Gender-related qualitative differences in baseline and post-stress anxiety responses are not reflected in the incidence of criterion-based PTSD-like behaviour patterns

World Journal of Biological Psychiatry

Volumn 10, Issue 4 PART 3, 2009, Pages 856-869

  Mazor, Adi ^a   Matar, Michael A ^a   Kaplan, Zeev ^a   Kozlovsky, Nitsan ^a   Zohar, Joseph ^b   Cohen, Hagit ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

Animal model; Estrous cycle; Extreme behavioural response; Gender; Posttraumatic stress disorder

Indexed keywords

CORTICOSTERONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; AUDITORY STIMULATION; BEHAVIORAL RESEARCH; CONTROLLED STUDY; ESTRUS CYCLE; EXPOSURE; FEMALE; INCIDENCE; LEARNING; MALE; NONHUMAN; POPULATION RESEARCH; POSTTRAUMATIC STRESS DISORDER; PREVALENCE; QUALITATIVE ANALYSIS; RAT; SEX DIFFERENCE; SPATIAL MEMORY; STARTLE REFLEX; STRESS; ANIMAL; ANIMAL BEHAVIOR; ANXIETY DISORDER; BLOOD; DISEASE MODEL; EVALUATION; MAJOR DEPRESSION; MAZE TEST; PSYCHOLOGICAL ASPECT; RANDOMIZATION; SOCIAL BEHAVIOR; SPRAGUE DAWLEY RAT;

ANIMALS; ANXIETY DISORDERS; BEHAVIOR, ANIMAL; CORTICOSTERONE; DEPRESSIVE DISORDER, MAJOR; DISEASE MODELS, ANIMAL; ESTROUS CYCLE; FEMALE; INCIDENCE; MALE; MAZE LEARNING; PREVALENCE; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; SEX FACTORS; SOCIAL BEHAVIOR; STARTLE REACTION; STRESS DISORDERS, POST-TRAUMATIC;

EID: 77949527334     PISSN: 15622975     EISSN: 18141412     Source Type: Journal    
DOI: 10.1080/15622970701561383     Document Type: Article

References (62)

1. Adamec R. 1997. Transmitter systems involved in neural plasticity underlying increased anxiety and defence-implications for understanding anxiety following traumatic stress. Neurosci Biobehav Rev 21:755-765.
2. Adamec RE, Shallow T. 1993. Lasting effects on rodent anxiety of a single exposure to a cat. Physiol Behav 54:101-109.
3. Adamec RE, Shallow T, Budgell J. 1997. 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 111:435-449.
4. Adamec R, Kent P, Anisman H, Shallow T, Merali. 1998. Neural plasticity, neuropeptides and anxiety in animals-implications for understanding and treating affective disorder following traumatic stress in humans. Neurosci Biobehav Rev 23:301-318.
5. Adamec RE, Burton P, Shallow T, Budgell J. 1999. NMDA receptors mediate lasting increases in anxiety-like behavior produced by the stress of predator exposure-implications for anxiety associated with posttraumatic stress disorder. Physiol Behav 65:723-737.
6. Adamec RE, Blundell J, Burton P. 2003. Phosphorylated cyclic AMP response element binding protein expression induced in the periaqueductal gray by predator stress: its relationship to the stress experience, behavior and limbic neural plasticity. Prog Neuropsychopharmacol Biol Psychiatry 27:1243-1267.
7. Adamec R, Head D, Blundell J, Burton P, Berton O. 2006. Lasting anxiogenic effects of feline predator stress in mice: Sex differences in vulnerability to stress and predicting severity of anxiogenic response from the stress experience. Physiol Behav 88:12-29.
8. Blanchard RJ, Blanchard DC, Rodgers J, Weiss SM. 1990a. The characterization and modelling of antipredator defensive behavior. Neurosci Biobehav Rev 14:463-472
9. Blanchard RJ, Blanchard DC, Weiss SM, Meyer S. 1990b. The effects of ethanol and diazepam on reactions to predatory odors. Pharmacol Biochem Behav 35:775-780.
10. Blanchard RJ, Shepherd JK, Rodgers RJ, Magee L, Blanchard DC. 1993. Attenuation of antipredator defensive behavior in rats following chronic treatment with imipramine. Psychophar-macology 110:245-253.
11. Blanchard RJ, Nikulina JN, Sakai RR, McKittrick C, McEwen B, Blanchard DC. 1998. Behavioural and endocrine change following chronic predatory stress. Physiol Behav 63:561-569.
12. Blanchard RJ, Yang M, Li CI, Gervacio A, Blanchard DC. 2001. Cue and context conditioning of defensive behaviors to cat odor stimuli. Neurosci Biobehav Rev 25:587-595.
13. Bowman RE, Zrull MC, Luine VN. 2001. Chronic restraint stress enhances radial arm maze performance in female rats. Brain Res 904:279-289
14. Breslau N, Chilcoat HD, Kessler RC, Peterson EL, Lucia VC. 1999. Vulnerability to assaultive violence: further specification of the sex difference in post-traumatic stress disorder. Psychol Med 29:813-821.
15. Brewin CR, Andrews B, Valentine JD. 2000. Meta-analysis of risk factors for posttraumatic stress disorder in trauma-exposed adults. J Consult Clin Psychol 68:748-766.
16. Bridges NJ, Starkey NJ. 2004. Sex differences in Mongolian gerbils in four tests of anxiety. Physiol Behav 83:119-127.
17. Chadda R, Devaud LL. 2004. Sex differences in effects of mild chronic stress on seizure risk and GABAA receptors in rats. Pharmacol Biochem Behav 78:495-504.
18. Chadda R, Devaud LL. 2005. Differential effects of mild repeated restraint stress on behaviors and GABA(A) receptors in male and female rats. Pharmacol Biochem Behav 81:854-863.
19. Cohen H, Zohar J. 2004. Animal models of post traumatic stress disorder: The use of cut off behavioral criteria. Ann NY Acad Sci 1032:167-178.
20. Cohen H, Friedberg S, Michael M, Kotler M, Zeev K. 1996. Interaction of CCK-4 induced anxiety and post-cat exposure anxiety in rats. Depress Anxiety 4:144-145.
21. Cohen H, Kaplan Z, Kotler M. 1999. CCK-antagonists in a rat exposed to acute stress: implication for anxiety associated with post-traumatic stress disorder. Depress Anxiety 10:8-17.
22. Cohen H, Benjamin J, Kaplan Z, Kotler M. 2000. Administration of high-dose ketoconazole, an inhibitor of steroid synthesis, prevents posttraumatic anxiety in an animal model. Eur Neuropsychopharmacol 10:429-435
23. Cohen H, Joseph Z, Matar M. 2003. The relevance of differential response to trauma in an animal model of post-traumatic stress disorder. Biol Psychiatry 53:463-473
24. Cohen H, Zohar J, Matar MA, Zeev K, Loewenthal U, Richter-Levin G. 2004. Setting apart the affected: the use of behavioral criteria in animal models of post traumatic stress disorder. Neuropsychopharmacology 29:1962-1970.
25. Cohen H, Zohar J, Matar MA, Kaplan Z, Geva AB. 2005. Unsupervised fuzzy clustering analysis supports behavioral cutoff criteria in an animal model of posttraumatic stress disorder. Biol Psychiatry 58:640-650.
26. Cohen H, Kaplan Z, Matar A, Loewenthal U, Kozlovsky N, Zohar J. 2006a. Anisomycin, a protein synthesis inhibitor, disrupts traumatic memory consolidation and attenuates post traumatic stress response in rats. Biol Psychiatry 60:767-776.
27. Cohen H, Ziv Y, Cardon M, et al. 2006b. Maladaptation to mental stress mitigated by the adaptive immune system via depletion of naturally occurring regulatory CD4 + CD25 + cells. J Neurobiol 66:552-563.
28. Cohen H, Zohar J, Gidron Y, et al. 2006c. Blunted HPA axis response to stress influences susceptibility to posttraumatic stress response in rats. Biol Psychiatry 59:1208-1218.
29. Cohen H, Maayan R, Touati-Werner D. 2007. Decreased circulatory levels of neuroactive steroids in behaviorally more extremely affected rats subsequent to exposure to a potentially traumatic experience. Int J Neuropsychopharmacol 10:203-209.
30. Dalla C, Antoniou K, Drossopoulou G, et al. 2005. Chronic mild stress impact: are females more vulnerable? Neuroscience 135:703-714.
31. Diaz-Veliz G, Alarcon T, Espinoza C, Dussaubat N, Mora S. 1997. Ketanserin and anxiety levels: influence of gender, estrous cycle, ovariectomy and ovarian hormones in female rats. Pharmacol Biochem Behav 58:637-642.
32. Drossopoulou G, Antoniou K, Kitraki E, et al. 2004. Sex differences in behavioral, neurochemical and neuroendocrine effects induced by the forced swim test in rats. Neuroscience 126:849-857.
33. Evans HM, Long JA. 1922. Characteristic effects upon growth, oestrus and ovulation induced by the intraperitoneal administration of fresh anterior hypophyseal substance. Proc Natl Acad Sci USA 8:38-39.
34. Freedman SA, Gluck N, Tuval-Mashiach R, Brandes D, Peri T, Shalev AY. 2002. Gender differences in responses to traumatic events: a prospective study. J Trauma Stress 15:407-413
35. Gerrits M, Grootkarijn A, Bekkering BF, Bruinsma M, Den Boer JA, Ter Horst GJ. 2005. Cyclic estradiol replacement attenuates stress-induced c-Fos expression in the PVN of ovariecto-mized rats. Brain Res Bull 67:147-155.
36. Griebel G, Blanchard DC, Jung A, Blanchard RJ. 1995. A model of 'antipredator' defense in Swiss-Webster mice: effects of benzodiazepine receptor ligands with different intrinsic activities. Behav Pharmacol 6:732-745.
37. Griebel G, Blanchard DC, Blanchard RJ. 1996. Predator-elicited flight responses in Swiss-Webster mice: an experimental model of panic attacks. Prog Neuropsychopharmacol Biol Psychiatry 20:185-205.
38. Gulinello M, Lebesgue D, Jover-Mengual T, Zukin RS, Etgen AM. 2006. Acute and chronic estradiol treatments reduce memory deficits induced by transient global ischemia in female rats. Horm Behav 49:246-260.
39. Hiroi R, Neumaier JF. 2006. Differential effects of ovarian steroids on anxiety versus fear as measured by open field test and fear-potentiated startle. Behav Brain Res 166:93-100.
40. Kim JJ, Yoon KS. 1998. Stress: metaplastic effects in the hippocampus. Trends Neurosci 21:505-509.
41. Kitraki E, Kremmyda O, Youlatos D, Alexis MN, Kittas C. 2004. Gender-dependent alterations in corticosteroid receptor status and spatial performance following 21 days of restraint stress. Neuroscience 125:47-55. (Pubitemid 38402158)
42. Luine V, Villegas M, Martinez C, McEwen BS. 1994. Repeated stress causes reversible impairments of spatial memory performance. Brain Res 639:167-170.
43. Marcondes FK, Miguel KJ, Melo LL, Spadari-Bratfisch RC. 2001. Estrous cycle influences the response of female rats in the elevated plus-maze test. Physiol Behav 74:435-440.
44. McEwen BS. 2002. The neurobiology and neuroendocrinology of stress. Implications for post-traumatic stress disorder from a basic science perspective. Psychiatr Clin North Am 25:469-494.
45. Morris R. 1984. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11:47-60.
46. Mueller BR, Bale TL. 2007. Early prenatal stress impact on coping strategies and learning performance is sex dependent. Physiol Behav 91:55-65.
47. Nomikos GG, Spyraki C. 1988. Influence of oestrogen on spontaneous and diazepam-induced exploration of rats in an elevated plus maze. Neuropharmacology 27:691-696.
48. Olff M, Langeland W, Draijer N, Gersons BP. 2007. Gender differences in posttraumatic stress disorder. Psychol Bull 133:183-204.
49. Pavlides C, Watanabe Y, McEwen BS. 1993. Effects of glucocorticoids on hippocampal long-term potentiation. Hippocampus 3:183-192.
50. Perrot-Sinal TS, Gregus A, Boudreau D, Kalynchuk LE. 2004. Sex and repeated restraint stress interact to affect cat odor-induced defensive behavior in adult rats. Brain Res 1027:161-172.
51. Plappert CF, Rodenbucher AM, Pilz PK. 2005. Effects of sex and estrous cycle on modulation of the acoustic startle response in mice. Physiol Behav 84:585-594.
52. Robin RW, Chester B, Rasmussen JK, Jaranson JM, Goldman D. 1997. Prevalence and characteristics of trauma and posttraumatic stress disorder in a southwestern American Indian community. Am J Psychiatry 154:1582-1588.
53. Sapolsky RM. 1996. Why stress is bad for your brain. Science 273:749-750.
54. Sapolsky RM. 2000. Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry 57:925-935.
55. Sapolsky RM, Uno H, Rebert CS, Finch CE. 1990. Hippocampal damage associated with prolonged glucocorticoid exposure in primates. J Neurosci 10:2897-2902.
56. Shepherd JK, Flores T, Rodgers RJ, Blanchard RJ, Blanchard DC. 1992. The anxiety/defense test battery: influence of gender and ritanserin treatment on antipredator defensive behavior. Physiol Behav 51:277-285.
57. Shors TJ, Foy MR, Levine S, Thompson R. 1990. Unpredictable and uncontrollable stress impairs neuronal plasticity in the rat hippocampus. Brain Res Bull 24:663-667.
58. Vedhara K, Hyde J, Gilchrist ID, Tytherleigh M, Plummer S. 2000. Acute stress, memory, attention and cortisol. Psycho-neuroendocrinology 25:5355-5359
59. Walf AA, Frye CA. 2006. A review and update of mechanisms of estrogen in the hippocampus and amygdala for anxiety and depression behavior. Neuropsychopharmacology 31:1097-1111.
60. Watanabe Y, Gould E, McEwen BS. 1992. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 588:341-345.
61. Welberg L, Thrivikraman KV, Plotsky PM. 2006. Combined pre-and postnatal environmental enrichment programs the HPA axis differentially in male and female rats. Psychoneuroendo-crinology 31:553-564.
62. Woolley CS, Gould E, McEwen BS. 1990. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 531:225-231.