Abstract
Sex differences in social behaviors exist in mammals during adulthood, and further evidence suggests that sex differences in behavior are present before sexual maturity. In order to model behavioral disorders in animals, it is important to assess baseline sex-related behavioral differences, especially when studying disorders for which sex-related behavioral effects are expected. We investigated the effect of sex on behavior in three strains of prepubertal mice (C57BL/6, CFW, and CF1) using a wheel-running assay. We found no significant sex differences in latency to run on the wheel or total duration of wheel running within each strain. During the social interaction test, there were no differences between the sexes in latency or total duration of contact or following between a subject and a novel mouse. We also evaluated behavioral patterns of wheel running and stereotypical behaviors such as burrowing and grooming. Both sexes showed characteristic wheel-running behavior, spending the majority of each trial interacting with the wheel when it was free and more time performing other activities (e.g., stereotypical behaviors, general locomotion) when it was jammed. These results provide evidence that, among various strains of prepubertal mice, baseline sex-related behavioral differences are not strong enough to influence the measured behaviors.
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References
Albert M, Roussel C (1984) Strain differences in the concentration, motility and morphology of epididymal sperm in relation to puberty in mice. Int J Androl 7:34–37
Beatty WW (1992) Gonadal hormones and sex differences in nonreproductive behaviors. In: Gerall AMA, Howard, Ward, Ingeborg L (eds) Sexual differentiation, vol 11. Plenum, New York, pp 85–128
Beery AK, Zucker I (2011) Sex bias in neuroscience and biomedical research. Neurosci Biobehav Rev 35(3):565–572. doi:10.1016/j.neubiorev.2010.07.002
Bowen RS, Knab AM, Hamilton AT, McCall JR, Moore-Harrison TL, Lightfoot JT (2012) Effects of supraphysiological doses of sex steroids on wheel running activity in mice. J Steroids Horm Sci 3(2):110. doi:10.4172/2157-7536.1000110
Broida J, Svare B (1984) Sex differences in the activity of mice: modulation by postnatal gonadal hormones. Horm Behav 18(1):65–78
Cahill L (2012) A half-truth is a whole lie: on the necessity of investigating sex influences on the brain. Endocrinology 153(6):2541–2543. doi:10.1210/en.2011-2167
Charles River Laboratories International Inc. (2014a) CF-1™ mouse growth chart. http://www.criver.com/products-services/basic-research/find-a-model/cf-1-mouse. Retrieved 14 Aug 2014
Charles River Laboratories International Inc. (2014b). Swiss Webster (CFW®) growth chart. http://www.criver.com/products-services/basic-research/find-a-model/swiss-webster-%28cfw%29-mouse. Retrieved 14 Aug 2014
Colledge WH, Mei H, d’Anglemont de Tassigny X (2010) Mouse models to study the central regulation of puberty. Mol Cell Endocrinol 324(1–2):12–20. doi:10.1016/j.mce.2010.01.015
Crawley JN (2007) Mouse behavioral assays relevant to the symptoms of autism. Brain Pathol 17(4):448–459. doi:10.1111/j.1750-3639.2007.00096.x
Dowse H, Umemori J, Koide T (2010) Ultradian components in the locomotor activity rhythms of the genetically normal mouse, Mus musculus. J Exp Biol 213(Pt 10):1788–1795. doi:10.1242/jeb.038877
Evans JS, Varney Roger F, Koch FC (1941) The mouse uterine weight method for the assay of estrogens. Endocrinology 28(5):747–752
Garland T Jr, Kelly SA, Malisch JL, Kolb EM, Hannon RM, Keeney BK, Middleton KM (2011) How to run far: multiple solutions and sex-specific responses to selective breeding for high voluntary activity levels. Proc Biol Sci 278(1705):574–581. doi:10.1098/rspb.2010.1584
Karvat G, Kimchi T (2012) Systematic autistic-like behavioral phenotyping of 4 mouse strains using a novel wheel-running assay. Behav Brain Res 233(2):405–414. doi:10.1016/j.bbr.2012.05.028
Kelly SJ, Ostrowski NL, Wilson MA (1999) Gender differences in brain and behavior: hormonal and neural bases. Pharmacol Biochem Behav 64(4):655–664
Kent S, Hurd M, Satinoff E (1991) Interactions between body temperature and wheel running over the estrous cycle in rats. Physiol Behav 49(6):1079–1084
Lamberty Y, Gower AJ (1988) Investigation into sex-related differences in locomotor activity, place learning and passive avoidance responding in NMRI mice. Physiol Behav 44(6):787–790
Lenz KM, Nugent BM, McCarthy MM (2012) Sexual differentiation of the rodent brain: dogma and beyond. Front Neurosci 6:26. doi:10.3389/fnins.2012.00026
Mayer C, Acosta-Martinez M, Dubois SL, Wolfe A, Radovick S, Boehm U, Levine JE (2010) Timing and completion of puberty in female mice depend on estrogen receptor alpha-signaling in kisspeptin neurons. Proc Natl Acad Sci USA 107(52):22693–22698. doi:10.1073/pnas.1012406108
McCarthy MM, Arnold AP, Ball GF, Blaustein JD, De Vries GJ (2012) Sex differences in the brain: the not so inconvenient truth. J Neurosci 32(7):2241–2247. doi:10.1523/JNEUROSCI.5372-11.2012
Meaney MJ, Stewart J, Beatty WW (1985) Sex-differences in social play—the socialization of sex-roles. Adv Study Behav 15:1–58. doi:10.1016/S0065-3454(08)60486-6
Meziane H, Ouagazzal AM, Aubert L, Wietrzych M, Krezel W (2007) Estrous cycle effects on behavior of C57BL/6 J and BALB/cByJ female mice: implications for phenotyping strategies. Genes Brain Behav 6(2):192–200. doi:10.1111/j.1601-183X.2006.00249.x
Moldin SO, Rubenstein JLR (2006) Understanding autism: from basic neuroscience to treatment. Taylor and Francis, Boca Raton
National Research Council Committee for the Update of the Guide for the Care and Use of Laboratory Animals (2011) Guide for the care and use of laboratory animals. National Academies, Washington, DC
Nature (2010) Putting gender on the agenda (editorial). Nature 465:665. doi: 10.1038/465665a
Novak CM, Burghardt Paul R, Levine James A (2012) The use of a running wheel to measure activity in rodents: relationship to energy balance, general activity, and reward. Neurosci Biobehav Rev 36:1001–1014. doi:10.1016/j.neubiorev.2011.12.012
Oddi D, Crusio WE, D’Amato FR, Pietropaolo S (2013) Monogenic mouse models of social dysfunction: implications for autism. Behav Brain Res 251:75–84. doi:10.1016/j.bbr.2013.01.002
Phoenix CG, Gerall RW, Young WC AA (1959) Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65:369–382
Pinter O, Beda Z, Csaba Z, Gerendai I (2007) Differences in the onset of puberty in selected inbred mouse strains. In: 9th Eur Congr Endocrinology, Budapest, Hungary, 28 Apr–2 May 2007
Prendergast BJ, Onishi KG, Zucker I (2014) Female mice liberated for inclusion in neuroscience and biomedical research. Neurosci Biobehav Rev 40:1–5. doi:10.1016/j.neubiorev.2014.01.001
Rice WR (1988) Analyzing tables of statistical tests. Evolution 43(1):223–225
Silverman JL, Yang M, Lord C, Crawley JN (2010) Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci 11(7):490–502. doi:10.1038/nrn2851
Swallow JG, Carter PA, Garland T Jr (1998) Artificial selection for increased wheel-running behavior in house mice. Behav Genet 28(3):227–237
The Jackson Laboratory (2014) Body weight information—JAX® mice strain C57BL/6 J (000664). http://jaxmice.jax.org/strain/000664.html. Retrieved 14 Aug 2014
Werme M, Messer C, Olson L, Gilden L, Thoren P, Nestler EJ, Brene S (2002) Delta FosB regulates wheel running. J Neurosci 22(18):8133–8138
Acknowledgments
This work was supported by a Research and Creative Activities Grant, University of Louisville College of Arts and Sciences to EAG, an Intramural Research Incentive Grant, University of Louisville to CC, and an AREA award from the Kentucky Biomedical Research Infrastructure Network, which was funded by NIGMS grant #P20GM103436. We thank Sanaya Bamji, Dharti Patel and Kimberly Bencker for behavioral trials assistance, Dr. Manuel Casanova for helpful discussions, and Dr. Susanna Remold for help with the statistical analyses.
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Gordon, E.A., Corbitt, C. Investigation of prepubertal sex differences in wheel running and social behavior in three mouse strains. J Ethol 33, 177–187 (2015). https://doi.org/10.1007/s10164-015-0429-5
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DOI: https://doi.org/10.1007/s10164-015-0429-5