Psychoneuroendocrinology
Volume 33, Issue 8 , Pages 1139-1150 , September 2008

Marked dissociation between hypothalamic–pituitary–adrenal activation and long-term behavioral effects in rats exposed to immobilization or cat odor

  • C. Muñoz-Abellán

      Affiliations

    • Institut de Neurociències, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
    • Unitat de Fisiologia Animal (Facultat de Biociències), Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
  • ,
  • R. Andero

      Affiliations

    • Institut de Neurociències, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
    • Unitat de Fisiologia Animal (Facultat de Biociències), Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
  • ,
  • R. Nadal

      Affiliations

    • Institut de Neurociències, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
    • Unitat de Psicobiologia (Facultat de Psicologia), Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
  • ,
  • A. Armario

      Affiliations

    • Institut de Neurociències, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
    • Unitat de Fisiologia Animal (Facultat de Biociències), Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain
    • Corresponding Author InformationCorresponding author. Tel.: +34 93581664; fax: +34 935812390.

Received 29 January 2008 ,Revised 5 June 2008 ,Accepted 5 June 2008.

References 

  1. Adamec R. Transmitter systems involved in neural plasticity underlying increased anxiety and defense–implications for understanding anxiety following traumatic stress. Neurosci. Biobehav. Rev. 1997;21:755–765
  2. Adamec R, Kent P, Anisman H, Shallow T, Merali Z. Neural plasticity, neuropeptides and anxiety in animals—implications for understanding and treating affective disorder following traumatic stress in humans. Neurosci. Biobehav. Rev. 1998;23:301–318
  3. Adamec R, Muir C, Grimes M, Pearcey K. Involvement of noradrenergic and corticoid receptors in the consolidation of the lasting anxiogenic effects of predator stress. Behav. Brain Res. 2007;179:192–207
  4. Adamec RE, Shallow T. Lasting effects on rodent anxiety of a single exposure to a cat. Physiol. Behav. 1993;54:101–109
  5. Adamec RE, Shallow T, Budgell J. Blockade of CCK(B) but not CCK(A) receptors before and after the stress of predator exposure prevents lasting increases in anxiety-like behavior: implications for anxiety associated with posttraumatic stress disorder. Behav. Neurosci. 1997;111:435–449
  6. Armario A. The hypothalamic–pituitary–adrenal axis: what can it tell us about stressors?. CNS Neurol. Disord. Drug Targets. 2006;5:485–501
  7. Armario A, Jolin T. Influence of intensity and duration of exposure to various stressors on serum TSH and GH levels in adult male rats. Life Sci. 1989;44:215–221
  8. Belda X, Márquez C, Armario A. Long-term effects of a single exposure to stress in adult rats on behavior and hypothalamic–pituitary–adrenal responsiveness: comparison of two outbred rat strains. Behav. Brain Res. 2004;154:399–408
  9. Bialik RJ, Smythe JW, Roberts DC. Alpha 2-adrenergic receptors mediate the increase in blood glucose levels induced by epinephrine and brief footshock stress. Prog. Neuropsychopharmacol. Biol. Psychiatry. 1988;12:307–314
  10. Bialik RJ, Smythe JW, Sardelis M, Roberts DC. Adrenal demedullation blocks and brain norepinephrine depletion potentiates the hyperglycemic response to a variety of stressors. Brain. Res. 1989;502:88–98
  11. Blanchard DC, Griebel G, Blanchard RJ. Conditioning and residual emotionality effects of predator stimuli: some reflections on stress and emotion. Prog. Neuropsychopharmacol. Biol. Psychiatry. 2003;27:1177–1185
  12. Blanchard DC, Markham C, Yang M, Hubbard D, Madarang E, Blanchard RJ. Failure to produce conditioning with low-dose trimethylthiazoline or cat feces as unconditioned stimuli. Behav. Neurosci. 2003;117:360–368
  13. Blanchard RJ, Blanchard DC. Antipredator defensive behaviors in a visible burrow system. J. Comp. Psychol. 1989;103:70–82
  14. Blanchard RJ, Blanchard DC, Rodgers J, Weiss SM. The characterization and modelling of antipredator defensive behavior. Neurosci. Biobehav. Rev. 1990;14:463–472
  15. Bruske GR, Vendruscolo LF, Ramos A. Two inbred rat strains contrasting for anxiety-related behaviors show similar levels of defensive responses to cat odor. Behav. Brain. Funct. 2007;3:17
  16. Cohen H, Benjamin J, Kaplan Z, Kotler M. Administration of high-dose ketoconazole, an inhibitor of steroid synthesis, prevents posttraumatic anxiety in an animal model. Eur. Neuropsychopharmacol. 2000;10:429–435
  17. Cohen H, Friedberg S, Michael M, Kotler M, Zeev K. Interaction of CCK-4 induced anxiety and post-cat exposure anxiety in rats. Depress. Anxiety. 1996/1997;4:144–145
  18. Cohen H, Kaplan Z, Kotler M. CCK-antagonists in a rat exposed to acute stress: implication for anxiety associated with post-traumatic stress disorder. Depress. Anxiety. 1999;10:8–17
  19. Cohen H, Zohar J, Gidron Y, Matar MA, Belkind D, Loewenthal U, et al. Blunted HPA axis response to stress influences susceptibility to posttraumatic stress response in rats. Biol. Psychiatry. 2006;59:1208–1218
  20. Cohen H, Zohar J, Matar M. The relevance of differential response to trauma in an animal model of posttraumatic stress disorder. Biol. Psychiatry. 2003;53:463–473
  21. Cohen H, Zohar J, Matar MA, Kaplan Z, Geva AB. Unsupervised fuzzy clustering analysis supports behavioral cutoff criteria in an animal model of posttraumatic stress disorder. Biol. Psychiatry. 2005;58:640–650
  22. Cohen H, Zohar J, Matar MA, Zeev K, Loewenthal U, Richter-Levin G. Setting apart the affected: the use of behavioral criteria in animal models of post traumatic stress disorder. Neuropsychopharmacology. 2004;29:1962–1970
  23. Dal-Zotto S, Martí O, Armario A. Glucocorticoids are involved in the long-term effects of a single immobilization stress on the hypothalamic–pituitary–adrenal axis. Psychoneuro-endocrinology. 2003;28:992–1009
  24. Dal-Zotto S, Martí O, Delgado R, Armario A. Potentiation of glucocorticoid release does not modify the long-term effects of a single exposure to immobilization stress. Psychopharmacology. 2004;177:230–237
  25. Dielenberg RA, Hunt GE, McGregor IS. “When a rat smells a cat”: the distribution of Fos immunoreactivity in rat brain following exposure to a predatory odor. Neuroscience. 2001;104:1085–1097
  26. Dielenberg RA, McGregor IS. Defensive behavior in rats towards predatory odors: a review. Neurosci. Biobehav. Rev. 2001;25:597–609
  27. Figueiredo HF, Bodie BL, Tauchi M, Dolgas CM, Herman JP. Stress integration after acute and chronic predator stress: differential activation of central stress circuitry and sensitization of the hypothalamo-pituitary-adrenocortical axis. Endocrinology. 2003;144:5249–5258
  28. File SE, Zangrossi H, Sanders FL, Mabbutt PS. Dissociation between behavioral and corticosterone responses on repeated exposures to cat odor. Physiol. Behav. 1993;54:1109–1111
  29. File SE, Zangrossi H, Sanders FL, Mabbutt PS. Raised corticosterone in the rat after exposure to the elevated plus-maze. Psychopharmacology. 1994;113:543–546
  30. Fleshner M, Campisi J, Amiri L, Diamond DM. Cat exposure induces both intra- and extracellular Hsp72: the role of adrenal hormones. Psychoneuroendocrinology. 2004;29:1142–1152
  31. Gagliano H, Fuentes S, Nadal R, Armario A. Previous exposure to immobilisation and repeated exposure to a novel environment demonstrate a marked dissociation between behavioral and pituitary–adrenal responses. Behav. Brain Res. 2008;187:239–245
  32. García A, Martí O, Vallès A, Dal-Zotto S, Armario A. Recovery of the hypothalamic–pituitary–adrenal response to stress. Effect of stress intensity, stress duration and previous stress exposure. Neuroendocrinology. 2000;72:114–125
  33. Johnson JD, O’Connor KA, Deak T, Stark M, Watkins LR, Maier SF. Prior stressor exposure sensitizes LPS-induced cytokine production. Brain Behav. Immun. 2002;16:461–476
  34. Kemble ED, Bolwahnn BL. Immediate and long-term effects of novel odors on risk assessment in mice. Physiol. Behav. 1997;61:543–549
  35. Le Mevel JC, Abitbol S, Beraud G, Maniey J. Temporal changes in plasma adrenocorticotropin concentration after repeated neurotropic stress in male and female rats. Endocrinology. 1979;105:812–817
  36. Maier SF. Learned helplessness and animal models of depression. Prog. Neuropsychopharmacol. Biol. Psychiatry. 1984;8:435–446
  37. Maier SF, Ryan SM, Barksdale CM, Kalin NH. Stressor controllability and the pituitary–adrenal system. Behav. Neurosci. 1986;100:669–674
  38. Márquez C, Belda X, Armario A. Post-stress recovery of pituitary–adrenal hormones and glucose, but not the response during exposure to the stressor, is a marker of stress intensity in highly stressful situations. Brain. Res. 2002;926:181–185
  39. Márquez C, Nadal R, Armario A. Responsiveness of the hypothalamic–pituitary–adrenal axis to different novel environments is a consistent individual trait in adult male outbred rats. Psychoneuroendocrinology. 2005;30:179–187
  40. Márquez C, Nadal R, Armario A. Influence of reactivity to novelty and anxiety on hypothalamic–pituitary–adrenal and prolactin responses to two different novel environments in adult male rats. Behav. Brain Res. 2006;168:13–22
  41. Martí O, García A, Vallès A, Harbuz MS, Armario A. Evidence that a single exposure to aversive stimuli triggers long-lasting effects in the hypothalamus–pituitary–adrenal axis that consolidate with time. Eur. J. Neurosci. 2001;13:129–136
  42. Masini CV, Sauer S, Campeau S. Ferret odor as a processive stress model in rats: neurochemical, behavioral, and endocrine evidence. Behav. Neurosci. 2005;119:280–292
  43. Matar MA, Cohen H, Kaplan Z, Zohar J. The effect of early poststressor intervention with sertraline on behavioral responses in an animal model of post-traumatic stress disorder. Neuropsychopharmacology. 2006;31:2610–2618
  44. McCulloch C, Searle S. Generalized, linear and mixed models. New York: Wiley and Sons; 2001;
  45. McGregor IS, Dielenberg RA. Differential anxiolytic efficacy of a benzodiazepine on first versus second exposure to a predatory odor in rats. Psychopharmacology. 1999;147:174–181
  46. McGregor IS, Schrama L, Ambermoon P, Dielenberg RA. Not all ‘predator odours’ are equal: cat odour but not 2,4,5 trimethylthiazoline (TMT; fox odour) elicits specific defensive behaviours in rats. Behav. Brain Res. 2002;129:1–16
  47. Merali Z, Kent P, Michaud D, McIntyre D, Anisman H. Differential impact of predator or immobilization stressors on central corticotropin-releasing hormone and bombesin-like peptides in Fast and Slow seizing rat. Brain Res. 2001;906:60–73
  48. Mesches MH, Fleshner M, Heman KL, Rose GM, Diamond DM. Exposing rats to a predator blocks primed burst potentiation in the hippocampus in vitro. J. Neurosci. 1999;19:RC18
  49. O’Connor KA, Ginsberg AB, Maksimova E, Wieseler Frank JL, Johnson JD, Spencer RL, et al. Stress-induced sensitization of the hypothalamic-pituitary adrenal axis is associated with alterations of hypothalamic and pituitary gene expression. Neuroendocrinology. 2004;80:252–263
  50. O’Connor KA, Johnson JD, Hammack SE, Brooks LM, Spencer RL, Watkins LR, et al. Inescapable shock induces resistance to the effects of dexamethasone. Psychoneuroendocrinology. 2003;28:481–500
  51. Pellow S, File SE. Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol. Biochem. Behav. 1986;24:525–529
  52. Roy V, Belzung C, Delarue C, Chapillon P. Environmental enrichment in BALB/c mice: effects in classical tests of anxiety and exposure to a predatory odor. Physiol. Behav. 2001;74:313–320
  53. Staples LG, McGregor IS. Defensive responses of Wistar and Sprague-Dawley rats to cat odour and TMT. Behav. Brain Res. 2006;172:351–354
  54. Takahashi LK, Nakashima BR, Hong H, Watanabe K. The smell of danger: a behavioral and neural analysis of predator odor-induced fear. Neurosci. Biobehav. Rev. 2005;29:1157–1167
  55. Thomas RM, Urban JH, Peterson DA. Acute exposure to predator odor elicits a robust increase in corticosterone and a decrease in activity without altering proliferation in the adult rat hippocampus. Exp. Neurol. 2006;201:308–315
  56. Van Dijken HH, de Goeij DC, Sutanto W, Mos J, de Kloet ER, Tilders FJ. Short inescapable stress produces long-lasting changes in the brain–pituitary–adrenal axis of adult male rats. Neuroendocrinology. 1993;58:57–64
  57. Van Dijken HH, Mos J, van der Heyden JA, Tilders FJ. Characterization of stress-induced long-term behavioural changes in rats: evidence in favor of anxiety. Physiol. Behav. 1992;52:945–951
  58. Van Dijken HH, Van der Heyden JA, Mos J, Tilders FJ. Inescapable footshocks induce progressive and long-lasting behavioural changes in male rats. Physiol. Behav. 1992;51:787–794
  59. Will MJ, Der-Avakian A, Pepin JL, Durkan BT, Watkins LR, Maier SF. Modulation of the locomotor properties of morphine and amphetamine by uncontrollable stress. Pharmacol. Biochem. Behav. 2002;71:345–351
  60. Will MJ, Watkins LR, Maier SF. Uncontrollable stress potentiates morphine's rewarding properties. Pharmacol. Biochem. Behav. 1998;60:655–664
  61. Woodson JC, Macintosh D, Fleshner M, Diamond DM. Emotion-induced amnesia in rats: working memory-specific impairment, corticosterone-memory correlation, and fear versus arousal effects on memory. Learn. Mem. 2003;10:326–336
  62. Zangrossi H, File SE. Behavioral consequences in animal tests of anxiety and exploration of exposure to cat odor. Brain Res. Bull. 1992;29:381–388

PII: S0306-4530(08)00155-8

doi: 10.1016/j.psyneuen.2008.06.002

Psychoneuroendocrinology
Volume 33, Issue 8 , Pages 1139-1150 , September 2008