Long-term effects of prenatal stress experience and postnatal maternal separation on emotionality and attentional processes

Behavioural Brain Research

Volumn 107, Issue 1-2, 2000, Pages 133-144

  Lehmann, Julia ^a   Stöhr, Thomas ^a   Feldon, Joram ^a  

^a SWISS FEDERAL INSTITUTE OF TECHNOLOGY   (Switzerland)

Author keywords

Latent inhibition; Maternal separation; Open field; Prenatal stress; Prepulse inhibition; Sex differences

Indexed keywords

ANIMAL MODEL; ARTICLE; ATTENTION; BEHAVIOR; CONTROLLED STUDY; EMOTIONALITY; FEAR; FEMALE; FETUS; LATENT INHIBITION; MALE; NONHUMAN; PRENATAL PERIOD; PREPULSE INHIBITION; PRIORITY JOURNAL; RAT; SEPARATION ANXIETY; SEX DIFFERENCE; STRESS;

ANIMALS; AROUSAL; ATTENTION; AVOIDANCE LEARNING; CONDITIONING, CLASSICAL; EMOTIONS; FEAR; FEMALE; MALE; MATERNAL DEPRIVATION; MOTOR ACTIVITY; NEURAL INHIBITION; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; SEX FACTORS; STARTLE REACTION; STRESS;

EID: 0344771166     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-4328(99)00122-9     Document Type: Article

References (72)

1. Ader R., Belfer M.L. Prenatal maternal anxiety and offspring emotionality in the rat. Psychol. Rep. 10:1962;711-718.
2. Alonso J., Castellano M.A., Rodriguez M. Behavioral lateralization in rats: prenatal stress effects on sex differences. Brain Res. 539:1991;45-50.
3. Alonso S.J., Arevalo R., Afonso D., Rodriguez M. Effects of maternal stress during pregnancy on forced swimming test behavior of the offspring. Physiol. Behav. 50:1991;511-517.
4. Alonso S.J., Navarro E., Rodriguez M. Permanent dopaminergic alterations in the n. accumbens after prenatal stress. Pharmacol. Biochem. Behav. 49(2):1994;353-358.
5. Archer J.E., Blackman D.E. Prenatal psychological stress and offspring behavior in rats and mice. Dev. Psychobiol. 4(3):1971;193-248.
6. Barbazanges A., Vallee M., Mayo W., Day J., Simon H., Le Moal M., Maccari S. Early and later adoptions have different long-term effects on male rat offspring. J. Neurosci. 16(23):1996;7783-7790.
7. Biagini G., Pich E.M., Carani C., Marrama P., Agnati L.F. Postnatal maternal separation during stress hyporesponsive period enhances the adrenocortical response to novelty in adult rats by affecting feedback regulation in the CA1 hippocampal field. Int. J. Dev. Neurosci. 16(3-4):1989;187-197.
8. Chapman R.H., Stern J.M. Failure of severe maternal stress or ACTH during pregnancy to affect emotionality of male rat offspring: implications of litter size effects for prenatal studies. Dev. Psychobiol. 12(3):1979;255-267.
9. Crnic L.C. Separation-induced early malnutrition: maternal, physiological and behavioral effects. Physiol. Behav. 26:1981;695-707.
10. Denenberg V.H. Assessing the effects of early experience. Myers R.D. Methods in Psychobiology. 3:1977;Academic Press, New York.
11. Ellenbroek B.A., Cools A.R. Maternal separation reduces latent inhibition in the conditioned taste aversion paradigm. Neurosci. Res. Commun. 17(1):1995;27-33.
12. Ellenbroek B.A., Budde S., Cools A.R. Prepulse inhibition and latent inhibition: the role of dopamine in the medial prefrontal cortex. Neuroscience. 75(2):1996;535-542.
13. Ellenbroek B.A., van den Kroonenberg P.T.J.M., Cools A.R. The effects of an early stressful life event on sensorimotor gating in adult rats. Schizophr. Res. 30:1998;251-260.
14. Feldon J., Weiner I. An animal model of attention deficit. Boulton A.A., Baker G.B., Martin-Iverson M.T. Animal Models in Psychiatry, Neuromethods. 18:1991;313-361 Humana Press, Clifton, NJ.
15. Feldon J., Weiner I. From an animal model of an attentional deficit towards new insights into the pathophysiology of schizophrenia. J. Psychiatric Res. 26(4):1992;345-366.
16. Feldon J., Avnimelech-Gigus N., Weiner I. The effects of pre- and postweaning rearing conditions on latent inhibition and partial reinforcement extinction effect in male rats. Behav. Neural. Biol. 53:1990;189-204.
17. Fride E., Dan Y., Feldon J., Halevy G., Weinstock M. Effects of prenatal stress on vulnerability to stress in prepubertal and adult rats. Physiol. Behav. 37:1986;681-687.
18. Fride E., Dan Y., Gavish M., Weinstock M. Prenatal stress impairs maternal behavior in a conflict situation and reduces hippocampal benzodiazepine receptors. Life Sci. 36:1985;2103-2109.
19. Geyer M.A., Wilkinson L.S., Humby T., Robbins T.W. Isolation rearing of rat produces a deficit in prepulse inhibition of acoustic startle similar to that in schizophrenia. Biol. Psychiatry. 34:1993;361-372.
20. Gray J.A., Joseph M.H., Hemsley D.R., Young A.M.J., Warburton E.C., Boulenguez P. et al. The role of mesolimbic dopaminergic and retrohippocampal afferents to the nucleus accumbens in latent inhibition: implications for schizophrenia. Behav. Brain. Res. 71(1-2):1995;19-31.
21. Gray J.A., Moran P.M., Grigoryan G., Peters S.L., Young A.M.J., Joseph M.H. Latent inhibition: the nucleus accumbens connection revisited. Behav. Brain. Res. 88:1997;27-34.
22. Hall F.S. Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Crit. Rev. Neurobiol. 12(1-2):1998;129-162.
23. Henry C., Guegant G., Arbauld E., Arsaut J., Le Moal M., Demotes-Mainard J. Prenatal stress in rats facilitates amphetamine-induced sensitization and induces long-lasting changes in dopamine receptors in the nucleus accumbens. Brain Res. 685(1-2):1995;179-186.
24. Hilakivi-Clarke L.A., Turkka J., Lister R.G., Linnoila M. Effects of early postnatal handling on brain β-adrenoceptors and behavior in tests related to stress. Brain Res. 542:1991;286-292.
25. Hockman C.H. Prenatal maternal stress in the rat: its effects on emotional behavior in the offspring. J. Comp. Physiol. Psychol. 54(6):1961;679-684.
26. von Hoersten S., Dimitrijevic M., Macrovic B.M., Jankovic B.D. Effect of early experience on behavior and immune response in the rat. Physiol. Behav. 54:1993;931-940.
27. Kaneko W.M., Riley E.P., Ehlers C.L. Behavioral and electrophysiological effects of early repeated maternal separation. Depression. 2:1994;43-53.
28. Koch M., Schnitzler H.U. The acoustic startle response in rats - circuits mediating evocation, inhibition and potentiation. Behav. Brain Res. 89(1-2):1997;35-49.
29. Lehmann J, Pryce CR, Bettschen D, Feldon J. The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacol Biochem Behav (in press).
30. Lehmann J, Pryce CR, Feldon J. Lack of effect of an early stressful life event on sensorimotor gating in adult rats. Schizophr Res (in press).
31. Lehmann J., Stöhr T., Schuller J., Domeney A., Heidbreder C., Feldon J. Long-term effects of maternal separation on three different latent inhibition paradigms. Pharmacol. Biochem. Behav. 59(4):1998;873-882.
32. Levine S., Huchton D.M., Wiener S.G., Rosenfeld P. Time course of the effect of maternal deprivation on the hypothalamic-pituitary-adrenal axis of the infant rat. Dev. Psychobiol. 24(8):1992;547-558.
33. Lubow R.E. Latent Inhibition and Conditioned Attention Theory. 1989;Cambridge University Press, Cambridge.
34. Lubow R.E., Weiner I., Feldon J. An animal model of attention. Spiegelstein M.Y., Levy A. Behavioral Models and the Analysis of Drug Action. 1982;89-107 Elsevier, Amsterdam.
35. Matthews K., Robbins T., Everitt B.J., Caine S.B. Repeated neonatal maternal separation alters intravenous cocaine self-administration in adult rats. Psychopharmacology. 141:1999;123-134.
36. Matthews K., Wilkinson L.S., Robbins T.W. Repeated maternal separation of preweanling rats attenuates behavioral responses to primary and conditioned incentives in adulthood. Physiol. Behav. 59(1):1996;99-107.
37. McIntosh J., Anisman H., Merali Z. Short- and long-periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: gender-dependent effects. Dev. Brain Res. 113:1999;97-106.
38. 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. 18:1996;49-72.
39. Meisel R.L., Dohanich G.P., Ward I.L. Effects of prenatal stress on avoidance acquisition, open field performance and lordotic behavior in male rats. Physiol. Behav. 22:1979;527-530.
40. Nishikouri Y. Effect of prenatal administration of diazepam and buspirone on brain monoamines and avoidance learning behavior in offspring rats in relation to the influence of maternal stress caused by subcutaneous injection. Nihon Shinkei Seishin Yakurigaku Zasshi. 15(1):1995;61-69.
41. Ogawa T., Mikuni M., Kuroda Y., Muneoka K., Mori K.J., Takahashi K. Periodic maternal deprivation alters stress response in adult offspring: potentiates the negative feedback regulation of restraint stress-induced adrenocortical response and reduces the frequencies of open field-induced behaviors. Pharmacol. Biochem. Behav. 49(4):1994;961-967.
42. Peters S.L., Gray J.A., Joseph M.H. Pre-weaning non-handling of rats disrupts latent inhibition in males, and results in persisting sex- and area-dependent increases in dopamine and serotonin turnover. Behav. Pharmacol. 2:1991;215-223.
43. Pfister H.P., Muir J.L. Prenatal exposure to predictable and unpredictable novelty stress and oxytocin treatment affects offspring development and behavior in rats. Int. J. Neurosci. 62:1992;227-241.
44. Plotyrev T., Keshet G.I., Kay G., Weinstock M. Role of experimental conditions in determining differences in exploratory behavior of prenatally stressed rats. Dev. Psychobiol. 29(5):1996;453-462.
45. Rots N.Y., De Jong J., Workel J.O., Levine S., Cools A.R., De Kloet E.R. Neonatal maternally deprived rats have as adult elevated basal pituitary-adrenal activity and enhanced susceptibility to apomorphine. J. Neuroendocrinol. 8:1996;501-506.
46. Secoli S.R., Teixeira N.A. Chronic prenatal stress affects development and behavioral depression in rats. Stress. 2(4):1998;273-280.
47. Smith B.L., Wills G., Naylor D. The effect of prenatal stress on rat offsprings' learning ability. J. Psychol. 107:1981;45-51.
48. Smith D.J., Joffe J.M., Heseltine G.F. Modification of prenatal stress effects in rats by adrenalectomy, dexamethasone and chlorpromazine. Physiol. Behav. 15(5):1975;461-469.
49. Smythe J.W., McCormick C.M., Meaney M.J. Median eminence corticotrophin-releasing hormone content following prenatal stress and neonatal handling. Brain Res. Bull. 40(3):1996;195-199.
50. Smythe J.W., McCormick C.M., Rochford J., Meaney M.J. The interaction between prenatal stress and neonatal handling on nociceptive response latencies in male and female rats. Physiol. Behav. 55(5):1994;971-974.
51. Spear L.P., File S.E. Methodological considerations in neurobehavioral teratology. Pharmacol. Biochem. Behav. 55(4):1996;455-457.
52. Stanton M.E., Guitierrez Y.R., Levine S. Maternal deprivation potentiates pituitary-adrenal stress responses in infant rats. Behav. Neurosci. 102(5):1988;692-700.
53. Suchecki D., Tufik S. Long-term effects of maternal deprivation on the corticosterone response to stress in rats. Am. J. Physiol. 273:1997;R1332-R1338.
54. Swerdlow N.R., Geyer M.A. Using an animal model of deficient sensorimotor gating to study the pathophysiology and new treatments of schizophrenia. Schizophr. Bull. 24(2):1998;285-301.
55. Swerdlow N.R., Braff D.L., Taaid N., Geyer M.A. Assessing the validity of an animal model of deficient sensorimotor gating in schizophrenic patients. Arch. Gen. Psychiatry. 51:1994;139-154.
56. Swerdlow N.R., Caine S.B., Braff D.L., Geyer M.A. The neural substrates of sensorimotor gating of the startle reflex: a review of recent findings and their implications. J. Psychopharmacol. 6(2):1992;176-190.
57. Szuran T. Prenatal Stress in the Rat: Influence on the Behavior and Endocrine Regulation of the Offspring. Doctoral Dissertation No. 12366. Zurich, Switzerland: Swiss Federal Institute of Technology, 1997.
58. Vallée M., Mayo W., Dellu F., Le Moal M., Simon H., Maccari S. Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J. Neurosci. 17(7):1997;2626-2636.
59. Vallée M., Mayo W., Maccari S., Le Moal M., Simon H. Long-term effects of prenatal stress and handling on metabolic parameters: relationship to corticosterone secretion response. Brain Res. 712:1996;287-292.
60. Van Oers H.J.J., De Kloet E.R., Levine S. Early versus late maternal deprivation differentially alters the endocrine and hypothalamic response to stress. Dev. Brain Res. 111:1998;245-252.
61. Varty G.B., Higgins G.A. Examination of drug-induced and isolation-induced disruptions of prepulse inhibition as models to screen antipsychotic drugs. Psychopharmacology. 122:1995;15-26.
62. Wakshlak A., Weinstock M. Neonatal handling reverses behavioral abnormalities induced in rats by prenatal stress. Physiol. Behav. 48:1990;289-292.
63. Walker C.-D., Perrin M., Vale W., Rivier C. Ontogeny of the stress response in the rat: role of the pituitary and the hypothalamus. Endocrinology. 118(4):1986;1445-1451.
64. Ward I.L. The prenatal stress syndrome: current status. Psychoneuroendocrinology. 9(1):1984;3-11.
65. Weiner I., Feldon J. The switching model of latent inhibition: an update of neural substrates. Behav. Brain Res. 88(1):1997;11-25.
66. Weiner I., Schnabel I., Lubow R.E., Feldon J. The effect of early handling on latent inhibition in male and female rats. Dev. Psychobiol. 18:1985;291-297.
67. Weinstock M. Does prenatal stress impair coping and regulation of hypothalamic-pituitary-adrenal axis? Neurosci. Biobehav. Rev. 21(1):1997;1-10.
68. Weinstock M., Matlina E., Maor G.I., Rosen H., McEwen B.S. Prenatal stress selectively alters the reactivity of the hypothalamic-pituitary adrenal system in the female rat. Brain Res. 595:1992;195-200.
69. Wigger A., Neumann I. Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol. Behav. 66(2):1999;293-302.
70. Wilkinson L.S., Killcross S.S., Humby T., Hall F.S., Geyer M.A., Robbins T.W. Social isolation in the rat produces developmentally specific deficits in prepulse inhibition of the acoustic startle response without disrupting latent inhibition. Neuropsychopharmacology. 10:1994;61-72.
71. Zimmerberg B., Brown R.C. Prenatal experience and postnatal stress modulate the adult neurosteroid and catecholaminergic stress response. Int. J. Neurosci. 16(3-4):1998;217-228.
72. Zimmerberg B., Shartrand A.M. Temperature dependent effects of maternal separation on growth, activity, and amphetamine sensitivity in rats. Dev. Psychobiol. 25(3):1992;213-226.