Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2007, Article ID 71203, 12 pages
http://dx.doi.org/10.1155/2007/71203
Research Article

Stress before Puberty Exerts a Sex- and Age-Related Impact on Auditory and Contextual Fear Conditioning in the Rat

Brain Mind Institute, Ecole Polytechnique Federale de Lausanne (EPFL), Lausanne 1015, Switzerland

Received 5 January 2007; Revised 27 February 2007; Accepted 4 April 2007

Academic Editor: Robert E. Adamec

Copyright © 2007 Maria Toledo-Rodriguez and Carmen Sandi. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. L. Steinberg, R. Dahl, D. Keating, D. Kupfer, A. Masten, and D. Pine, “The study of developmental psychopathology in adolescence: integrating affective neuroscience with the study of context,” in Handbook of Developmental Psychopathology, D. Cicchetti, Ed., John Wiley & Sons, New York, NY, USA, 2005. View at Google Scholar
  2. K. M. Penza, C. Heim, and C. B. Nemeroff, “Neurobiological effects of childhood abuse: implications for the pathophysiology of depression and anxiety,” Archives of Women's Mental Health, vol. 6, no. 1, pp. 15–22, 2003. View at Publisher · View at Google Scholar
  3. R. C. Kessler, “Epidemiology of women and depression,” Journal of Affective Disorders, vol. 74, no. 1, pp. 5–13, 2003. View at Publisher · View at Google Scholar
  4. D. P. Farrington and R. Loeber, “Epidemiology of juvenile violence,” Child and Adolescent Psychiatric Clinics of North America, vol. 9, no. 4, pp. 733–748, 2000. View at Google Scholar
  5. J. N. Giedd, J. Blumenthal, N. O. Jeffries et al., “Brain development during childhood and adolescence: a longitudinal MRI study,” Nature Neuroscience, vol. 2, no. 10, pp. 861–863, 1999. View at Publisher · View at Google Scholar
  6. E. R. Sowell, P. M. Thompson, C. J. Holmes, T. L. Jernigan, and A. W. Toga, “In vivo evidence for post-adolescent brain maturation in frontal and striatal regions,” Nature Neuroscience, vol. 2, no. 10, pp. 859–861, 1999. View at Publisher · View at Google Scholar
  7. C. Hayward and K. Sanborn, “Puberty and the emergence of gender differences in psychopathology,” Journal of Adolescent Health, vol. 30, no. 4, supplement 1, pp. 49–58, 2002. View at Publisher · View at Google Scholar
  8. R. E. Dahl, “Adolescent brain development: a period of vulnerabilities and opportunities. Keynote address,” Annals of the New York Academy of Sciences, vol. 1021, pp. 1–22, 2004. View at Publisher · View at Google Scholar
  9. O. Agid, Y. Kohn, and B. Lerer, “Environmental stress and psychiatric illness,” Biomedicine and Pharmacotherapy, vol. 54, no. 3, pp. 135–141, 2000. View at Publisher · View at Google Scholar
  10. R. C. Kessler and W. J. Magee, “Childhood adversities and adult depression: basic patterns of association in a US national survey,” Psychological Medicine, vol. 23, no. 3, pp. 679–690, 1993. View at Google Scholar
  11. C. Heim, P. M. Plotsky, and C. B. Nemeroff, “Importance of studying the contributions of early adverse experience to neurobiological findings in depression,” Neuropsychopharmacology, vol. 29, no. 4, pp. 641–648, 2004. View at Publisher · View at Google Scholar
  12. C. M. McCormick and I. Z. Mathews, “HPA function in adolescence: role of sex hormones in its regulation and the enduring consequences of exposure to stressors,” Pharmacology Biochemistry and Behavior, vol. 86, no. 2, pp. 220–233, 2007. View at Publisher · View at Google Scholar
  13. R. Fernández-Fernández, V. M. Navarro, M. L. Barreiro et al., “Effects of chronic hyperghrelinemia on puberty onset and pregnancy outcome in the rat,” Endocrinology, vol. 146, no. 7, pp. 3018–3025, 2005. View at Publisher · View at Google Scholar
  14. M. G. Cunningham, S. Bhattacharyya, and F. M. Benes, “Amygdalo-cortical sprouting continues into early adulthood: implications for the development of normal and abnormal function during adolescence,” Journal of Comparative Neurology, vol. 453, no. 2, pp. 116–130, 2002. View at Publisher · View at Google Scholar
  15. L. P. Spear, “The adolescent brain and age-related behavioral manifestations,” Neuroscience and Biobehavioral Reviews, vol. 24, no. 4, pp. 417–463, 2000. View at Publisher · View at Google Scholar
  16. A. Avital, E. Ram, R. Maayan, A. Weizman, and G. Richter-Levin, “Effects of early-life stress on behavior and neurosteroid levels in the rat hypothalamus and entorhinal cortex,” Brain Research Bulletin, vol. 68, no. 6, pp. 419–424, 2006. View at Publisher · View at Google Scholar
  17. A. Avital and G. Richter-Levin, “Exposure to juvenile stress exacerbates the behavioural consequences of exposure to stress in the adult rat,” The International Journal of Neuropsychopharmacology, vol. 8, no. 2, pp. 163–173, 2005. View at Publisher · View at Google Scholar
  18. M. Tsoory, H. Cohen, and G. Richter-Levin, “Juvenile stress induces a predisposition to either anxiety or depressive-like symptoms following stress in adulthood,” European Neuropsychopharmacology, vol. 17, no. 4, pp. 245–256, 2007. View at Publisher · View at Google Scholar
  19. M. Tsoory and G. Richter-Levin, “Learning under stress in the adult rat is differentially affected by ‘juvenile’ or ‘adolescent’ stress,” The International Journal of Neuropsychopharmacology, vol. 9, no. 6, pp. 713–728, 2006. View at Publisher · View at Google Scholar
  20. L. N. Maslova, V. V. Bulygina, and N. K. Popova, “Immediate and long-lasting effects of chronic stress in the prepubertal age on the startle reflex,” Physiology and Behavior, vol. 75, no. 1-2, pp. 217–225, 2002. View at Publisher · View at Google Scholar
  21. C. M. McCormick, D. Robarts, E. Gleason, and J. E. Kelsey, “Stress during adolescence enhances locomotor sensitization to nicotine in adulthood in female, but not male, rats,” Hormones and Behavior, vol. 46, no. 4, pp. 458–466, 2004. View at Publisher · View at Google Scholar
  22. C. M. McCormick, D. Robarts, K. Kopeikina, and J. E. Kelsey, “Long-lasting, sex- and age-specific effects of social stressors on corticosterone responses to restraint and on locomotor responses to psychostimulants in rats,” Hormones and Behavior, vol. 48, no. 1, pp. 64–74, 2005. View at Publisher · View at Google Scholar
  23. C. Isgor, M. Kabbaj, H. Akil, and S. J. Watson, “Delayed effects of chronic variable stress during peripubertal-juvenile period on hippocampal morphology and on cognitive and stress axis functions in rats,” Hippocampus, vol. 14, no. 5, pp. 636–648, 2004. View at Publisher · View at Google Scholar
  24. J. Sala-Catala, C. Torrero, M. Regalado, M. Salas, and A. Ruiz-Marcos, “Movements restriction and alterations of the number of spines distributed along the apical shafts of layer V pyramids in motor and primary sensory cortices of the peripubertal and adult rat,” Neuroscience, vol. 133, no. 1, pp. 137–145, 2005. View at Publisher · View at Google Scholar
  25. M. Kabbaj, C. Isgor, S. J. Watson, and H. Akil, “Stress during adolescence alters behavioral sensitization to amphetamine,” Neuroscience, vol. 113, no. 2, pp. 395–400, 2002. View at Publisher · View at Google Scholar
  26. G. E. Hodes and T. J. Shors, “Distinctive stress effects on learning during puberty,” Hormones and Behavior, vol. 48, no. 2, pp. 163–171, 2005. View at Publisher · View at Google Scholar
  27. R. E. Bowman, K. D. Beck, and V. N. Luine, “Chronic stress effects on memory: sex differences in performance and monoaminergic activity,” Hormones and Behavior, vol. 43, no. 1, pp. 48–59, 2003. View at Publisher · View at Google Scholar
  28. R. E. Bowman, “Stress-induced changes in spatial memory are sexually differentiated and vary across the lifespan,” Journal of Neuroendocrinology, vol. 17, no. 8, pp. 526–535, 2005. View at Publisher · View at Google Scholar
  29. R. E. Bowman, N. J. Maclusky, S. E. Diaz, M. C. Zrull, and V. N. Luine, “Aged rats: sex differences and responses to chronic stress,” Brain Research, vol. 1126, no. 1, pp. 156–166, 2006. View at Publisher · View at Google Scholar
  30. T. J. Shors, “Stressful experience and learning across the lifespan,” Annual Review of Psychology, vol. 57, pp. 55–85, 2006. View at Publisher · View at Google Scholar
  31. R. L. Roof, “Neonatal exogenous testosterone modifies sex difference in radial arm and Morris water maze performance in prepubescent and adult rats,” Behavioural Brain Research, vol. 53, no. 1-2, pp. 1–10, 1993. View at Publisher · View at Google Scholar
  32. K. D. Beck and V. N. Luine, “Sex differences in behavioral and neurochemical profiles after chronic stress: role of housing conditions,” Physiology and Behavior, vol. 75, no. 5, pp. 661–673, 2002. View at Publisher · View at Google Scholar
  33. C. D. Conrad, K. A. Grote, R. J. Hobbs, and A. Ferayorni, “Sex differences in spatial and non-spatial Y-maze performance after chronic stress,” Neurobiology of Learning and Memory, vol. 79, no. 1, pp. 32–40, 2003. View at Publisher · View at Google Scholar
  34. E. Kitraki, O. Kremmyda, D. Youlatos, M. N. Alexis, and C. Kittas, “Gender-dependent alterations in corticosteroid receptor status and spatial performance following 21 days of restraint stress,” Neuroscience, vol. 125, no. 1, pp. 47–55, 2004. View at Publisher · View at Google Scholar
  35. R. E. Bowman, M. C. Zrull, and V. N. Luine, “Chronic restraint stress enhances radial arm maze performance in female rats,” Brain Research, vol. 904, no. 2, pp. 279–289, 2001. View at Publisher · View at Google Scholar
  36. E. L. Weiss, J. G. Longhurst, and C. M. Mazure, “Childhood sexual abuse as a risk factor for depression in women: psychosocial and neurobiological correlates,” American Journal of Psychiatry, vol. 156, no. 6, pp. 816–828, 1999. View at Google Scholar
  37. S. Maren, “Nuerobiology of Pavlovian fear conditioning,” Annual Review of Neuroscience, vol. 24, pp. 897–931, 2001. View at Publisher · View at Google Scholar
  38. I. C. Weiss, C. R. Pryce, A. L. Jongen-Rêlo, N. I. Nanz-Bahr, and J. Feldon, “Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat,” Behavioural Brain Research, vol. 152, no. 2, pp. 279–295, 2004. View at Publisher · View at Google Scholar
  39. T. A. Kosten, M. J. D. Miserendino, J. C. Bombace, H. J. Lee, and J. J. Kim, “Sex-selective effects of neonatal isolation on fear conditioning and foot shock sensitivity,” Behavioural Brain Research, vol. 157, no. 2, pp. 235–244, 2005. View at Publisher · View at Google Scholar
  40. T. A. Kosten, H. J. Lee, and J. J. Kim, “Early life stress impairs fear conditioning in adult male and female rats,” Brain Research, vol. 1087, no. 1, pp. 142–150, 2006. View at Publisher · View at Google Scholar
  41. J. Lehmann, C. R. Pryce, D. Bettschen, and J. Feldon, “The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats,” Pharmacology Biochemistry and Behavior, vol. 64, no. 4, pp. 705–715, 1999. View at Publisher · View at Google Scholar
  42. V. Luine, C. Martinez, M. Villegas, A. M. Magariños, and B. S. McEwen, “Restraint stress reversibly enhances spatial memory performance,” Physiology and Behavior, vol. 59, no. 1, pp. 27–32, 1996. View at Publisher · View at Google Scholar
  43. V. Luine, M. Villegas, C. Martinez, and B. S. McEwen, “Repeated stress causes reversible impairments of spatial memory performance,” Brain Research, vol. 639, no. 1, pp. 167–170, 1994. View at Publisher · View at Google Scholar
  44. M. I. Cordero, C. Venero, N. D. Kruyt, and C. Sandi, “Prior exposure to a single stress session facilitates subsequent contextual fear conditioning in rats: evidence for a role of corticosterone,” Hormones and Behavior, vol. 44, no. 4, pp. 338–345, 2003. View at Publisher · View at Google Scholar
  45. J. W. Rudy, K. Kuwagama, and C. R. Pugh, “Isolation reduces contextual but not auditory-cue fear conditioning: a role for endogenous opioids,” Behavioral Neuroscience, vol. 113, no. 2, pp. 316–323, 1999. View at Publisher · View at Google Scholar
  46. C. R. Pugh, D. Tremblay, M. Fleshner, and J. W. Rudy, “A selective role for corticosterone in contextual-fear conditioning,” Behavioral Neuroscience, vol. 111, no. 3, pp. 503–511, 1997. View at Publisher · View at Google Scholar
  47. M. Fleshner, C. R. Pugh, D. Tremblay, and J. W. Rudy, “DHEA-S selectively impairs contextual-fear conditioning: support for the antiglucocorticoid hypothesis,” Behavioral Neuroscience, vol. 111, no. 3, pp. 512–517, 1997. View at Publisher · View at Google Scholar
  48. C. R. Pugh, M. Fleshner, and J. W. Rudy, “Type II glucocorticoid receptor antagonists impair contextual but not auditory-cue fear conditioning in juvenile rats,” Neurobiology of Learning and Memory, vol. 67, no. 1, pp. 75–79, 1997. View at Publisher · View at Google Scholar
  49. J. J. Kim and M. S. Fanselow, “Modality-specific retrograde amnesia of fear,” Science, vol. 256, no. 5057, pp. 675–677, 1992. View at Publisher · View at Google Scholar
  50. J. E. LeDoux, “Brain mechanisms of emotion and emotional learning,” Current Opinion in Neurobiology, vol. 2, no. 2, pp. 191–197, 1992. View at Publisher · View at Google Scholar
  51. L. Calandreau, A. Desmedt, L. Decorte, and R. Jaffard, “A different recruitment of the lateral and basolateral amygdala promotes contextual or elemental conditioned association in Pavlovian fear conditioning,” Learning and Memory, vol. 12, no. 4, pp. 383–388, 2005. View at Publisher · View at Google Scholar
  52. S. L. Andersen and M. H. Teicher, “Delayed effects of early stress on hippocampal development,” Neuropsychopharmacology, vol. 29, no. 11, pp. 1988–1993, 2004. View at Publisher · View at Google Scholar
  53. T. R. Insel, L. P. Miller, and R. E. Gelhard, “The ontogeny of excitatory amino acid receptors in rat forebrain—I. N-methyl-D-aspartate and quisqualate receptors,” Neuroscience, vol. 35, no. 1, pp. 31–43, 1990. View at Publisher · View at Google Scholar
  54. J. Shumake, D. Barrett, and F. Gonzalez-Lima, “Behavioral characteristics of rats predisposed to learned helplessness: reduced reward sensitivity, increased novelty seeking, and persistent fear memories,” Behavioural Brain Research, vol. 164, no. 2, pp. 222–230, 2005. View at Publisher · View at Google Scholar
  55. F. A. Henn and E. Edwards, “Animal models in the sutdy of genetic factors in human psychopathology,” in Genetic Studies in Affective Disorders: Overview of Basic Methods, Current Directions and Critical Research Issues, D. F. Papolos and H. M. Lachman, Eds., pp. 177–192, John Wiley & Sons, New York, NY, USA, 1994. View at Google Scholar
  56. J. Shumake, A. Poremba, E. Edwards, and F. Gonzalez-Lima, “Congenital helpless rats as a genetic model for cortex metabolism in depression,” NeuroReport, vol. 11, no. 17, pp. 3793–3798, 2000. View at Publisher · View at Google Scholar
  57. J. Shumake, N. Conejo-Jimenez, H. Gonzalez-Pardo, and F. Gonzalez-Lima, “Brain differences in newborn rats predisposed to helpless and depressive behavior,” Brain Research, vol. 1030, no. 2, pp. 267–276, 2004. View at Publisher · View at Google Scholar
  58. C. G. van Eden, J. M. Kros, and H. B. M. Uylings, “The development of the rat prefrontal cortex: its size and development of connections with thalamus, spinal cord and other cortical areas,” in Progress in Brain Research, the Prefrontal Cortex: Its Structure, Function and Pathology, H. B. M. Uylings, C. G. van Eden, J. P. C. de Bruin, M. A. Corner, and M. G. P. Feenstra, Eds., pp. 169–183, Elsevier, Amsterdam, The Netherlands, 1990. View at Google Scholar
  59. N. B. Farber, D. F. Wozniak, M. T. Price et al., “Age-specific neurotoxicity in the rat associated with NMDA receptor blockade: potential relevance to schizophrenia?” Biological Psychiatry, vol. 38, no. 12, pp. 788–796, 1995. View at Publisher · View at Google Scholar
  60. A. Kalsbeek, P. Voorn, R. M. Buijs, C. W. Pool, and H. B. M. Uylings, “Development of the dopaminergic innervation in the prefrontal cortex of the rat,” Journal of Comparative Neurology, vol. 269, no. 1, pp. 58–72, 1988. View at Publisher · View at Google Scholar
  61. C. A. Leslie, M. W. Robertson, A. J. Cutler, and J. P. Bennett Jr., “Postnatal development of D1 dopamine receptors in the medial prefrontal cortex, striatum and nucleus accumbens of normal and neonatal 6-hydroxydopamine treated rats: a quantitative autoradiographic analysis,” Developmental Brain Research, vol. 62, no. 1, pp. 109–114, 1991. View at Publisher · View at Google Scholar
  62. C. L. Coulter, H. K. Happe, and L. C. Murrin, “Postnatal development of the dopamine transporter: a quantitative autoradiographic study,” Developmental Brain Research, vol. 92, no. 2, pp. 172–181, 1996. View at Publisher · View at Google Scholar
  63. E. Gould, N. J. Woolf, and L. L. Butcher, “Postnatal development of cholinergic neurons in the rat: I. Forebrain,” Brain Research Bulletin, vol. 27, no. 6, pp. 767–789, 1991. View at Publisher · View at Google Scholar