Sex differences and phase of light cycle modify chronic stress effects on anxiety and depressive-like behavior

Behavioural Brain Research

Volumn 222, Issue 1, 2011, Pages 212-222

  Huynh, Thu N ^a   Krigbaum, Amanda M ^a   Hanna, Jeffery J ^a   Conrad, Cheryl D ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Anxiety; Chronic stress; Depression; Light cycle; Sex differences

Indexed keywords

SUCROSE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; CHRONIC STRESS; CIRCADIAN RHYTHM; CONTROLLED STUDY; DEPRESSION; EXPERIMENTAL TEST; FEMALE; FORCED SWIMMING TEST; IMMOBILIZATION STRESS; LIGHT DARK CYCLE; LOCOMOTION; MALE; MAZE TEST; NEUROPATHOLOGY; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; RAT; RESPONSE TIME; SEX DIFFERENCE; SUCROSE PREFERENCE TEST; TASK PERFORMANCE;

ANIMALS; ANXIETY; BODY WEIGHT; CONDITIONING, OPERANT; DEPRESSION; EXPLORATORY BEHAVIOR; FEMALE; FOOD PREFERENCES; MALE; MAZE LEARNING; PHOTOPERIOD; RATS; SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL; SUCRASE; SWIMMING;

EID: 79954571674     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.03.038     Document Type: Article

References (90)

1. Nestler E.J., Barrot M., DiLeone R.J., Eisch A.J., Gold S.J., Monteggia L.M. Neurobiology of depression. Neuron 2002, 34:13-25.
2. Fava M., Kendler K.S. Major depressive disorder. Neuron 2000, 28:335-341.
3. Piccinelli M., Wilkinson G. Gender differences in depression. Critical review. Br J Psychiatry 2000, 177:486-492.
4. Willner P. Animal models as simulations of depression. Trends Pharmacol Sci 1991, 12:131-136.
5. Cryan J.F., Markou A., Lucki I. Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 2002, 23:238-245.
6. Binder E.B., Nemeroff C.B. The CRF system, stress, depression and anxiety-insights from human genetic studies. Mol Psychiatry 2010, 15:574-588.
7. Katz R.J. Animal model of depression: pharmacological sensitivity of a hedonic deficit. Pharmacol Biochem Behav 1982, 16:965-968.
8. McEwen B.S. Stress and hippocampal plasticity. Annu Rev Neurosci 1999, 22:105-122.
9. Willner P. The validity of animal models of depression. Psychopharmacology 1984, 83:1-16.
10. Katz R.J. Animal models and human depressive disorders. Neurosci Biobehav Rev 1981, 5:231-246.
11. Porsolt R.D., Anton G., Blavet N., Jalfre M. Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 1978, 47:379-391.
12. Muscat R., Papp M., Willner P. Reversal of stress-induced anhedonia by the atypical antidepressants, fluoxetine and maprotiline. Psychopharmacology 1992, 109:433-438.
13. Sampson D., Willner P., Muscat R. Reversal of antidepressant action by dopamine antagonists in an animal model of depression. Psychopharmacology 1991, 104:491-495.
14. Katz R.J., Roth K.A., Carroll B.J. Acute and chronic stress effects on open field activity in the rat: implications for a model of depression. Neurosci Biobehav Rev 1981, 5:247-251.
15. Willner P. Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 2005, 52:90-110.
16. Kompagne H., Bardos G., Szenasi G., Gacsalyi I., Harsing L.G., Levay G. Chronic mild stress generates clear depressive but ambiguous anxiety-like behaviour in rats. Behav Brain Res 2008, 193:311-314.
17. D'Aquila P.S., Brain P., Willner P. Effects of chronic mild stress on performance in behavioural tests relevant to anxiety and depression. Physiol Behav 1994, 56:861-867.
18. Willner P., Towell A., Sampson D., Sophokleous S., Muscat R. Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology 1987, 93:358-364.
19. Konkle A.T., Baker S.L., Kentner A.C., Barbagallo L.S., Merali Z., Bielajew C. Evaluation of the effects of chronic mild stressors on hedonic and physiological responses: sex and strain compared. Brain Res 2003, 992:227-238.
20. Gouirand A.M., Matuszewich L. The effects of chronic unpredictable stress on male rats in the water maze. Physiol Behav 2005, 86:21-31.
21. Adamec R., Walling S., Burton P. Long-lasting, selective, anxiogenic effects of feline predator stress in mice. Physiol Behav 2004, 83:401-410.
22. Mendelson S.D., McEwen B.S. Autoradiographic analyses of the effects of restraint-induced stress on 5-HT1A, 5-HT1C and 5-HT2 receptors in the dorsal hippocampus of male and female rats. Neuroendocrinology 1991, 54:454-461.
23. Gronli J., Murison R., Fiske E., Bjorvatn B., Sorensen E., Portas C.M., et al. Effects of chronic mild stress on sexual behavior, locomotor activity and consumption of sucrose and saccharine solutions. Physiol Behav 2005, 84:571-577.
24. Mineur Y.S., Belzung C., Crusio W.E. Effects of unpredictable chronic mild stress on anxiety and depression-like behavior in mice. Behav Brain Res 2006, 175:43-50.
25. Kalynchuk L.E., Gregus A., Boudreau D., Perrot-Sinal T.S. Corticosterone increases depression-like behavior, with some effects on predator odor-induced defensive behavior, in male and female rats. Behav Neurosci 2004, 118:1365-1377.
26. Rygula R., Abumaria N., Flugge G., Fuchs E., Ruther E., Havemann-Reinecke U. Anhedonia and motivational deficits in rats: impact of chronic social stress. Behav Brain Res 2005, 162:127-134.
27. Ulrich-Lai Y.M., Herman J.P. Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 2009, 10:397-409.
28. Crabbe J.C., Wahlsten D., Dudek B.C. Genetics of mouse behavior: interactions with laboratory environment. Science 1999, 284:1670-1672.
29. Luine V.N., Beck K.D., Bowman R.E., Frankfurt M., Maclusky N.J. Chronic stress and neural function: accounting for sex and age. J Neuroendocrinol 2007, 19:743-751.
30. McLaughlin K.J., Gomez J.L., Baran S.E., Conrad C.D. The effects of chronic stress on hippocampal morphology and function: an evaluation of chronic restraint paradigms. Brain Res 2007, 1161:56-64.
31. Pare W.P. Open field, learned helplessness, conditioned defensive burying, and forced-swim tests in WKY rats. Physiol Behav 1994, 55:433-439.
32. Korte S.M. Corticosteroids in relation to fear, anxiety and psychopathology. Neurosci Biobehav Rev 2001, 25:117-142.
33. Muscat R., Willner P. Suppression of sucrose drinking by chronic mild unpredictable stress: a methodological analysis. Neurosci Biobehav Rev 1992, 16:507-517.
34. Sampson D., Muscat R., Phillips G., Willner P. Decreased reactivity to sweetness following chronic exposure to mild unpredictable stress or acute administration of pimozide. Neurosci Biobehav Rev 1992, 16:519-524.
35. Sobrian S.K., Marr L., Ressman K. Prenatal cocaine and/or nicotine exposure produces depression and anxiety in aging rats. Prog Neuropsychopharmacol Biol Psychiatry 2003, 27:501-518.
36. Dishman R.K., Dunn A.L., Youngstedt S.D., Davis J.M., Burgess M.L., Wilson S.P., et al. Increased open field locomotion and decreased striatal GABAA binding after activity wheel running. Physiol Behav 1996, 60:699-705.
37. Prut L., Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 2003, 463:3-33.
38. Vallee 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.
39. Heisler L.K., Chu H.M., Brennan T.J., Danao J.A., Bajwa P., Parsons L.H., et al. Elevated anxiety and antidepressant-like responses in serotonin 5-HT1A receptor mutant mice. Proc Natl Acad Sci USA 1998, 95:15049-15054.
40. Carobrez A.P., Bertoglio L.J. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev 2005, 29:1193-1205.
41. Pellow S., Chopin P., File S.E., 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.
42. Hogg S. A review of the validity and variability of the elevated plus-maze as an animal model of anxiety. Pharmacol Biochem Behav 1996, 54:21-30.
43. Hoffman A.N., Armstrong C.E., Hanna J.J., Conrad C.D. Chronic stress, cyclic 17β-estradiol, and daily handling influences on fear conditioning in the female rat. Neurobiol Learn Mem 2010, 94:422-433.
44. Bohacek J., Daniel J.M. Increased daily handling of ovariectomized rats enhances performance on a radial-maze task and obscures effects of estradiol replacement. Horm Behav 2007, 52:237-243.
45. Dobrakovova M., Kvetnansky R., Oprsalova Z., Jezova D. Specificity of the effect of repeated handling on sympathetic-adrenomedullary and pituitary-adrenocortical activity in rats. Psychoneuroendocrinology 1993, 18:163-174.
46. Osborn J.A., Kim C.K., Yu W., Herbert L., Weinberg J. Fetal ethanol exposure alters pituitary-adrenal sensitivity to dexamethasone suppression. Psychoneuroendocrinology 1996, 21:127-143.
47. Barrett A.M., Stockham M.A. The effect of housing conditions and simple experimental procedures upon the corticosterone level in the plasma of rats. J Endocrinol 1963, 26:97-105.
48. Crawley J.N. Exploratory behavior models of anxiety in mice. Neurosci Biobehav Rev 1985, 9:37-44.
49. Conrad C.D., Grote K.A., Hobbs R.J., Ferayorni A. Sex differences in spatial and non-spatial Y-maze performance after chronic stress. Neurobiol Learn Mem 2003, 79:32-40.
50. Magarinos A.M., McEwen B.S. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 1995, 69:89-98.
51. Sapolsky R.M. The possibility of neurotoxicity in the hippocampus in major depression: a primer on neuron death. Biol Psychiatry 2000, 48:755-765.
52. Conrad C.D. Chronic stress-induced hippocampal vulnerability: the glucocorticoid vulnerability hypothesis. Rev Neurosci 2008, 19:395-411.
53. Conrad C.D., Magariños A.M., LeDoux J.E., McEwen B.S. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav Neurosci 1999, 113:902-913.
54. Sousa N., Lukoyanov N.V., Madeira M.D., Almeida O.F., Paula-Barbosa M.M. Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 2000, 97:253-266.
55. Sheline Y.I., Gado M.H., Kraemer H.C. Untreated depression and hippocampal volume loss. Am J Psychiatry 2003, 160:1516-1518.
56. Sapolsky R.M. Stress and plasticity in the limbic system. Neurochem Res 2003, 28:1735-1742.
57. Karlson P., Luscher M. Pheromones: a new term for a class of biologically active substances. Nature 1959, 183:55-56.
58. Wysocki C.J. Neurobehavioral evidence for the involvement of the vomeronasal system in mammalian reproduction. Neurosci Biobehav Rev 1979, 3:301-341.
59. Bouwknecht J.A., Spiga F., Staub D.R., Hale M.W., Shekhar A., Lowry C.A. Differential effects of exposure to low-light or high-light open-field on anxiety-related behaviors: relationship to c-Fos expression in serotonergic and non-serotonergic neurons in the dorsal raphe nucleus. Brain Res Bull 2007, 72:32-43.
60. Hale M.W., Bouwknecht J.A., Spiga F., Shekhar A., Lowry C.A. Exposure to high- and low-light conditions in an open-field test of anxiety increases c-Fos expression in specific subdivisions of the rat basolateral amygdaloid complex. Brain Res Bull 2006, 71:174-182.
61. Hall C.S. Emotional behavior in the rat. I. Defecation and urination as measures of individual differences in emotionality. J Comp Psychol 1934, 18:385-403.
62. Cohen H., Geva A.B., Matar M.A., Zohar J., Kaplan Z. Post-traumatic stress behavioural responses in inbred mouse strains: can genetic predisposition explain phenotypic vulnerability?. Int J Neuropsychopharmacol 2008, 11:331-349.
63. Cohen H., Matar M.A., Buskila D., Kaplan Z., Zohar J. Early post-stressor intervention with high-dose corticosterone attenuates posttraumatic stress response in an animal model of posttraumatic stress disorder. Biol Psychiatry 2008, 64:708-717.
64. Mazor A., Matar M.A., Kaplan Z., Kozlovsky N., Zohar J., Cohen H. 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 J Biol Psychiatry 2009, 10:856-869.
65. Detke M.J., Rickels M., Lucki I. Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology 1995, 121:66-72.
66. Piras G., Giorgi O., Corda M.G. Effects of antidepressants on the performance in the forced swim test of two psychogenetically selected lines of rats that differ in coping strategies to aversive conditions. Psychopharmacology 2010, 211:403-414.
67. Brown T.S., Murphy H.M. Factors affecting sucrose preference behavior in rats with hippocampal lesions. Physiol Behav 1973, 11:833-844.
68. Blizard D.A., Lippman H.R., Chen J.J. Sex differences in open-field behavior in the rat: the inductive and activational role of gonadal hormones. Physiol Behav 1975, 14:601-608.
69. Beatty W.W., Fessler R.G. Ontogeny of sex differences in open-field behavior and sensitivity to electric shock in the rat. Physiol Behav 1976, 16:413-417.
70. Archer J. Rodent sex differences in emotional and related behavior. Behav Biol 1975, 14:451-479.
71. Johnston A.L., File S.E. Sex differences in animal tests of anxiety. Physiol Behav 1991, 49:245-250.
72. Schweizer M.C., Henniger M.S., Sillaber I. Chronic mild stress (CMS) in mice: of anhedonia, 'anomalous anxiolysis' and activity. PLoS ONE 2009, 4:e4326.
73. Fonken L.K., Finy M.S., Walton J.C., Weil Z.M., Workman J.L., Ross J., et al. Influence of light at night on murine anxiety- and depressive-like responses. Behav Brain Res 2009, 205:349-354.
74. Roybal K., Theobold D., Graham A., DiNieri J.A., Russo S.J., Krishnan V., et al. Mania-like behavior induced by disruption of CLOCK. Proc Natl Acad Sci USA 2007, 104:6406-6411.
75. Gorka Z., Moryl E., Papp M. Effect of chronic mild stress on circadian rhythms in the locomotor activity in rats. Pharmacol Biochem Behav 1996, 54:229-234.
76. Conrad C.D. A critical review of chronic stress effects on spatial learning and memory. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:742-755.
77. Wright R.L., Lightner E.N., Harman J.S., Meijer O.C., Conrad C.D. Attenuating corticosterone levels on the day of memory assessment prevents chronic stress-induced impairments in spatial memory. Eur J Neurosci 2006, 24:595-605.
78. Kleen J.K., Sitomer M.T., Killeen P.R., Conrad C.D. Chronic stress impairs spatial memory and motivation for reward without disrupting motor ability and motivation to explore. Behav Neurosci 2006, 120:842-851.
79. Baran S.E., Armstrong C.E., Niren D.C., Hanna J.J., Conrad C.D. Chronic stress and sex differences on the recall of fear conditioning and extinction. Neurobiol Learn Mem 2009, 91:323-332.
80. McLaughlin K.J., Baran S.E., Conrad C.D. Chronic stress- and sex-specific neuromorphological and functional changes in limbic structures. Mol Neurobiol 2009, 40:166-182.
81. Haller J., Fuchs E., Halasz J., Makara G.B. Defeat is a major stressor in males while social instability is stressful mainly in females: towards the development of a social stress model in female rats. Brain Res Bull 1999, 50:33-39.
82. Verma P., Hellemans K.G., Choi F.Y., Yu W., Weinberg J. Circadian phase and sex effects on depressive/anxiety-like behaviors and HPA axis responses to acute stress. Physiol Behav 2010, 99:276-285.
83. Bellani R., Luecken L.J., Conrad C.D. Peripubertal anxiety profile can predict predisposition to spatial memory impairments following chronic stress. Behav Brain Res 2006, 166:263-270.
84. Vyas A., Chattarji S. Modulation of different states of anxiety-like behavior by chronic stress. Behav Neurosci 2004, 118:1450-1454.
85. McCormick C.M., Smith C., Mathews I.Z. Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behav Brain Res 2008, 187:228-238.
86. Popoli M. Agomelatine: innovative pharmacological approach in depression. CNS Drugs 2009, 23(Suppl. 2):27-34.
87. Watt M.J., Burke A.R., Renner K.J., Forster G.L. Adolescent male rats exposed to social defeat exhibit altered anxiety behavior and limbic monoamines as adults. Behav Neurosci 2009, 123:564-576.
88. McLaughlin K.J., Wilson J.O., Harman J., Wright R.L., Wieczorek L., Gomez J., et al. Chronic 17β-estradiol or cholesterol prevents stress-induced hippocampal CA3 dendritic retraction in ovariectomized female rats: possible correspondence between CA1 spine properties and spatial acquisition. Hippocampus 2010, 20:768-786.
89. Estrada-Camarena E., Lopez-Rubalcava C., Vega-Rivera N., Recamier-Carballo S., Fernandez-Guasti A. Antidepressant effects of estrogens: a basic approximation. Behav Pharmacol 2010, 21:451-464.
90. Conrad C.D. What is the functional significance of chronic stress-induced CA3 dendritic retraction within the hippocampus?. Behav Cognit Neurosci Rev 2006, 5:41-60.