Psychoneuroendocrinology
Volume 32, Issue 7 , Pages 765-776 , August 2007

Prenatal stress alters the negative correlation between neuronal activation in limbic regions and behavioral responses in rats exposed to high and low anxiogenic environments

  • Jérôme Mairesse

      Affiliations

    • Neuroscience/Perinatal Stress Team, Univ. Lille 1, 59655 Villeneuve d’Ascq, France
    • These two authors contributed equally to the work.
    • ,
  • Odile Viltart

      Affiliations

    • Neuroscience/Perinatal Stress Team, Univ. Lille 1, 59655 Villeneuve d’Ascq, France
    • These two authors contributed equally to the work.
    • ,
  • Nicolas Salomé

      Affiliations

    • Neuroscience/Perinatal Stress Team, Univ. Lille 1, 59655 Villeneuve d’Ascq, France
    • ,
  • Alessandro Giuliani

      Affiliations

    • Environment and Health Department, Istituto Superiore di Sanita’, Rome, Italy
    • ,
  • Assia Catalani

      Affiliations

    • Department of Human Physiology and Pharmacology, University of Rome La Sapienza, Rome, Italy
    • ,
  • Paola Casolini

      Affiliations

    • Department of Human Physiology and Pharmacology, University of Rome La Sapienza, Rome, Italy
    • ,
  • Sara Morley-Fletcher

      Affiliations

    • Neuroscience/Perinatal Stress Team, Univ. Lille 1, 59655 Villeneuve d’Ascq, France
    • ,
  • Ferdinando Nicoletti

      Affiliations

    • Department of Human Physiology and Pharmacology, University of Rome La Sapienza, Rome, Italy
    • Neuromed (I.R.C.C.S.), Venafro, Italy
    • ,
  • Stefania Maccari

      Affiliations

    • Neuroscience/Perinatal Stress Team, Univ. Lille 1, 59655 Villeneuve d’Ascq, France
    • Sapienza University of Rome, Italy
    • Corresponding Author InformationCorresponding author. Neuroscience/Perinatal Stress Team, University of Lille 1,59655 Villeneuve d’Ascq, France. Tel.: +393331273160; fax: +390649912524.

Received 20 December 2006 ,Revised 25 March 2007 ,Accepted 29 March 2007.

References 

  1. Benigni R, Giuliani A. Quantitative modeling and biology: the multivariate approach. Am. J. Physiol. 1994;266:1697–1704
  2. Carobrez AP, Bertoglio LJ. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci. Biobehav. Rev. 2005;29:1193–1205
  3. Chapman RH, Stern JM. Failure of severe maternal stress or ACTH during pregnancy to affect emotionality of male rat offspring: implications of litter effects for prenatal studies. Dev. Psychobiol. 1979;12:255–267
  4. Dayas CV, Buller KM, Day TA. Neuroendocrine responses to an emotional stressor: evidence for involvement of the medial but not the central amygdala. Eur. J. Neurosci. 1999;11:2312–2322
  5. De Boer SF, Slangen JL, Van der Gugten J. Plasma catecholamine and corticosterone levels during active and passive shock-prod avoidance behavior in rats: effects of chlordiazepoxide. Physiol. Behav. 1990;47:1089–1098
  6. de Kloet ER, Joels M, Holsboer F. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 2005;6:463–475
  7. de Kloet ER, Sibug RM, Helmerhorst FM, Schmidt MV. Stress, genes and the mechanism of programming the brain for later life. Neurosci. Biobehav. Rev. 2005;29:271–281
  8. Ebner K, Rupniak NM, Saria A, Singewald N. Substance P in the medial amygdala: emotional stress-sensitive release and modulation of anxiety-related behavior in rats. Proc. Natl. Acad. Sci. USA. 2004;101:4280–4285
  9. Herman JP, Ostrander MM, Mueller NK, Figueiredo H. Limbic system mechanisms of stress regulation: hypothalamo–pituitary–adrenocortical axis. Prog. Neuro-Psychopharmacol. Biol. Psychiatry. 2005;29:1201–1213
  10. Jinks AL, McGregor IS. Modulation of anxiety-related behaviours following lesions of the prelimbic or infralimbic cortex in the rat. Brain Res. 1997;772:181–190
  11. Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, et al. Coping styles in animals: current status in behavior and stress-physiology. Neurosci. Biobehav. Rev. 1999;23:925–935
  12. Lawley DN, Maxwell AE. Factor analysis as a statistical method. Statist. 1962;12:209–229
  13. LeDoux JE. Emotion, memory and the brain. Sci. Am. 1994;270:50–59
  14. Lemaire V, Koehl M, Le Moal M, Abrous DN. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc. Natl. Acad. Sci. USA. 2000;97:11032–11037
  15. Lemaire V, Lamarque S, Le Moal M, Piazza PV, Abrous DN. Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis. Biol. Psychiatry. 2006;59:786–792
  16. Louvart H, Maccari S, Darnaudery M. Prenatal stress affects behavioral reactivity to an intense stress in adult female rats. Brain Res. 2005;1031:67–73
  17. Maccari S, Piazza PV, Kabbaj M, Barbazanges A, Simon H, Le Moal M. Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J. Neurosci. 1995;15:110–116
  18. Maccari S, Darnaudery M, Morley-Fletcher S, Zuena AR, Cinque C, Van Reeth O. Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci. Biobehav. Rev. 2003;27:119–127
  19. McEwen BS. Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabolism. 2005;54:20–23
  20. McNaughton N, Corr PJ. A two-dimensional neuropsychology of defense: fear/anxiety and defensive distance. Neurosci. Biobehav. Rev. 2004;28:285–305
  21. Morley-Fletcher S, Darnaudery M, Koehl M, Casolini P, Van Reeth O, Maccari S. Prenatal stress in rats predicts immobility behavior in the forced swim test. Effects of a chronic treatment with tianeptine. Brain Res. 2003;989:246–251
  22. Morley-Fletcher S, Darnaudery M, Mocaer E, Froger N, Lanfumey L, Laviola G, et al. Chronic treatment with imipramine reverses immobility behaviour, hippocampal corticosteroid receptors and cortical 5-HT(1A) receptor mRNA in prenatally stressed rats. Neuropharmacology. 2004;47:841–847
  23. Ma S, Morilak DA. Norepinephrine release in medial amygdala facilitates activation of the hypothalamic–pituitary–adrenal axis in response to acute immobilisation stress. J. Neuroendocrinol. 2005;17:22–28
  24. Pace TW, Gaylord R, Topczewski F, Girotti M, Rubin B, Spencer RL. Immediate-early gene induction in hippocampus and cortex as a result of novel experience is not directly related to the stressfulness of that experience. Eur. J. Neurosci. 2005;22:1679–1690
  25. Paxinos, G., Watson, C., 1997. The Rat Brain in Stereotaxic Coordinates, compact third ed. San Diego, CA.
  26. Pellow S, Chopin P, File SE, Briley M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods. 1985;14:149–167
  27. Rimondini R, Agren G, Borjesson S, Sommer W, Heilig M. Persistent behavioral and autonomic supersensitivity to stress following prenatal stress exposure in rats. Behav. Brain. Res. 2003;140:75–80
  28. Salomé N, Viltart O, Darnaudery M, Salchner P, Singewald N, Landgraf R, et al. Reliability of high and low anxiety-related behaviour: influence of laboratory environment and multifactorial analysis. Behav. Brain Res. 2002;136:227–237
  29. Salomé N, Salchner P, Viltart O, Sequeira H, Wigger A, Landgraf R, et al. Neurobiological correlates of high (HAB) versus low anxiety-related behavior (LAB): differential Fos expression in HAB and LAB rats. Biol. Psychiatry. 2004;55:715–723
  30. Salomé N, Landgraf R, Viltart O. Confinement to the open arm of the elevated-plus maze as anxiety paradigm: behavioral validation. Behav. Neurosci. 2006;120:719–723
  31. Sapolsky RM, Krey LC, McEwen BS. Glucocorticoid sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc. Natl. Acad. Sci. USA. 1984;81:6174–6177
  32. Senba E, Ueyama T. Stress-induced expression of immediate early genes in the brain and peripheral organs of the rat. Neurosci. Res. 1997;29:183–207
  33. Sgoifo A, de Boer SF, Haller J, Koolhaas JM. Individual differences in plasma catecholamine and corticosterone stress responses of wild-type rats: relationship with aggression. Physiol. Behav. 1996;60:1403–1437
  34. Shu SY, Ju G, Fan LZ. The glucose oxidase-DABnickel method in peroxidase histochemistry of the nervous system. Neurosci. Lett. 1988;85:169–171
  35. Spencer SJ, Day TA. Role of catecholaminergic inputs to the medial prefrontal cortex in local and subcortical expression of Fos After psychological stress. J. Neurosci. Res. 2004;78:279–288
  36. Stewart DW. The application and misapplication of factor analysis in marketing research. J. Mark. Res. 1981;18:51–62
  37. 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. 1997;17:2626–2636
  38. Van den Hove DL, Blanco CE, Aendekerk B, Desbonnet L, Bruschettini M, Steinbusch HP, et al. Prenatal restraint stress and long-term affective consequences. Dev. Neurosci. 2005;27:313–320
  39. Viltart O, Mairesse J, Darnaudéry M, Louvart H, Vanbesien-Mailliot C, Catalani A, et al. Prenatal stress alters Fos protein expression in hippocampus and locus coeruleus stress-related brain structures. Psychoneuroendocrinology. 2006;31:769–780
  40. Weller A, Glaubman H, Yehuda S, Caspy T, Ben-Uria Y. Acute and repeated gestational stress affect offspring learning and activity in rats. Physiol. Behav. 1988;43:139–143

PII: S0306-4530(07)00079-0

doi: 10.1016/j.psyneuen.2007.03.013

Psychoneuroendocrinology
Volume 32, Issue 7 , Pages 765-776 , August 2007

Article Tools

* Image Usage & Resolution