in the rat. Am. J. Physiol. 235, E451-E456.
18. Henry C., Kabbaj M., Simon H., Le Moat M. and Maccari S. (1994) Prenatal stress increases the hypothalamo-pituitary-adrenal axis response in young and adult rats. J. Neuroendocrinol. 6, 341-345.
19. Kalimi M. and Hubbard J. R. (1983) Development of an exchange essay for cytosolic glucocorticoid receptors using the synergic effects of molybdate plus dithiotreitol. Endocrinology 113, 1161-1163.
20. Kuhn C. M., Pauk J. and Schanberg S. M. (1990) Endocrine responses to mother-infant separation in developing rats. Devl Psychobiol. 23, 395-410.
21. Lee M. H. S. and Williams D. I. (1974) Changes in licking behavior of the rat mother following handling of young. Anim. Behav. 22, 679-681.
22. Levine S. and Thoman E. B. (1969) Physiological and behavioral consequences of postnatal maternal stress in rats. Physiol. Behav. 4, 139-142.
23. Lowry O. H., Rosenbrough N., Farr A. L. and Randall R. J. (1951) Protein measurement with the Folin phenol reagent. J. biol. Chem. 193, 265-267.
24. Maccari S., Mormède P., Piazza P. V., Simon H., Angelucci L. and Le Moat M. (1992) Hippocampal type I and type II corticosteroid receptors are modulate by central noradrenergic systems. Psychoneuroendocrinology 17, 103-112.
25. Maccari S., Piazza P. V., Kabbaj M., Barbazanges A., Simon H. and Le Moal M. (1995) Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J. Neurosci. 15, 110-116.
26. Maccari S., Piazza P. V., Rougé-Pont F., Angelucci L., Simon H. and Le Moal M. (1992) Noradrenergic regulation of type I and type II corticosteroid receptors in amygdala and hypothalamus. Brain Res. 587, 313-318.
27. McEwen B. S., de Kloet E. R. and Rostene W. (1986) Adrenal steroid receptors and actions in the nervous system. Physiol. Rev. 66, 1121-1188.
28. Meaney M. J. and Aitken D. H. (1985) The effects of early postnatal handling on hippocampal glucocorticoid receptor concentrations: temporal parameters. Brain Res. 354, 301-304.
29. Meaney M. J., Aitken D. H., Viau V., Sharma S. and Sarrieau A. (1989) Neonatal handling alters adrenocortical negative feedback sensitivity and hippocampal type II glucocorticoid receptor binding in the rat. Neuroendocrinology 50, 597-604.
30. Meaney M. J., Bhatnagar S., Diorio J., Larocque S., Francis D., O'Donnell D., Shanks N., Sharma S., Smythe J. and Viau V. (1993) Molecular basis for the development of individual differences in the hypothalamic-pituitary-adrenal stress response. Cell. molec. Neurobiol. 13, 321-347.
31. Meaney M. J., Viau V., Aitken D. H. and Bhatnagar S. (1988) Stress-induced occupancy and translocation of hippocampal glucocorticoid receptors. Brain Res. 445, 198-203.
32. Meyer J. S. (1985) Biochemical effects of corticosteroids on neural tissues. Physiol. Rev. 65, 946-1020.
33. Mitchell J. B., Iny L. J. and Meaney M. J. (1990) The role of serotonin in the development and environmental regulation of hippocampal type II corticosteroid receptor binding. Devl Brain Res. 56, 231-235.
34. Mitchell J. B., Rowe W., Boksa P. and Meaney M. A. (1990) Serotonin regulates type II corticosteroid receptor binding in hippocampal cell cultures. J. Neurosci. 10, 1745-1752.
35. Moguilevski M. and Raynaud J. P. (1980) Evidence for a specific mineralcorticoid receptor in rat pituitary and brain. J. steroid Biochem. 12, 309-315.
36. Oitzl M. S. and de Kloet E. R. (1992) Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav. Neurosci. 106, 62-71.
37. Olton D. S. (1983) Memory functions and the hippocampus. In Neurobiology of the Hippocampus (ed. Seifert W.), pp. 335-373. Academic, London.
38. Pihoker C., Owens M. J., Kuhn C. M., Schanberg S. M. and Nemeroff C. B. (1993) Maternal separation in neonatal rats elicits activation of the hypothalamic-pituitary-adrenocortical axis: a putative role for corticotropin-releasing factor. Psychoneuroendocrinology 18, 485-493.
39. Ratka A., Sutanto W., Bloemers M. and de Kloet E. R. (1989) On the role of brain mineralcorticoid (type I) and glucocorticoid (type II) receptors in neuroendocrine regulation. Neuroendocrinology 50, 117-123.
40. Rosenfeld P., Eekelen J. A. M., Levine S. and Kloet E. (1993) Ontogeny of corticosteroid receptors in the brain. Cell. molec. Neurobiol. 13, 295-317.
41. Rudy J. W., Stadler Morris S. and Albert P. (1987) Ontogeny of spatial navigation behaviors in the rat: dissociation of "proximal"- and "distal"-cue-based behaviors. Behav. Neurosci. 101, 62-73.
42. Sapolsky R. M. and Meaney M. J. (1986) Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res. 396, 64-76.
43. Scatchard G. (1949) The attraction of proteins for small molecules and ions. Ann. N. Y. Acad. Sci. 51, 660.
44. Smotherman W. P., Wiener S. G., Mendoza S. P. and Levine S. (1977) Maternal pituitary-adrenal responsiveness as a function of differential treatment of rat pups. Devl Psychobiol. 10, 113-122.
45. Squire L. R. (1983) The hippocampus and the neuropsychology of memory. In Neurobiology of the Hippocampus (ed. Seifert W.), pp. 491-511. Academic, London.
46. Sugishita M., Takashima M., Takeuchi Y., Kato Y., Yamauchi T. and Takahashi L. K. (1993) Periodic mother deprivation during the light period reversed the phase of serotonin N-Acetyltransferase activity rhythm of the pineal gland in rat pups. Pharmac. Biochem. Behav. 46, 609-615.
47. Walker C. D. and Aubert M. L. (1988) Effects of early undernutrition and handling on the adrenocortical activity of neonatal rats. Life Sci. 43, 1983-1990.
48. Weinstock M., Fride E. and Hertzberg R. (1988) Prenatal stress effects on functional development of the offspring. Prog. Brain Res. 73, 319-331.