Sex does matter: Comments on the prevalence of male-only investigations of drug effects on rodent behaviour

Behavioural Pharmacology

Volumn 18, Issue 7, 2007, Pages 583-589

  Hughes, Robert N ^a  

^a UNIVERSITY OF CANTERBURY   (New Zealand)

Author keywords

Drugs; Mouse; Rat; Sex differences

Indexed keywords

ANIMAL BEHAVIOR; DRUG EFFECT; ESTRUS CYCLE; NONHUMAN; REVIEW; SEX DIFFERENCE; SEXUAL BEHAVIOR;

ANIMALS; BEHAVIOR, ANIMAL; FEMALE; LEARNING; MALE; MICE; PHARMACOLOGY; RATS; RESEARCH DESIGN; SEX FACTORS;

EID: 34948884575     PISSN: 09558810     EISSN: None     Source Type: Journal    
DOI: 10.1097/FBP.0b013e3282eff0e8     Document Type: Review

References (87)

1. Abdul-Monim Z, Reynolds GP, Neill JC (2006). The effects of atypical and classical antipsychotics on sub-chronic PCP-induced cognitive deficits in a reversal-learning paradigm. Behav Brain Res 169:263-273.
2. Aguilar R, Gil L, Gray JA, Driscoll P, Flint J, Dawson GR, et al. (2003). Fearfulness and sex in F2 Roman rats: males display more fear though both sexes share the same fearfulness traits. Physiol Behav 78:723-732.
3. Ammar AA, Nergårdh R, Fredholm BB, Brodin U, Södersten P (2005). Intake inhibition by NPY and CCK-8: a challenge of the notion of NPY as an 'Orexigen'. Behav Brain Res 161:82-87.
4. Araujo NP, Fukushiro DF, Cunha JLS, Levin R, Chinen CC, Carvalho RC, et al. (2006). Drug-induced home cage conspecifics' behavior can potentiate behavioral sensitization in mice. Pharmacol Biochem Behav 84:142-147.
5. Archer J (1975). Rodent sex differences in emotional and related behavior. Behav Biol 14:451-479.
6. Archer J, Mehdikhani M (2003). Variability among males in sexually selected attributes. Rev Gen Psychol 7:219-236.
7. Bardo MT, Bowling SL, Rowlett JK, Manderscheid P, Buxton ST, Dwoskin LP (1995). Environmental enrichment attenuates locomotor sensitization, but no in vitro dopamine release, induced by amphetamine. Pharmacol Biochem Behav 51:397-405.
8. Becker JB (1999). Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacol Biochem Behav 64:803-812.
9. Becker JB, Cha JH (1989). Estrous cycle-dependent variation in amphetamine-induced behaviors and striatal dopamine release assessed with microdialysis. Behav Brain Res 35:117-125.
10. Becker JB, Arnold AP, Berkley KJ, Blaustein JD, Eckel LA, Hampson E, et al. (2006). Strategies and methods for research on sex differences in brain and behavior. Endocrinology 146:1650-1673.
11. Berger-Sweeney J, Arnold A, Gabeau D, Mills J (1995). Sex differences in learning and memory in mice: effects of sequence of testing and cholinergic blockade. Behav Neurosci 109:859-873.
12. Blanchard DC, Shepherd JK, Rodgers RJ, Blanchard RJ (1992). Evidence for differential effects of 8-OH-DPAT on male and female rats in the Anxiety/Defense Test Battery. Psychopharmacology 106:531-539.
13. Blanchard DC, Griebel G, Blanchard RJ (1995). Gender bias in the preclinical psychopharmacology of anxiety: male models for (predominantly) female disorders. J Psychopharmacol 9:79-82.
14. Blehar MC (1995). Gender differences in risk factors for mood and anxiety disorders: implication for clinical treatment research. Psychopharmacol Bull 31:4687-4691.
15. Blokland A, Rutten K, Prickaerts J (2006). Analysis of spatial orientation strategies of male and female Wistar rats in a Morris water escape task. Behav Brain Res 171:216-224.
16. Bowers JM, Alexander BK (1967). Mice: individual recognition by olfactory cues. Science 158:1208-1210.
17. Bradley DWM, Joyce D, Murphy EH, Nash BM, Porsolt RD, Summerfield RD, et al. (1968). Amphetamine-barbiturate mixture: effects on the behaviour of mice. Nature 220:187-188.
18. Breedlove SM (1992). Sexual differentiation of the brain and behavior. In: Becker JB, Breedlove SM, Crews D, editors. Behavioral endocrinology. Cambridge, Massachusetts: The MIT Press; pp. 39-68.
19. Broadhurst PL (1977). Pharmacogenetics. In: Iversen LL, Iversen SD, Snyder SH, editors. Handbook of psychopharmacology. Vol 7. Principles of behavioral pharmacology. New York: Plenum Press; pp. 265-320.
20. Cahill L (2006). Why sex matters. Nature Rev Neurosci 7:477-484.
21. Cameron OG, Hill EM (1989.) Women and anxiety. In: Perry BL, editor. The psychiatric clinics of North America. Philadelphia, Pennsylvania: WB Saunders; pp. 175-186.
22. Camp DM, Robinson TE (1988). Susceptibility to sensitization. I. Sex differences in the enduring effects of chronic D-amphetamine treatment on locomotion, stereotyped behavior and brain monoamines. Behav Brain Res 30:55-68.
23. Carlsson M, Carlsson A (1988). A regional study of sex differences in rat brain serotonin. Prog Neuropsychopharmacol Biol Psychiatry 12:53-61.
24. Carter SC (1992a). Neuroendocrinology of sexual behavior in the female. In: Becker JB, Breedlove SM, Crews D, editors. Behavioral endocrinology. Cambridge, Massachusetts: The MIT Press; pp. 71-95.
25. Carter SC (1992b). Hormonal influences on human sexual behavior. In: Becker JB, Breedlove SM, Crews D, editors. Behavioral endocrinology. Cambridge, Massachusetts: The MIT Press; pp. 131-142.
26. Claassen V (1994). Neglected factors in pharmacology and neuroscience research. Amsterdam: Elsevier.
27. Cooper GD, Pickavance LC, Wilding JPH, Halford JCG, Goudie AJ (2005). A parametric analysis of olanzapine-induced weight gain in female rats. Psychopharmacology 181:80-89.
28. Creel S, Creel NM, Mills MGL, Monfort SL (1997). Rank and reproduction in cooperatively breeding African wild dogs: behavioral and endocrine correlates. Behav Ecol 8:298-306.
29. Croft AP, Brooks SP, Cole J, Little HJ (2005). Social defeat increases alcohol preference of C57BL/10 strain mice; effect prevented by a CCKB antagonist. Psychopharmacology 183:163-170.
30. DeBold JF, Miczek KA (1985). Testosterone modulates the effects of ethanol on male mouse aggression. Psychopharmacology 86:286-290.
31. Doty RL (1986). Odor-guided behavior in mammals. Experientia 42:257-271.
32. D'Souza DN, Harlan RE, Garcia MM (1999). Sexual dimorphism in the response to N-methyl-D-aspartate antagonists and morphine on behavior and c-Fos induction in the rat brain. Neuroscience 93:1539-1547.
33. Dwyer DS, Donohue D (2003). Induction of hyperglycemia in mice with atypical antipsychotic drugs that inhibit glucose uptake. Pharmacol Biochem Behav 75:255-260.
34. Feingold A (1992). Sex differences in variability in intellectual abilities: a new look at an old controversy. Rev Ed Res 62:61-84.
35. Feingold A (1994). Sex differences in personality: a meta-analysis. Psychol Bull 116:429-456.
36. Fox KA, Tuckosh JR, Wilcox AH (1970). Increased aggression among grouped male mice fed chlordiazepoxide. Eur J Pharmacol 11:119-121.
37. 1 receptor knockout newborn and adult mice. Behav Pharmacol 16:431-440.
38. Gorski RA, Gordon JH, Shryne JE, Southam AM (1978). Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Res 148:333-346.
39. Gray JA (1971). Sex differences in emotional behavior in mammals including man: endocrine bases. Acta Psychol 35:29-46.
40. Gupta BD, Holland HC (1972). Emotion as a determinant of the effects of drugs and their combination on different components of behaviour in rats. Neuropharmacology 11:31-38.
41. L/Bax ratio in the posterior cingulate cortex in rats. Behav Brain Res 168:236-242.
42. Hines M, Allen LS, Gorski RA (1992). Sex differences in subregions of the medial nucleus of the amygdala and the bed nucleus of the stria terminalis of the rat. Brain Res 579:321-326.
43. Hitchcock FA (1925). Studies of vigor. V. The comparative activity of male and female albino rats. Am J Physiol 75:205-210.
44. Holloway WR Jr, Thor DH (1984). Testosterone dependent effects of caffeine on social investigation by adult male rats. Physiol Behav 33:959-964.
45. Hu M, Becker JB (2003). Effects of sex and estrogen on behavioral sensitization to cocaine in rats. J Neurosci 23:693-699.
46. Hughes RN (2006). Memory-dependent novelty-related location preferences: sex-related attenuation of forgetting by D-glucose and tacrine. Behav Brain Res 166:39-44.
47. Hughes RN (2007). Neotic preferences in laboratory rodents: issues, assessment and substrates. Neurosci Biobehav Rev 31:441-464.
48. Hughes RN, Syme LA (1972). The role of social isolation and sex in determining effects of chlordiazepoxide and methylphenidate on exploratory behaviour. Psychopharmacologia 27:359-366.
49. Irwin S, Slabok M, Thomas G (1958). Individual differences: I. Correlation between control locomotor activity and sensitivity to stimulant and depressant drugs. J Pharmacol ExpThera 125:206-211.
50. Jones JD, Busse GD, Riley AL (2006). Strain-dependent sex differences in the effects of alcohol in cocaine-induced taste aversion. Pharmacol Biochem Behav 83:554-560.
51. Juraska JM (1991). Sex differences in 'cognitive' regions of the rat brain. Psychoneuroendocrinology 16:105-109.
52. Kanit L, Taskiran D, Furedy JJ, Kulali B, McDonald R, Pogun S (1998). Nicotine interacts with sex in affecting rat choice between 'lookout' and 'navigational' cognitive styles in the Morris water maze place learning task. Brain Res Bull 46:441-445.
53. Kavaliers M, Choleris E, Colwell DD (2001). Brief exposure to female odors 'emboldens' male mice by reducing predator-induced behavioral and hormonal responses. Horm Behav 40:497-509.
54. Kelly SJ, Ostrowski NL, Wilson MA (1999). Gender differences in brain and behavior: hormonal and neural bases. Pharmacol Biochem Behav 64:655-664.
55. Koenig J, Lazarus C, Jeltsch H, Hamida SB, Riegert C, Kelche C, et al. (2005). MDMA (ecstasy) effects in pubescent rats: males are more sensitive than females. Pharmacol Biochem Behav 81:635-644.
56. Komiya M, Takeuchi T, Harada E (2006). Lemon oil vapour causes an antistress effect via modulating the 5-HT and DA activities in mice. Behav Brain Res 172:240-249.
57. Koyla E, Demirgoren S, London ED, Pogun S (1997). Sex difference in upregulation of nicotinic acetylcholine receptors in rat brain. Life Sci 61:185-190.
58. Larson EB, Carroll ME (2005). Wheel running as a predictor of cocaine self-administration and reinstatement in female rats. Pharmacol Biochem Behav 82:590-600.
59. Lehman O, Jeltsch H, Lazarus C, Tritschler L, Fabrice B, Cassel J-C (2002). Combined 192 IgG-saporin and 5,7-dihydroxytryptamine lesions in the male rat brain: a neurochemical and behavioral study. Pharmacol Biochem Behav 72:899-912.
60. Lydell K, Doty RL (1972). Male rat odor preferences for female urine as a function of sexual experience, urine age, and urine source. Horm Behav 3:205-212.
61. Madeira MD, Lieberman AR (1995). Sexual dimorphism in the mammalian limbic system. Prog Neurobiol 45:275-333.
62. Madison DM (1980). Space use and social structure in meadow voles, Microtus pennsylvanicus. Behav Ecol Sociobiol 7:65-71.
63. Maxwell DR (1968). Principles of animal experimentation in psychopharmacology. In: Joyce CRB, editor. Psychopharmacology: Dimensions and perspectives. London: Tavistock Publications; pp. 57-93.
64. Meziane H, Ouagazzal A-M, Aubert L, Wietrzych M, Krezel W (2007). Estrous cycle effects on behavior of C57BL/6J and BALB/cByJ female mice: implications for phenotyping strategies. Genes Brain Behav 6:192-200.
65. Mizukami S, Nishizuka M, Arai Y (1983). Sexual difference in nuclear volume and its ontogeny in the rat amygdala. Exp Neurol 79:569-575.
66. Mock EJ, Norton HW, Frankel AI (1978). Daily rhythmicity of serum testosterone concentration in the male laboratory rat. Endocrinology 103:1111-1121.
67. Mora S, Díaz-Véliz G, Millán R, Lungenstrass S, Quirós S, Coto-Morales T, et al. (2005). Anxiolytic and antidepressant-like effects of the hydroalcoholic extract from Aloysia polystachya in rats. Pharmacol Biochem Behav 82:373-378.
68. Munn NL (1950). Handbook of psychological research on the rat. Boston: Houghton Mifflin.
69. + channels pathway by codeine. Pharmacol Biochem Behav 82:695-703.
70. Palanza P (2001). Animal models of anxiety and depression: how are females different? Neurosci Biobehav Rev 25:219-233.
71. Palenicek T, Votava M, Bubenikova V, Horacek J (2005). Increased sensitivity to the acute effects of MDMA (ecstasy) in female rats. Physiol Behav 86:546-553.
72. Patti CL, Frussa-Filho R, Silva RH, Carvalho RC, Kameda SR, Takatsu-Coleman AL, et al. (2005). Behavioral characterization of morphine effects on motor activity in mice. Pharmacol Biochem Behav 81:923-927.
73. Paul V (2003a). Inhibition of acute hyperammonemia-induced convulsions by systemically administered gamma aminobutyric acid in rats. Pharmacol Biochem Behav 74:523-528.
74. Paul V (2003b). The effect of N-nitro-L-arginine methyl ester posttreatment on the anticonvulsant effect of phenobarbitone and diazepam on picrotoxin-induced convulsions in rats. Pharmacol Biochem Behav 74:789-794.
75. Paul V, Subramanian EH (2002). Evidence for an involvement of nitric oxide and gamma aminobutyric acid in the anticonvulsant action of L-arginine on picrotoxin-induced convulsions in rats. Pharmacol Biochem Behav 72:515-519.
76. Paul V, Reddy L, Ekambaram P (2003). Prevention of picrotoxin convulsions-induced learning and memory impairment by nitric oxide increasing dose of L-arginine in rats. Pharmacol Biochem Behav 75:329-334.
77. Ploj K, Roman E, Nylander I (2002). Effects of maternal separation on brain nociceptin/orphanin FG peptide levels in male Wistar rats. Pharmacol Biochem Behav 73:123-129.
78. Porsolt RD, Bertin A, Jalfre M (1978).'Behavioural despair' in rats and mice: strain differences and the effects of imipramine. Eur J Pharmacol 51:291-294.
79. Rezvani AH, Levin ED (2003). Nicotine-alcohol interactions and attentional performance on an operant visual signal detection task in female rats. Pharmacol Biochem Behav 76:75-83.
80. Roberts DCS, Bennett SAL, Vickers GJ (1989). The estrus cycle affects cocaine self-administration on a progressive ratio schedule in rats. Psychopharmacology 98:408-411.
81. Sell SL, Scalzitti JM, Thomas ML, Cunningham KA (2000). Influence of ovarian hormones and estrous cycle on the behavioral response to cocaine in female rats. J Pharmacol Exp Thera 293:879-886.
82. Sircar R, Kim D (1999). Female gonadal hormones differentially modulate cocaine-induced behavioral sensitization in Fischer, Lewis, and Sprague-Dawley rats. J Pharmacol Exp Ther 289:54-65.
83. Tirelli E, Laviola G, Adriani W(2003). Ontogenesis of behavioral sensitization and conditioned place preference induced by psychostimulants in laboratory rodents. Neurosci Biobehav Rev 27:163-178.
84. Yonkers KA, Kando JC, Cole JO, Blumenthal S (1992). Gender differences in pharmacokinetics and pharmacodynamics of psychotropic medication. Am J Psychiatry 149:587-595.
85. Van Haaren F, Meyer ME (1991). Sex differences in locomotor activity after acute and chronic cocaine administration. Pharmacol Biochem Behav 39:923-927.
86. Walf AA, Frye CA (2007). The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protocols 2:322-328.
87. Zhang L, Ma W, Barker JL, Rubinow DR (1999). Sex differences in expression of serotonin receptors (subtypes 1A and 2A) in rat's brain: a possible role of testosterone. Neuroscience 94:251-259.