Sex differences in baseline and drug-induced behavioural responses in classical behavioural tests

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 37, Issue 2, 2012, Pages 227-236

  Simpson, Joy ^a   Ryan, Colin ^a   Curley, Anita ^a   Mulcaire, Jeffrey ^a   Kelly, John P ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Behavioural pharmacology; Elevated plus maze; Forced swim test; Locomotor activity; Rat; Sex differences

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BEHAVIORAL SCIENCE; CONTROLLED STUDY; FEMALE; FORCED SWIMMING TEST; LOCOMOTION; MALE; MAZE TEST; NONHUMAN; OPEN FIELD TEST; RAT; SEX DIFFERENCE; SPRAGUE DAWLEY RAT;

ADRENERGIC UPTAKE INHIBITORS; AMPHETAMINE; ANIMALS; ANTI-ANXIETY AGENTS; BEHAVIOR, ANIMAL; CENTRAL NERVOUS SYSTEM STIMULANTS; DESIPRAMINE; DIAZEPAM; FEMALE; MALE; MOTOR ACTIVITY; RATS; RATS, SPRAGUE-DAWLEY; SEX CHARACTERISTICS;

EID: 84859620984     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2012.02.004     Document Type: Article

References (81)

1. Albonetti M.E., Farabollini F. Effects of single restraint on the defensive behavior of male and female rats. Physiol Behav 1995, 57:431-437.
2. Barros H.M., Ferigolo M. Ethopharmacology of imipramine in the forced-swimming test: gender differences. Neurosci Biobehav Rev 1998, 23:279-286.
3. Beatty W.W., Holzer G.A. Sex differences in stereotyped behavior in the rat. Pharmacol Biochem Behav 1978, 9:777-783.
4. Becker J.B. Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacol Biochem Behav 1999, 64:803-812.
5. Becker J.B., Hu M. Sex differences in drug abuse. Front Neuroendocrinol 2008, 29:36-47.
6. Becker J.B., Molenda H., Hummer D.L. Gender differences in the behavioral responses to cocaine and amphetamine. Implications for mechanisms mediating gender differences in drug abuse. Ann N Y Acad Sci 2001, 937:172-187.
7. Becker J.B., Robinson T.E., Lorenz K.A. Sex differences and estrous cycle variations in amphetamine-elicited rotational behavior. Eur J Pharmacol 1982, 80:65-72.
8. Bisagno V., Ferguson D., Luine V.N. Chronic d-amphetamine induces sexually dimorphic effects on locomotion, recognition memory, and brain monoamines. Pharmacol Biochem Behav 2003, 74:859-867.
9. Blanchard D.C., Blanchard R.J., Tom P., Rodgers R.J. Diazepam changes risk assessment in an anxiety/defense test battery. Psychopharmacology (Berl) 1990, 101:511-518.
10. Bosse R., Rivest R., Di Paolo T. Ovariectomy and estradiol treatment affect the dopamine transporter and its gene expression in the rat brain. Brain Res Mol Brain Res 1997, 46:343-346.
11. Brady K.T., Randall C.L. Gender differences in substance use disorders. Psychiatr Clin North Am 1999, 22:241-252.
12. Brotto L.A., Barr A.M., Gorzalka B.B. Sex differences in forced-swim and open-field test behaviours after chronic administration of melatonin. Eur J Pharmacol 2000, 402:87-93.
13. Camp D.M., Becker J.B., Robinson T.E. Sex differences in the effects of gonadectomy on amphetamine-induced rotational behavior in rats. Behav Neural Biol 1986, 46:491-495.
14. Castner S.A., Becker J.B. Sex differences in the effect of amphetamine on immediate early gene expression in the rat dorsal striatum. Brain Res 1996, 712:245-257.
15. Castner S.A., Xiao L., Becker J.B. Sex differences in striatal dopamine: in vivo microdialysis and behavioral studies. Brain Res 1993, 610:127-134.
16. Cicero T.J., Aylward S.C., Meyer E.R. Gender differences in the intravenous self-administration of mu opiate agonists. Pharmacol Biochem Behav 2003, 74:541-549.
17. Connor T.J., Kelly J.P., Leonard B.E. forced swim test-induced endocrine and immune changes in the rat: effect of subacute desipramine treatment. Pharmacol Biochem Behav 1998, 59:171-177.
18. Dalla C., Antoniou K., Drossopoulou G., Xagoraris M., Kokras N., Sfikakis A., et al. Chronic mild stress impact: are females more vulnerable?. Neuroscience 2005, 135:703-714.
19. Dalla C., Edgecomb C., Whetstone A.S., Shors T.J. Females do not express learned helplessness like males do. Neuropsychopharmacology 2008, 33:1559-1569.
20. Dalla C., Shors T.J. Sex differences in learning processes of classical and operant conditioning. Physiol Behav 2009, 97:229-238.
21. Diaz-Veliz G., Butron S., Benavides M.S., Dussaubat N., Mora S. Gender, estrous cycle, ovariectomy, and ovarian hormones influence the effects of diazepam on avoidance conditioning in rats. Pharmacol Biochem Behav 2000, 66:887-892.
22. Donny E.C., Caggiula A.R., Rowell P.P., Gharib M.A., Maldovan V., Booth S., et al. Nicotine self-administration in rats: estrous cycle effects, sex differences and nicotinic receptor binding. Psychopharmacology (Berl) 2000, 151:392-405.
23. Duchesne A., Dufresne M.M., Sullivan R.M. Sex differences in corticolimbic dopamine and serotonin systems in the rat and the effect of postnatal handling. Prog Neuropsychopharmacol Biol Psychiatry 2009, 33:251-261.
24. Duncko R., Kiss A., Skultetyova I., Rusnak M., Jezova D. Corticotropin-releasing hormone mRNA levels in response to chronic mild stress rise in male but not in female rats while tyrosine hydroxylase mRNA levels decrease in both sexes. Psychoneuroendocrinology 2001, 26:77-89.
25. Dunne F., O'Halloran A., Kelly J.P. Development of a home cage locomotor tracking system capable of detecting the stimulant and sedative properties of drugs in rats. Prog Neuropsychopharmacol Biol Psychiatry 2007, 31:1456-1463.
26. Fernandes C., Gonzalez M.I., Wilson C.A., File S.E. Factor analysis shows that female rat behaviour is characterized primarily by activity, male rats are driven by sex and anxiety. Pharmacol Biochem Behav 1999, 64:731-738.
27. Fernandez-Guasti A., Picazo O. Anxiolytic actions of diazepam, but not of buspirone, are influenced by gender and the endocrine stage. Behav Brain Res 1997, 88:213-218.
28. Fernandez-Guasti A., Reyes R., Martinez-Mota L., Lopez-Munoz F.J. Influence of inflammatory nociception on the anxiolytic-like effect of diazepam and buspirone in rats. Psychopharmacology (Berl) 2005, 180:399-407.
29. Frye C.A. Progestins influence motivation, reward, conditioning, stress, and/or response to drugs of abuse. Pharmacol Biochem Behav 2007, 86:209-219.
30. Frye C.A., Cuevas C.A., Kanarek R.B. Diet and estrous cycle influence pain sensitivity in rats. Pharmacol Biochem Behav 1993, 45:255-260.
31. Frye C.A., Walf A.A. Changes in progesterone metabolites in the hippocampus can modulate open field and forced swim test behavior of proestrous rats. Horm Behav 2002, 41:306-315.
32. Gorman J.M. Gender differences in depression and response to psychotropic medication. Gend Med 2006, 3:93-109.
33. Gouveia A., dos Santos U.D., Felisbino F.E., de Afonseca T.L., Antunes G., Morato S. Influence of the estrous cycle on the behavior of rats in the elevated T-maze. Behav Processes 2004, 67:167-171.
34. Hafner H., Maurer K., Loffler W., Fatkenheuer B., an der Heiden W., Riecher-Rossler A., et al. The epidemiology of early schizophrenia. Influence of age and gender on onset and early course. Br J Psychiatry Suppl 1994, 29-38.
35. 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.
36. Hughes R.N. Sex does matter: comments on the prevalence of male-only investigations of drug effects on rodent behaviour. Behav Pharmacol 2007, 18:583-589.
37. Jamison R.N., Butler S.F., Budman S.H., Edwards R.R., Wasan A.D. Gender differences in risk factors for aberrant prescription opioid use. J Pain 2010, 11:312-320.
38. Johnston A.L., File S.E. Sex differences in animal tests of anxiety. Physiol Behav 1991, 49:245-250.
39. Juarez J., Barrios de Tomasi E. Sex differences in alcohol drinking patterns during forced and voluntary consumption in rats. Alcohol 1999, 19:15-22.
40. Kelly J.P., Leonard B.E. An investigation of the antidepressant properties of lofepramine and its desmethylated metabolites in the forced swim and olfactory bulbectomized rat models of depression. Eur Neuropsychopharmacol 1999, 9:101-105.
41. Kokras N., Antoniou K., Dalla C., Bekris S., Xagoraris M., Ovestreet D.H., et al. Sex-related differential response to clomipramine treatment in a rat model of depression. J Psychopharmacol 2009, 23:945-956.
42. Lifschytz T., Shalom G., Lerer B., Newman M.E. Sex-dependent effects of fluoxetine and triiodothyronine in the forced swim test in rats. Eur Neuropsychopharmacol 2006, 16:115-121.
43. Linzer M., Spitzer R., Kroenke K., Williams J.B., Hahn S., Brody D., et al. Gender, quality of life, and mental disorders in primary care: results from the PRIME-MD 1000 study. Am J Med 1996, 101:526-533.
44. Lynch W.J. Sex differences in vulnerability to drug self-administration. Exp Clin Psychopharmacol 2006, 14:34-41.
45. Lynch W.J., Roth M.E., Carroll M.E. Biological basis of sex differences in drug abuse: preclinical and clinical studies. Psychopharmacology (Berl) 2002, 164:121-137.
46. Maggi A., Perez J. Progesterone and estrogens in rat brain: modulation of GABA (gamma-aminobutyric acid) receptor activity. Eur J Pharmacol 1984, 103:165-168.
47. Maggi A., Perez J. Estrogen-induced up-regulation of gamma-aminobutyric acid receptors in the CNS of rodents. J Neurochem 1986, 47:1793-1797.
48. Marcondes F.K., Miguel K.J., Melo L.L., Spadari-Bratfisch R.C. Estrous cycle influences the response of female rats in the elevated plus-maze test. Physiol Behav 2001, 74:435-440.
49. Marvan M.L., Chavez-Chavez L., Santana S. Clomipramine modifies fluctuations of forced swimming immobility in different phases of the rat estrous cycle. Arch Med Res 1996, 27:83-86.
50. McDermott C., Kelly J.P. Comparison of the behavioural pharmacology of the Lister-Hooded with 2 commonly utilised albino rat strains. Prog Neuropsychopharmacol Biol Psychiatry 2008, 32:1816-1823.
51. Milesi-Halle A., Hendrickson H.P., Laurenzana E.M., Gentry W.B., Owens S.M. Sex- and dose-dependency in the pharmacokinetics and pharmacodynamics of (+)-methamphetamine and its metabolite (+)-amphetamine in rats. Toxicol Appl Pharmacol 2005, 209:203-213.
52. Milesi-Halle A., McMillan D.E., Laurenzana E.M., Byrnes-Blake K.A., Owens S.M. Sex differences in (+)-amphetamine- and (+)-methamphetamine-induced behavioral response in male and female Sprague-Dawley rats. Pharmacol Biochem Behav 2007, 86:140-149.
53. Mora S., Dussaubat N., Diaz-Veliz G. Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats. Psychoneuroendocrinology 1996, 21:609-620.
54. Mugford C.A., Kedderis G.L. Sex-dependent metabolism of xenobiotics. Drug Metab Rev 1998, 30:441-498.
55. Nolen-Hoeksema S. Gender differences in depression. Curr Dir Psychol Sci 2001, 10:173-177. (Wiley-Blackwell).
56. Olivier J.D., Van Der Hart M.G., Van Swelm R.P., Dederen P.J., Homberg J.R., Cremers T., et al. A study in male and female 5-HT transporter knockout rats: an animal model for anxiety and depression disorders. Neuroscience 2008, 152:573-584.
57. Padilla E., Barrett D., Shumake J., Gonzalez-Lima F. Strain, sex, and open-field behavior: factors underlying the genetic susceptibility to helplessness. Behav Brain Res 2009, 201:257-264.
58. Palanza P. Animal models of anxiety and depression: how are females different?. Neurosci Biobehav Rev 2001, 25:219-233.
59. 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.
60. Pena Y., Prunell M., Dimitsantos V., Nadal R., Escorihuela R.M. Environmental enrichment effects in social investigation in rats are gender dependent. Behav Brain Res 2006, 174:181-187.
61. Pena Y., Prunell M., Rotllant D., Armario A., Escorihuela R.M. Enduring effects of environmental enrichment from weaning to adulthood on pituitary-adrenal function, pre-pulse inhibition and learning in male and female rats. Psychoneuroendocrinology 2009, 34:1390-1404.
62. Perez J., Zucchi I., Maggi A. Sexual dimorphism in the response of the GABAergic system to estrogen administration. J Neurochem 1986, 47:1798-1803.
63. 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.
64. Roth M.E., Cosgrove K.P., Carroll M.E. Sex differences in the vulnerability to drug abuse: a review of preclinical studies. Neurosci Biobehav Rev 2004, 28:533-546.
65. Sadeghipour H.R., Ghasemi M., Sadeghipour H., Riazi K., Soufiabadi M., Fallahi N., et al. Nitric oxide involvement in estrous cycle-dependent changes of the behavioral responses of female rats in the elevated plus-maze test. Behav Brain Res 2007, 178:10-17.
66. Savageau M.M., Beatty W.W. Gonadectomy and sex differences in the behavioral responses to amphetamine and apomorphine of rats. Pharmacol Biochem Behav 1981, 14:17-21.
67. Sfikakis A., Spyraki C., Sitaras N., Varonos D. Implication of the estrous cycle on conditioned avoidance behavior in the rat. Physiol Behav 1978, 21:441-446.
68. Simoni-Wastila L. Gender and psychotropic drug use 1998.
69. Suckow M.A., Weisbroth S.H., Franklin C.L. The laboratory rat 2006, Elsevier, Boston.
70. Sullivan R.M., Dufresne M.M., Waldron J. Lateralized sex differences in stress-induced dopamine release in the rat. Neuroreport 2009, 20:229-232.
71. Tachibana T. Open-field test for rats - correlational analysis. Psychol Rep 1982, 50:899-910.
72. Tonelli L.H., Holmes A., Postolache T.T. Intranasal immune challenge induces sex-dependent depressive-like behavior and cytokine expression in the brain. Neuropsychopharmacology 2008, 33:1038-1048.
73. Violle N., Balandras F., Le Roux Y., Desor D., Schroeder H. Variations in illumination, closed wall transparency and/or extramaze space influence both baseline anxiety and response to diazepam in the rat elevated plus-maze. Behav Brain Res 2009, 203:35-42.
74. Walker Q.D., Ray R., Kuhn C.M. Sex differences in neurochemical effects of dopaminergic drugs in rat striatum. Neuropsychopharmacology 2006, 31:1193-1202.
75. Waxman D.J., Holloway M.G. Sex differences in the expression of hepatic drug metabolizing enzymes. Mol Pharmacol 2009, 76:215-228.
76. Weinstock M. Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem Res 2007, 32:1730-1740.
77. Weintraub A., Singaravelu J., Bhatnagar S. Enduring and sex-specific effects of adolescent social isolation in rats on adult stress reactivity. Brain Res 2010, 1343:83-92.
78. Willner P. Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology (Berl) 1997, 134:319-329.
79. Xiao L., Becker J.B. Quantitative microdialysis determination of extracellular striatal dopamine concentration in male and female rats: effects of estrous cycle and gonadectomy. Neurosci Lett 1994, 180:155-158.
80. Yokoyama F., Yamauchi M., Oyama M., Okuma K., Onozawa K., Nagayama T., et al. Anxiolytic-like profiles of histamine H3 receptor agonists in animal models of anxiety: a comparative study with antidepressants and benzodiazepine anxiolytic. Psychopharmacology (Berl) 2009, 205:177-187.
81. Yoshida T., Oguro T., Kuroiwa Y. Hepatic and extrahepatic metabolism of deprenyl, a selective monoamine oxidase (MAO) B inhibitor, of amphetamines in rats: sex and strain differences. Xenobiotica 1987, 17:957-963.