Abstract
One of the most important questions raised by modern psychiatry and experimental psychopathology is the origin of mental diseases. More concisely, clinical and experimental neurosciences are increasingly concerned with the factors that render one individual more vulnerable than another to a given pathological outcome. Animal models are now available to understand the sources of individual differences for specific phenotypes prone to behavioral disadaptations.
Over the last 10 years, we have explored the consequences of environmental perinatal maniqulations in the rat. We have shown that prenatal stress is at the origin of a wide range of physiological and behavioral aberrances such as alterations in the activity of the hormonal stress axis, increased vulnerability to drug of abuse, emotional liability, cognitive impairments and predisposition to pathological aging. Taken together, these abnormalities define a bio-behavioral syndrome. Furthermore, the cognitive disabilities observed in prenatally-stressed rats were recently related to an alteration of neurogenesis in the dentate gyrus, thus confirming the impact of early life events on brain morphology. A second model (handling model) has also been developed in which pups are briefly separated from their mothers during early postnatal life. In contrast with prenatallystressed animals, handled rats exhibited a reduced emotion response when confronted with novel situations and were protected against age-induced impairments of both the hormonal stress axis and cognitive functions.
Taken together, the results of these investigations show that the bio-behavioral phenotype that characterizes each individual is strongly linked to the nature and timing of perinatal experience. Furthermore, data collected in prenatally-stressed animals indicate that this model could be used profitably to understand the etiology and pathophysiology of affective disorders.
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Altman, J. and Das, G.D. (1965) “Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats”, J. Comp. Neurol. 124, 319–335.
Andreatini, R. and Leite, J.R. (1994) “The effect of corticosterone in rats submitted to the elevated plus-maze and to pentylenetetrazol-induced convulsions”, Prog. Neuro-Psychopharmacol. Biol. Psychiatry 18, 1333–1347.
Baez, M. and Volosin, M. (1994) “Corticosterone influences forced swim-induced immobility”, Pharmacol. Biochem. Behav. 49, 729–736.
Barbazanges, A., Piazza, P.V., Le Moal, M. and Maccari, S. (1996) “Maternal glucocorticoid secretion mediates long-term effects of prenatal stress”, J. Neurosci. 16, 3943–3949.
Barden, N., Reul, J.M. and Holsboer, F. (1995) “Do antidepressants stabilize mood through actions on the hypothalamic-pituitary-adrenocortical system?”, Trends Neurosci. 18, 6–11.
Bardo, M.T., Bevins, R.A., Klebaur, J.E., Crooks, P.A. and Dwoskin, L.P. (1997) “(−)-Nornicotine partially substitutes for (+)-amphetamine in a drug discrimination paradigm in rats”, Pharmacol. Biochem. Behav. 58, 1083–1087.
Bauman, R.A. and Kant, G.J. (1992) “Circadian effects of escapable and inescapable shock on the food intake and wheelrunning of rats”, Physiol. Behav. 51, 167–174.
Baxter, M.G. and Gallagher, M. (1996) “Neurobiological substrates of behavioral decline: models and data analytic strategies for individual differences in aging”, Neurobiol. Aging. 17, 491–495.
Birrell, C.E. and Balfour, D.J. (1998) “The influence of nicotine pretreatment on mesoaccumbens dopamine overflow and locomotor responses to d-amphetamine”, Psychopharmacology (Berl.) 140, 142–149.
Bohn, M.C., O'Banion, M.K., Young, D.A., Giuliano, R., Hussain, S., Dean, D.O. and Cunningham, L.A. (1994) “In vitro, studies of glucocorticoid effects on neurons and astrocytes”, Ann. N.Y. Acad. Sci. 746, 243–258, discussion, 258–9, 289–93.
Bradbury, M.J., Akana, S.F. and Dallman, M.F. (1994) “Roles of type I and II corticosteroid receptors in regulation of basal activity in the hypothalamo-pituitary-adrenal axis during the diurnal trough and the peak: evidence for a nonadditive effect of combined receptor occupation”, Endocrinology 134, 1286–1296.
Cador, M., Cole, B.J., Koob, G.F., Stinus, L. and Le Moal, M. (1993) “Central administration of corticotropin releasing factor induces long- term sensitization to d-amphetamine”, Brain Res. 606, 181–186.
Cameron, H.A., Woolley, C.S., McEwen, B.S. and Gould, E. (1993) “Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat”, Neuroscience 56, 337–344.
Cintra, A., Solfrini, V., Bunnemann, B., Okret, S., Bortolotti, F., Gustafsson, J.A. and Fuxe, K. (1993) “Prenatal development of glucocorticoid receptor gene expression and immunoreactivity in the rat brain and pituitary gland: a combined in situ hybridization and immunocytochemical analysis,”, Neuroendocrinology 57, 1133–1147.
Dallman, M.F., Levin, N., Cascio, C.S. Akana, S.F., Jacobson, L. and Kuhn, R.W. (1989) “Pharmacological evidence that the inhibition of diurnal adrenocorticotropin secretion by corticosteroids is mediated via type I corticosterone-preferring receptors”, Endocrinology 124, 2844–2850.
Deguchi, T. (1975) “Ontogenesis of a biological clock for serotonin: acetyl coenzyme A N-acetyltransferase in pineal gland of rat”, Proc. Natl Acad. Sci. USA 72, 2814–2818.
De Kloet, E.R. and Reul, J.M. (1987) “Feedback action and tonic influence of corticosteroids on brain function: a concept arising from the heterogeneity of brain receptor systems”, Psychoneuroendocrinology 12, 83–105.
De Kloet E.R., Rosenfeld, P., Van Eekelen, J.A., Sutanto, W. and Levine, S. (1988) “Stress, glucocorticoids and development”, Prog. Brain Res. 73, 101–120.
Delfs, J.M., Schreiber, L. and Kelley, A.E. (1990) “Microinjection of cocaine into the nucleus accumbens elicits locomotor activation in the rat”, J. Neurosci. 10, 303–310.
Dellu, F., Mayo, W., Vallée, M., Maccari, S., Piazza, P.V., Le Moal, M. and Simon, H. (1996) “Behavioral reactivity to novelty during youth as a predictive factor of stress-induced corticosterone secretion in the elderly—a life-span study in rats”, Psychoneuroendocrinology 21, 441–453.
Deminiere, 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.
Denenberg, V.H. (1980) “General systems theory, brain organization, and early experiences”, Am. J. Physiol. 238, R3-R13.
Deroche, V., Piazza, P.V. Casolini, P., Maccari, S., Le Moal, M. and Simon, H. (1992) “Stress-induced sensitization to amphetamine and morphine psychomotor effects depend on stress-induced corticosterone secretion”, Brain Res. 598, 343–348.
Deroche, V., Marinelli, M., Maccari, S., Le Moal, M., Simon, H. and Piazza, P.V. (1995) “Stress-induced sensitization and glucocorticoids I. Sensitization of dopamine-dependent locomotor effects of amphetamine and morphine depends on stress-induced corticosterone secretion”, J. Neurosci. 15, 7181–7188.
Diaz, R., Brown, R.W. and Seckl, J.R. (1998) “Distinct ontogeny of glucocorticoid and mineralocorticoid receptor and 11 betahydroxysteroid dehydrogenase types I and II mRNAs in the fetal rat brain suggest a complex control of glucocorticoid actions”, J. Neurosci. 18, 2570–2580.
Glover, V. (1997) “Maternal stress or anxiety in pregnancy and emotional development of the child”, Br. J. Psychiatry 171, 105–106.
Gould, E., Cameron, H.A., Daniels, D.C., Woolley C.s. and McEwen, B.S. (1992) “Adrenal hormones suppress cell division in the adult rat dentate gyrus”, J. Neurosci. 12, 3642–3650.
Gould, E., Beylin, A., Tanapat, P., Reeves, A. and Shors, T.J. (1999a) “Learning enhances adult neurogenesis in the hippocampal formation [see comments]”, Nat. Neurosci. 2, 260–265.
Gould, E., Tanapat, P., Hastings, N.B. and Shors, T.J. (1999b) “Neurogenesis in adulthood: a possible role in learning”, Trends Cognit. Sci. 3, 186–192.
Graham, Y.P., Heim, C., Goodman, S.H., Miller, A.H. and Nemeroff, C.B. (1999) “The effects of neonatal stress on brain development: implications for psychopathology”, Dev. Psychopathol. 11, 545–565.
Hall, C.S. (1934) “Drive and emotionality factors associated with adjustment in the rat”, J Comp. Psychol. 17, 89–108.
Hassan, A.H., Patchev, V.K., von Rosenstiel, P., Holsboer, F. and Almeida, O.F. (1999) “Plasticity of hippocampal corticosteroid receptors during aging in the rat”, FASEB J. 13, 115–122.
Hayashi, A., Nagaoka, M., Yamada, K., Ichitani, Y., Miake, Y. and Okado, N. (1998) “Maternal stress induces synaptic loss and developmental disabilities of offspring,” Int. J. Dev. Neurosci. 16, 209–216.
Henry, C., Kabbaj, M., Simon, H., Le Moal M. and Maccari, S. (1994) “Prenatal stress increases the hypothalamo-pituitaryadrenal axis response in young and adult rats”, J. Neuroendocrinol. 6, 341–345.
Henry, C., Guegant, G., Cador, M., Arnauld, E., Arsaut, J., Le Moal, M. and Demotes-Mainard, J. (1995) “Prenatal stress in rats facilitates amphetamine-induced sensitization and induces long-lasting changes in dopamine receptors in the nucleus accumbens”, Brain Res. 685, 179–186.
Herman, J.P., Schafer, M.K., Young, E.A., Thompson, R., Douglass, J., Akil, H. and Watson, S.J. (1989) “Evidence for hippocampal regulation of neuroendocrine neurons of the hypothalamo-pituitary-adrenocortical axis”, J. Neurosci. 9, 3072–3082.
Hiroshige, T., Honma, K. and Watanabe, K. (1982a) “Ontogeny of the circadian rhythm of plasma corticosterone in blind infantile rats”, J. Physiol. (Lond.) 325, 493–506.
Hiroshige, T., Honma, K. and Watanabe, K., (1982b) “Possible zeitgebers for external entrainment of the circadian rhythm of plasma corticosterone in blind infantile rats”, J. Physiol. (Lond.) 325, 507–519.
Hiroshige, T., Honma, K. and Watanabe K. (1982c) “Prenatal onset and maternal modifications of the circadian rhythm of plasma corticosterone in blind infantile rats”, J. Physiol. (Lond.) 325, 521–532.
Holsboer, F. (1989) “Psychiatric implications of altered limbichypothalamic-pituitary-adrenocortical activity”, Eur. Arch. Psychiatry Neurol. Sci 238, 302–322.
Huttunen, M.O. (1971) “Persistent alteration of turnover of brain noradrenaline in the offspring of rats subjected to stress during pregnancy”, Nature 230, 53–55.
Issa, A.M., Rowe, W., Gauthier, S. and Meaney, M.J. (1990) “Hypothalamic-pituitary-adrenal activity in aged, cognitively impaired and cognitively unimpaired rats”, J. Neurosci. 10, 3247–3254.
Joffe, J.M. (1965) “Genotype and prenatal and premating stress interact to affect adult behavior in rats”, Science 150, 1844–1845.
Joffe, J.M. (1969) “Perinatal determinants of emotionality”, Ann. N.Y. Acad. Sci. 159, 668–680.
Joyce, E. M. and Iversen, S.D. (1979) “The effect of morphine applied locally to mesencephalic dopamine cell bodies on spontaneous motor activity in the rat”, Neurosci. Lett. 14, 207–212.
Jung, M.W. and McNaughton, B.L. (1993) “Spatial selectivity of unit activity in the hippocampal granular layer”, Hippocampus 3, 165–182.
Kant, G.J., Pastel, R.H., Bauman, R.A., Meininger, G.R., Maughan, K.R., Robinson, 3rd, T.N., Wright, W.L. and Covington, P.S. (1995) “Effects of chronic stress on sleep in rats”, Physiol. Behav. 57, 359–365.
Kirschbaum, C., Wolf, O.T., May, M., Wippich, W. and Hellhammer, D.H. (1996) “Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults”, Life Sci. 58, 1475–1483.
Koehl, M., Barbazanges, A., Le Moal, M. and Maccari, S. (1997) “Prenatal stress induces a phase advance of circadian corticosterone rhythm in adult rats which is prevented by postnatal stress”, Brain Res. 759, 317–320.
Koehl, M., Darnaudery, M., Dulluc, J., Van Reeth, O., Le Moal, M. and Maccari, S. (1999) “Prenatal stress alters circadian activity of hypothalamo-pituitary-adrenal axis and hippocampal corticosteroid receptors in adult rats of both gender”, J. Neurobiol. 40, 302–315.
Koehl, M., Bjijou, Y., Le Moal, M. and Cador, M. (2000) “Nicotineinduced locomotor activity is increased by preexposure of rats to prenatal stress”, Brain Res. 882, 196–200.
Koob, G.F. and Bloom, F.E. (1988) “Cellular and molecular mechanisms of drug dependence”, Science 242, 715–723.
Landfield, P.W., Waymire, J.C. and Lynch, G. (1978) “Hippocampal aging and adrenocorticoids: quantitative correlations”, Science 202, 1098–1102.
Lemaire, V., Koehl, M., Le Moal, M. and Abrous, D.N. (2000) “Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus”, Proc. Natl Acad. Sci. USA 97, 11032–11037.
Levine, S. (1962) “Plasma free corticosteroid response to electric shock in rats stimulated in infancy”, Science 135, 795–796.
Levine, S. and Lewis, G.W. (1959) “Critical period for the effects of infantile experience on maturation of stress”, Science, 129, 42–43.
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P.M. and Meaney, M.J. (1997) “Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress”, Science 277, 1659–1662.
Lupien, S., Lecours, A.R., Lussier, I., Schwartz, G., Nair, N.P. and Meaney, M.J. (1994) “Basal cortisol levels and cognitive deficits in human aging”, J. Neurosci. 14, 2893–2903.
Lupien, S.J., Gaudreau, S., Tchiteya, B.M., Maheu, F., Sharma, S., Nair, N.P., Hauger, R.L., McEwen, B.S. and Meaney, M.J. (1997) “Stress-induced declarative memory impairment in healthy elderly subjects: relationship to cortisol reactivity”, J. Clin. Endocrinol. Metab. 82, 2070–2075.
Lupien, S.J., de Leon, M., de Santi, S., Convit, A., Tarshish, C., Nair, N.P., Thakur, M., McEwen, B.S., Hauger, R.L. and Meaney, M.J. (1998) “Cortisol levels during human aging predict hippocampal atrophy and memory deficits”, Nat. Neurosci. 1, 69–73.
Maccari, S., Piazza, P.V., Deminiere, J.M., Angelucci, L., Simon, H. and Le Moal, M. (1991) “Hippocampal type I and type II corticosteroid receptor affinities are reduced in rats predisposed to develop amphetamine self-administration”, Brain Res. 548, 305–309.
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.
Marinelli, M., Piazza, P.V., Deroche, V., Maccari, S., Le Moal, M. and Simon, H. (1994) “Corticosterone circadian secretion differentially facilitates dopamine-mediated psychomotor effect of cocaine and morphine”, J Neurosci. 14, 2724–2731.
Marti, O., Marti, J. and Armario, A. (1994) “Effects of chronic stress on food intake in rats: influence of stressor intensity and duration of daily exposure” Physiol. Behav. 55, 747–753.
McEwen, B.S. and Sapolsky, R.M. (1995) “Stress and cognitive function”, Curr. Opin. Neurobiol. 5, 205–216.
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.
McGaugh, J.L. (1989) “Dissociating learning and performance: drug and hormone enhancement of memory storage”, Brain Res. Bull. 23, 339–345.
McNaughton, B.L., Barnes, C.A., Meltzer, J. and Sutherland, R.J. (1989) “Hippocampal granule cells are necessary for normal spatial learning but not for spatially-selective pyramidal cell discharge”, Exp. Brain Res. 76, 485–496.
Meaney, M.J., Aitken, D.H., Bodnoff, S.R., Iny, L.J. and Sapolsky, R.M. (1985a) “The effects of postnatal handling on the development of the glucocorticoid receptor systems and stress recovery in the rat”, Prog Neuro-Psychopharmacol. Biol. Psychiatry 9, 731–734.
Meaney, M.J., Aitken, D.H., Bodnoff, S.R., Iny, L.J., Tatarewicz, J.E. and Sapolsky, R.M. (1985b) “Early postnatal handling alters glucocorticoid receptor concentrations in selected brain regions”, Behav. Neurosci. 99, 765–770.
Meaney, M.J., Sapolsky, R.M. and McEwen, B.S. (1985c) “The development of the glucocorticoid receptor system in the rat limbic brain I. Ontogeny and autoregulation”, Brain Res. 350, 159–164.
Meaney, M.J., Sapolsky, R.M. and McEwen, B.S. (1985d) “The development of the glucocorticoid receptor system in the rat limbic brain II. An autoradiographic study”, Brain Res. 350, 165–168.
Meaney, M.J., Bhatnagar, S., Larocque, S., McCormick, C., Shanks, N., Sharma, S., Smythe, J., Viau, V. and Plotsky, P.M. (1993) “Individual differences in the hypothalamic-pituitaryadrenal stress response and the hypothalamic CRF system”, Ann. N.Y. Acad. Sci. 697, 70–85.
Milkovic, S., Milkovic, K. and Paunovic, J. (1973) “The initiation of fetal adrenocorticotrophic activity in the rat”, Endocrinology 92, 380–384.
Montaron, M.F., Petry, K.G., Rodriguez, J.J., Marinelli, M., Aurousseau, C., Rougon, G., Le, Moal, M. and Abrous, D.N. (1999) “Adrenalectomy increases neurogenesis but not PSANCAM expression in aged dentate gyrus”, Eur. J. Neurosci. 11, 1479–1485.
Ohkawa, T., Takeshita, S., Murase, T., Kambegawa, A., Okinaga, S. and Arai, K. (1991) “Ontogeny of the response of the hypothalamo-pituitary-adrenal axis to maternal immobilization stress in rats”, Endocrinol. Jpn 38, 187–194.
pardridge, W.M., Sakiyama, R. and Judd, H.L. (1983) “Proteinbound corticosteroid in human serum is selectively transported into rat brain and liver in vivo”, J. Clin. Endocrinol. Metab. 57, 160–165.
Piazza, P.V. and Le Moal, M.L. (1996) “Pathophysiological basis of vulnerability to drug abuse: role of an interaction between stress, glucocorticoids, and dopaminergic neurons”, Annu. Rev. Pharmacol. Toxicol. 36., 359–378.
Piazza, P.V., Deminiere, J.M., Le Moal, M. and Simon, H. (1989) “Factors that predict individual vulnerability to amphetamine self-administration”, Science 245., 1511–1513.
Piazza, P.V., Maccari, S., Deminiere, J.M., Le Moal, M., Mormede, P. and Simon, H. (1991a) “Corticosterone levels determine individual vulnerability to amphetamine self-administration”, Proc. Natl Acad. Sci. USA 88, 2088–2092.
Piazza, P.V., Rouge-Pont, F., Deminiere, J.M., Kharoubi, M., Le Moal, M. and Simon, H. (1991b) “Dopaminergic activity is reduced in the prefrontal cortex and increased in the nucleus accumbens of rats predisposed to develop amphetamine self-administration”, Brain Res. 567, 169–174.
Rapp, P.R. and Amaral, D.G. (1992) “Individual differences in the cognitive and neurobiological consequences of normal aging”, Trends Neurosci. 15, 340–345.
Ratka, A., Sutanto, W., Bloemers, M. and de Kloet, E.R. (1989) “On the role of brain mineralocorticoid (type I) and glucocorticoid (type II) receptors in neuroendocrine regulation”, Neuroendocrinology 50, 117–123.
Reppert S.M. and Schwartz, W.J. (1983) “Maternal coordination of the fetal biological clock in utero”, Science 220, 969–971.
Reul, J.M. and de Kloet, E.R. (1985) “Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation”, Endocrinology 117, 2505–2511.
Reul, J.M. and de Kloet, E.R. (1986) “Anatomical resolution of two types of corticosterone receptor sites in rat brain with in vitro autoradiography and computerized image analysis”, J. Steroid Biochem. 24, 269–272.
Robbins, T.W. and Everitt, B.J. (1982) “Functional studies of the central catecholamines”, Int. Rev. Neurobiol. 23, 303–365.
Rosenfeld, P., Sutanto, W., Levine, S. and De Kloet, E.R. (1988) “Ontogeny of type I and type II corticosteroid receptors in the rat hippocampus”, Brain Res. 470, 113–118.
Rouge-Pont, F., Marinelli, M., Le Moal, M., Simon, H. and Piazza, P.V. (1995) “Stress-induced sensitization and glucocorticoids. II. Sensitization of the increase in extracellular dopamine induced by cocaine depends on stress-induced corticosterone secretion”, J. Neurosci. 15, 7189–7195.
Rouge-Pont, F., Deroche, V., Le Moal, M. and Piazza, P.V. (1998) “Individual differences in stress-induced dopamine release in the nucleus accumbens are influenced by corticosterone” Eur. J. Neurosci. 10, 3903–3907.
Sandi, C., Loscertales, M. and Guaza, C. (1997) “Experiencedependent facilitating effect of corticosterone on spatial emmory formation in the water maze”, Eur. J. Neurosci. 9, 637–642.
Sapolsky, R.M. (1992), Stress, the Aging Brain, and the Mechanisms of Neuron Death (MIT Press, Cambridge).
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.
Sapolsky, R.M., Krey, L.C. and McEwen, B.S. (1984) “Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response”, Proc. Natl Acad. Sci. USA 81, 6174–6177.
Sapolsky, R.M., Krey, L.C. and McEwen, B.S. (1986) “The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis”, Endocr. Rev. 7, 284–301.
Schopke, R., Wolfer, D.P., Lipp, H.P. and Leisinger-Trigona, M.C. (1991) “Swimming navigation and structural variations of the infrapyramidal mossy fibers in the hippocampus of the mouse”, Hippocampus 1, 315–328.
Schwegler, H. and Crusio, W.E. (1995) “Correlations between radial-maze learning and structural variations of septum and hippocampus in rodents”, Behav. Brain Res. 67, 29–41.
Spencer, R.L., Kim, P.J., Kalman, B.A. and Cole, M.A. (1998) “Evidence for mineralocorticoid receptor facilitation of glucocorticoid receptor-dependent regulation of hypothalamic-pituitary-adrenal axis activity”, Endocrinology 139, 2718–2726.
Squire, L.R. (1992) “Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans”, Psychol. Rev. 99, 195–231, Published erratum appears in Psychol. Rev. 99(3): Jul. (1992) 582.
Stanfield, B.B. and Trice, J.E. (1988) “Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections”, Exp. Brain. Res. 72, 399–406.
Stenzel-Poore, M.P., Heinrichs, S.C., Rivest, S., Koob, G.F. and Vale, W.W. (1994) “Overproduction of corticotropin-releasing factor in transgenic mice: a genetic model of anxiogenic behavior”, J. Neurosci. 14, 2579–2584.
Suchecki, D., Rosenfeld, P. and Levine, S. (1993) “Maternal regulation of the hypothalamic-pituitary-adrenal axis in the infant rat: the roles of feeding and stroking”, Brain Res. Dev. Brain Res. 75, 185–192.
Suchecki, D., Nelson, D.Y., Van Oers, H. and Levine, S. (1995) “Activation and inhibition of the hypothalamic-pituitaryadrenal axis of the neonatal rat: effects of maternal deprivation”, Psychoneuroendocrinology 20, 169–182.
Takahashi, L.K., Turner, J.G. and Kalin, N.H. (1992) “Prenatal stress alters brain catecholaminergic activity and potentiates stress-induced behavior in adult rats”, Brain Res. 574, 131–137.
Vaid, R.R., Yee, B.K., Shalev, U., Rawlins, J.N., Weiner, I., Feldon, J. and Totterdell, S. (1997) “Neonatal nonhandling and in utero prenatal stress reduce the density of NADPH-diaphorase-reactive neurons in the fascia dentata and Ammon's horn of rats”, J. Neurosci. 17, 5599–5609.
Vallée, M., Mayo, W., Dellu, F., Le Moal, M., Simon, H. and Maccari, S. (1997) “Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion”, J. Neurosci. 17, 2626–2636.
Vallée, M., MacCari, S., Dellu, F., Simon, H., Le Moal, M. and Mayo, W. (1999) “Long-term effects of prenatal stress and postnatal handling on age-related glucocorticoid secretion and cognitive performance: a longitudinal study in the rat”, Eur. J. Neurosci. 11, 2906–2916.
Veldhuis, H.D., De Kloet, E.R., Van Zoest, I and Bohus, B. (1982) “Adrenalectomy reduces exploratory activity in the rat: a specific role of corticosterone”, Horm. Behav. 16, 191–198.
Ward, I.L. (1972) “Prenatal stress feminizes and demasculinizes the behavior of males”, Science 175, 82–84.
Ward, I.L. (1984) “The prenatal stress syndrome: current status”, Psychoneuroendocrinology 9, 3–11.
Walker, C.D., Scribner, K.A., Cascio, C.S and Dallman, M.E. (1991) “The pituitary-adrenocortical system of neonatal rats is responsive to stress throughout development in a time-dependent and stressor-specific fashion”, Endocrinology 128, 1385–1395.
Weinstock, M. (1997) “Does prenatal stress impair coping and regulation of hypothalamic-pituitary-adrenal axis?”, Neurosci. Biobehav. Rev. 21, 1–10.
Weinstock, M. (2001) “Alterations induced by gestational stress in brain morphology and behaviour of the offspring”, Prog. Neurobiol. 65, 427–451.
West, M.J. and King, A.P. (1987) “Settling nature and nurture into an ontogenetic niche”, Dev. Psychobiol. 20, 549–562.
Yau, J.L., Olsson, T., Morris, R.G., Meaney, M.J. and Seckl, J.R. (1995) “Glucocorticoids, hippocampal corticosteroid receptor gene expression and antidepressant treatment: relationship with spatial learning in young and aged rats”, Neuroscience 66, 571–581.
Zarrow, M.X., Philpott, J.E. and Denenberg, V.H. (1970) “Passage of 14C-4-corticosterone from the rat mother to the foetus and neonate”, Nature 226, 1058–1059.
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Koehl, M., Lemaire, V., Mayo, W. et al. Individual vulnerability to substance abuse and affective disorders: Role of early environmental influences. neurotox res 4, 281–296 (2002). https://doi.org/10.1080/1029842021000010866
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DOI: https://doi.org/10.1080/1029842021000010866