The influence of social subordinate housing on the withdrawal effects from progesterone and estradiol in male rats

General and Comparative Endocrinology

Volumn 177, Issue 1, 2012, Pages 62-69

  Löfgren, Magnus ^a   Johansson, Maja ^a   Strömberg, Jessica ^a   Meyerson, Bengt ^b   Bäckström, Torbjörn ^a  

^a UMEÅ UNIVERSITY HOSPITAL   (Sweden)

^b Division of Pharmacology   (Sweden)

Author keywords

Allopregnanolone; Elevated plus maze; Estradiol; Open field; Progesterone; Social stress

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; CORTICOSTERONE; ESTRADIOL; PROGESTERONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL HOUSING; ANXIETY; ARTICLE; CHRONIC STRESS; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; ELEVATED PLUS MAZE TEST; EXPERIMENTAL TEST; FEEDING BEHAVIOR; HORMONE DEPENDENCE; HORMONE DETERMINATION; INTERSPECIFIC COMPETITION; LOCOMOTION; MALE; MAZE TEST; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; RAT; SOCIAL CHALLENGE TEST; SOCIAL INTERACTION; SOCIAL STATUS; SOCIAL STRESS; SOCIAL SUBORDINATE HOUSING; TUBE TEST;

EID: 84860520405     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2012.02.011     Document Type: Article

References (72)

1. Avitsur R., Stark J.L., Sheridan J.F. Social stress induces glucocorticoid resistance in subordinate animals. Horm. Behav. 2001, 39:247-257.
2. Barbaccia M.L., Serra M., Purdy R.H., Biggio G. Stress and neuroactive steroids. Int. Rev. Neurobiol. 2001, 46:243-272.
3. Bitran D., Hilvers R.J., Kellogg C.K. Anxiolytic effects of 3 alpha-hydroxy-5 alpha[beta]-pregnan-20-one: endogenous metabolites of progesterone that are active at the GABAA receptor. Brain Res. 1991, 561:157-161.
4. Björkqvist K. Social defeat as a stressor in humans. Physiol. Behav. 2001, 73:435-442.
5. Blanchard D.C., Sakai R.R., McEwen B., Weiss S.M., Blanchard R.J. Subordination stress: behavioral, brain, and neuroendocrine correlates. Behav. Brain Res. 1993, 58:113-121.
6. Blanchard D.C., Spencer R.L., Weiss S.M., Blanchard R.J., McEwen B., Sakai R.R. Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates. Psychoneuroendocrinology 1995, 20:117-134.
7. Clarke F.M., Faulkes C.G. Hormonal and behavioural correlates of male dominance and reproductive status in captive colonies of the naked mole-rat, Heterocephalus glaber. Proc. Biol. Sci. 1998, 265:1391-1399.
8. Costa A.M., Spence K.T., Smith S.S., ffrench-Mullen J.M. Withdrawal from the endogenous steroid progesterone results in GABAA currents insensitive to benzodiazepine modulation in rat CA1 hippocampus. J. Neurophysiol. 1995, 74:464-469.
9. Crawley J.N., Glowa J.R., Majewska M.D., Paul S.M. Anxiolytic activity of an endogenous adrenal steroid. Brain Res. 1986, 398:382-385.
10. Cutler S.M., Pettus E.H., Hoffman S.W., Stein D.G. Tapered progesterone withdrawal enhances behavioral and molecular recovery after traumatic brain injury. Exp. Neurol. 2005, 195:423-429.
11. Davis J.F., Krause E.G., Melhorn S.J., Sakai R.R., Benoit S.C. Dominant rats are natural risk takers and display increased motivation for food reward. Neuroscience 2009, 162:23-30.
12. Devall A.J., Liu Z.W., Lovick T.A. Hyperalgesia in the setting of anxiety: sex differences and effects of the oestrous cycle in Wistar rats. Psychoneuroendocrinology 2009, 34:587-596.
13. Ebner K., Wotjak C.T., Landgraf R., Engelmann M. Neuroendocrine and behavioral response to social confrontation: residents versus intruders, active versus passive coping styles. Horm. Behav. 2005, 47:14-21.
14. Follesa P., Concas A., Porcu P., Sanna E., Serra M., Mostallino M.C., Purdy R.H., Biggio G. Role of allopregnanolone in regulation of GABA(A) receptor plasticity during long-term exposure to and withdrawal from progesterone. Brain Res. Brain Res. Rev. 2001, 37:81-90.
15. Frye C.A., Rhodes M.E. Progesterone's 5 alpha-reduced metabolite, 3 alpha,5 alpha-THP, mediates lateral displacement of hamsters. Brain Res. 2005, 1038:59-68.
16. Galea L.A., Wide J.K., Barr A.M. Estradiol alleviates depressive-like symptoms in a novel animal model of post-partum depression. Behav. Brain Res. 2001, 122:1-9.
17. Gallo M.A., Smith S.S. Progesterone withdrawal decreases latency to and increases duration of electrified prod burial: a possible rat model of PMS anxiety. Pharmacol. Biochem. Behav. 1993, 46:897-904.
18. Gentsch C., Lichtsteiner M., Feer H. Competition for sucrose-pellets in triads of male Wistar rats: the individuals' performances are differing but stable. Behav. Brain Res. 1988, 27:37-44.
19. Girdler S.S., Klatzkin R. Neurosteroids in the context of stress: implications for depressive disorders. Pharmacol. Ther. 2007, 116:125-139.
20. Girdler S.S., Pedersen C.A., Straneva P.A., Leserman J., Stanwyck C.L., Benjamin S., Light K.C. Dysregulation of cardiovascular and neuroendocrine responses to stress in premenstrual dysphoric disorder. Psychiatry Res. 1998, 81:163-178.
21. Goldman L., Winget C., Hollingshead G.W., Levine S. Postweaning development of negative feedback in the pituitary-adrenal system of the rat. Neuroendocrinology 1973, 12:199-211.
22. Gomez C., Saldivar-Gonzalez A., Delgado G., Rodriguez R. Rapid anxiolytic activity of progesterone and pregnanolone in male rats. Pharmacol. Biochem. Behav. 2002, 72:543-550.
23. Griffiths J., Lovick T. Withdrawal from progesterone increases expression of alpha4, beta1, and delta GABA(A) receptor subunits in neurons in the periaqueductal gray matter in female Wistar rats. J. Comp. Neurol. 2005, 486:89-97.
24. Gulinello M., Gong Q.H., Li X., Smith S.S. Short-term exposure to a neuroactive steroid increases alpha4GABA(A) receptor subunit levels in association with increased anxiety in the female rat. Brain Res. 2001, 910:55-66.
25. Guo A.L., Petraglia F., Criscuolo M., Ficarra G., Nappi R.E., Palumbo M.A., Trentini G.P., Purdy R.H., Genazzani A.R. Evidence for a role of neurosteroids in modulation of diurnal changes and acute stress-induced corticosterone secretion in rats. Gynecol. Endocrinol. 1995, 9:1-7.
26. Hall C.S. Emotional behavior in the rat: I. Defecation and urination as measures of individual differences in emotionality. J. Comp. Physiol. Psychol. 1934, 18:385-403.
27. Herrero A.I., Sandi C., Venero C. Individual differences in anxiety trait are related to spatial learning abilities and hippocampal expression of mineralocorticoid receptors. Neurobiol. Learn. Mem. 2006, 86:150-159.
28. Ho Y.J., Eichendorff J., Schwarting R.K. Individual response profiles of male Wistar rats in animal models for anxiety and depression. Behav. Brain Res. 2002, 136:1-12.
29. Joly D., Sanger D.J. Social competition in rats: a test sensitive to acutely administered anxiolytics. Behav. Pharmacol. 1991, 2:205-213.
30. Kabbaj M., Norton C.S., Kollack-Walker S., Watson S.J., Robinson T.E., Akil H. Social defeat alters the acquisition of cocaine self-administration in rats: role of individual differences in cocaine-taking behavior. Psychopharmacology 2001, 158:382-387.
31. Kayir H., Uzbay T. Effects of clozapine on ethanol withdrawal syndrome in rats. Alcohol Alcohol. 2008, 43:619-625.
32. Kessler R.C., Price R.H., Wortman C.B. Social factors in psychopathology: stress, social support, and coping processes. Annu. Rev. Psychol. 1985, 36:531-572.
33. Koolhaas J.M., De Boer S.F., De Rutter A.J., Meerlo P., Sgoifo A. Social stress in rats and mice. Acta Physiol. Scand. Suppl. 1997, 640:69-72.
34. Koolhaas J.M., Meerlo P., De Boer S.F., Strubbe J.H., Bohus B. The temporal dynamics of the stress response. Neurosci. Biobehav. Rev. 1997, 21:775-782.
35. Koss W.A., Gehlert D.R., Shekhar A. Different effects of subchronic doses of 17-beta estradiol in two ethologically based models of anxiety utilizing female rats. Horm. Behav. 2004, 46:158-164.
36. Kruk M.R., Halasz J., Meelis W., Haller J. Fast positive feedback between the adrenocortical stress response and a brain mechanism involved in aggressive behavior. Behav. Neurosci. 2004, 118:1062-1070.
37. Kunchandy J., Kulkarni S.K. Reversal by alpha-2 agonists of diazepam withdrawal hyperactivity in rats. Psychopharmacology 1986, 90:198-202.
38. Landgren S., Selstam G. Interaction between 17 beta-oestradiol and 3 alpha-hydroxy-5 alpha-pregnane-20-one in the control of neuronal excitability in slices from the CA1 hippocampus in vitro of guinea-pigs and rats. Acta Physiol. Scand. 1995, 154:165-176.
39. Löfgren M., Johansson I.M., Meyerson B., Lundgren P., Bäckström T. Progesterone withdrawal effects in the open field test can be predicted by elevated plus maze performance. Horm. Behav. 2006, 50:208-215.
40. Löfgren M., Johansson I.M., Meyerson B., Turkmen S., Bäckström T. Withdrawal effects from progesterone and estradiol relate to individual risk-taking and explorative behavior in female rats. Physiol. Behav. 2009, 96:91-97.
41. Lucion A.B., De-Almeida R.M., Da-Silva R.S. Territorial aggression, body weight, carbohydrate metabolism and testosterone levels of wild rats maintained in laboratory colonies. Braz. J. Med. Biol. Res. 1996, 29:1657-1662.
42. Lustyk M.K., Widman L., Paschane A., Ecker E. Stress, quality of life and physical activity in women with varying degrees of premenstrual symptomatology. Women Health 2004, 39:35-44.
43. Löfgren M., Johansson I.-M., Meyerson B., Turkmen S., Bäckström T. Withdrawal effects from progesterone and estradiol relate to individual risk-taking and explorative behavior in female rats. Physiol. Behav. 2009, 96:91.
44. Majewska M.D., Harrison N.L., Schwartz R.D., Barker J.L., Paul S.M. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 1986, 232:1004-1007.
45. Malatynska E., Goldenberg R., Shuck L., Haque A., Zamecki P., Crites G., Schindler N., Knapp R.J. Reduction of submissive behavior in rats: a test for antidepressant drug activity. Pharmacology 2002, 64:8-17.
46. Masur J., Maroni J.B., Benedito M.A. Genetically selected winner and loser rats in the tunnel competition: influence of apomorphine and dopa. Behav. Biol. 1975, 14:21-30.
47. Meerlo P., De Boer S.F., Koolhaas J.M., Daan S., Van den Hoofdakker R.H. Changes in daily rhythms of body temperature and activity after a single social defeat in rats. Physiol. Behav. 1996, 59:735-739.
48. Meerlo P., Overkamp G.J., Benning M.A., Koolhaas J.M., Van den Hoofdakker R.H. Long-term changes in open field behaviour following a single social defeat in rats can be reversed by sleep deprivation. Physiol. Behav. 1996, 60:115-119.
49. Meerlo P., Overkamp G.J., Daan S., Van Den Hoofdakker R.H., Koolhaas J.M. Changes in behaviour and body weight following a single or double social defeat in rats. Stress 1996, 1:21-32.
50. Miczek K.A., Barry H. What does the tube test measure?. Behav. Biol. 1975, 13:537-539.
51. Moran M.H., Goldberg M., Smith S.S. Progesterone withdrawal. II: Insensitivity to the sedative effects of a benzodiazepine. Brain Res. 1998, 807:91-100.
52. Noble R.E. Depression in women. Metabolism 2005, 54:49-52.
53. Pacak K., Palkovits M. Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr. Rev. 2001, 22:502-548.
54. Perkonigg A., Yonkers K.A., Pfister H., Lieb R., Wittchen H.U. Risk factors for premenstrual dysphoric disorder in a community sample of young women: the role of traumatic events and posttraumatic stress disorder. J. Clin. Psychiatry 2004, 65:1314-1322.
55. Ramos A., Berton O., Mormede P., Chaouloff F. A multiple-test study of anxiety-related behaviours in six inbred rat strains. Behav. Brain Res. 1997, 85:57-69.
56. Roca C.A., Schmidt P.J., Altemus M., Deuster P., Danaceau M.A., Putnam K., Rubinow D.R. Differential menstrual cycle regulation of hypothalamic-pituitary-adrenal axis in women with premenstrual syndrome and controls. J. Clin. Endocrinol. Metab. 2003, 88:3057-3063.
57. Romeo R.D., Karatsoreos I.N., McEwen B.S. Pubertal maturation and time of day differentially affect behavioral and neuroendocrine responses following an acute stressor. Horm. Behav. 2006, 50:463-468.
58. Romeo R.D., Karatsoreos I.N., McEwen B.S. Pubertal maturation and time of day differentially affect behavioral and neuroendocrine responses following an acute stressor. Horm. Behav. 2006, 50:463-468.
59. 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.
60. Sandbak T., Murison R., Sarviharju M., Hyytia P. Defensive burying and stress gastric erosions in alcohol-preferring AA and alcohol-avoiding ANA rats. Alcohol Clin. Exp. Res. 1998, 22:2050-2054.
61. Schmitt U., Hiemke C. Strain differences in open-field and elevated plus-maze behavior of rats without and with pretest handling. Pharmacol. Biochem. Behav. 1998, 59:807-811.
62. Schneider T., Popik P. Attenuation of estrous cycle-dependent marble burying in female rats by acute treatment with progesterone and antidepressants. Psychoneuroendocrinology 2007, 32:651-659.
63. Sgoifo A., Koolhaas J., De Boer S., Musso E., Stilli D., Buwalda B., Meerlo P. Social stress, autonomic neural activation, and cardiac activity in rats. Neurosci. Biobehav. Rev. 1999, 23:915-923.
64. Smith S.S., Gong Q.H., Li X., Moran M.H., Bitran D., Frye C.A., Hsu F.C. Withdrawal from 3alpha-OH-5alpha-pregnan-20-one using a pseudopregnancy model alters the kinetics of hippocampal GABAA-gated current and increases the GABAA receptor alpha4 subunit in association with increased anxiety. J. Neurosci. 1998, 18:5275-5284.
65. Smith S.S., Ruderman Y., Frye C., Homanics G., Yuan M. Steroid withdrawal in the mouse results in anxiogenic effects of 3alpha,5beta-THP: a possible model of premenstrual dysphoric disorder. Psychopharmacology 2006, 186:323-333.
66. Stefanski V., Knopf G., Schulz S. Long-term colony housing in Long Evans rats: immunological, hormonal, and behavioral consequences. J. Neuroimmunol. 2001, 114:122-130.
67. Stoffel E.C., Craft R.M. Ovarian hormone withdrawal-induced "depression" in female rats. Physiol. Behav. 2004, 83:505-513.
68. Strömberg J., Bäckström T., Lundgren P. Rapid non-genomic effect of glucocorticoid metabolites and neurosteroids on the gamma-aminobutyric acid-A receptor. Eur. J. Neurosci. 2005, 21:2083-2088.
69. 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.
70. Windle R.J., Gamble L.E., Kershaw Y.M., Wood S.A., Lightman S.L., Ingram C.D. Gonadal steroid modulation of stress-induced hypothalamo-pituitary-adrenal activity and anxiety behavior: role of central oxytocin. Endocrinology 2006, 147:2423-2431.
71. Xigeng Z., Yonghui L., Xiaojing L., Lin X., Dongmei W., Jie L., Xiaoyan Y., Nan S. Social crowding sensitizes high-responding rats to psychomotor-stimulant effects of morphine. Pharmacol. Biochem. Behav. 2004, 79:213-218.
72. Young E.A., Korszun A. The hypothalamic-pituitary-gonadal axis in mood disorders. Endocrinol. Metab. Clin. North Am. 2002, 31:63-78.