The overview shows that the scientific interest in social behaviour in mice has exponentially grown in the last two dec ades in parallel with advances in biotechnology and the emergence of genetically engineered mice. Most of the studies are psychopharmacological or look for the neurochemical bases of social behaviour and its alterations. However, the rol of social behaviour per se is increasing mainly in those research works aimed to model neuropsychiatric and neurode- generative diseases. In fact, at the translational level, the study of social behaviour in murine models is relevant because changes in social behaviour are present in most neuropsychiatric and neurodegenerative disorders as well as in other diseases that, directly or indirectly, affect the sphere of social relationships. The consideration of social behaviour in the experimental design of basic and translational research works using murine models may improve the predictive validity of new preventive and/or therapeutic strategies. The present work provides conceptual description of social behaviour in mice, the tests used to measure it and analyzes its increasing interest, mostly in the area of neuroscience. It reviews the 821 scientific studies (in English) included in the MEDLINE database from 1930 to December 2012. Keywords used for the search where those related to the different kinds of social behaviour (spontaneous or induced) in mice and took into account the diversity of experimental paradigms (dyads, groups, parental relationships, isolation) and the wide spectrum of behavioural tests available.
KeywordsSocial NeuroscienceAnimal ModelsBasic and Translational ResearchNeurodegenerative DiseasesNeuropsychiatric DisordersSocial Behaviour
H. J. Hedrich and G. R. Bulloch, “The Social Behaviour of Mice and Its Sensory Control,” The Handbook of Experimental Animals, The Laboratory Mice, Academic Press, London, 2004, pp. 287-298.
S. E. File, “The Use of Social Interaction as a Method for Detecting Anxiolytic Activity of Chlordiazepoxide-Like Drugs,” Journal of Neuroscience Methods, Vol. 2, No. 3, 1980, pp. 219-238. doi:10.1016/0165-0270(80)90012-6
M. B. Sokolowski, “Social Interactions in ‘Simple’ Model Systems,” Neuron, Vol. 65, No. 6, 2010, pp. 780-794. doi:10.1016/j.neuron.2010.03.007
I. Branchi, I. D’Andrea, F. Gracci, D. Santucci and E. Alleva, “Birth Spacing in the Mouse Communal Nest Shapes Adult Emotional and Social Behaviour,” Physiology & Behavior, Vol. 96, No. 4-5, 2009, pp. 532-539. doi:10.1016/j.physbeh.2008.12.003
L. Tremolizzo, M. Doueiri, E. Dong, D. R. Grayson, J. Davis and G. Pinna, “Valproate Corrects the Schizophrenia-Like Epigenetic Behavioural Modifications Induced by Methionine in Mice,” Biological Psychiatry, Vol. 57, No. 5, 2005, pp. 500-509. doi:10.1016/j.biopsych.2004.11.046
A. Venerosi, A. Valanzano, E. Alleva and G. Calamandrei, “Prenatal Exposure to Anti-HIV Drugs: Neurobehavioural Effects of Zidovudine (AZT) + Lamivudine (3TC) Treatment in Mice,” Teratology, Vol. 63, No. 1, 2001, pp. 26-37. doi:10.1002/1096-9926(200101)63:1 3.0.CO;2-G
J. N. Ferguson, J. M. Aldag, T. R. Insel and L. J. Young, “Oxytocin in the Medial Amygdala Is Essential for Social Recognition in the Mouse,” Journal of Neuroscience, Vol. 21, No. 20, 2001, pp. 8278-8285.
W. R. Holloway Jr. and D. H. Thor, “Social Memory Deficits in Adult Male Rats Exposed to Cadmium in Infancy,” Neurotoxicology and Teratology, Vol. 10, No. 3, 1988, pp. 193-197. doi:10.1016/0892-0362(88)90017-7
T. Spiteri, S. Musatov, S. Ogawa, A. Ribeiro, D. W. Pfaff and A. ?gmo, “The Role of the Estrogen Receptor α in the Medial Amygdala and Ventromedial Nucleus of the Hypothalamus in Social Recognition, Anxiety and Aggression,” Behavioural Brain Research, Vol. 210, No. 2, 2010, pp. 211-220. doi:10.1016/j.bbr.2010.02.033
R. M. Rodriguiz, R. Chu, M. G. Caron and W. C. Wetsel, “Aberrant Responses in Social Interaction of Dopamine Transporter Knockout Mice,” Behavioural Brain Research, Vol. 148, No. 1-2, 2004, pp. 185-198. doi:10.1016/S0166-4328(03)00187-6
B. Sobottka, F. Eggert, R. Ferstl and W. MullerRuchholtz, “Changed Chemosensory Identity Following Experimental Bone Marrow Transplantation: Recognition by Another Species,” Zeitschrift für Experimentelle und Angewandte Psychologie, Vol. 36, No. 4, 1989, pp. 654-664.
N. Lijam, R. Paylor, M. P. McDonald, J. N. Crawley, C. X. Deng and K. Herrup, “Social Interaction and Sensorimotor Gating Abnormalities in Mice Lacking Dvl1,” Cell, Vol. 90, No. 5, 1997, pp. 895-905. doi:10.1016/S0092-8674(00)80354-2
G. Lindzey, H. Winston and M. Manosevitz, “Social Dominance in Inbred Mouse Strains,” Nature, Vol. 191, 1961, pp. 474-476. doi:10.1038/191474a0
E. Strozik and M. F. Festing, “Whisker Trimming in Mice,” Laboratory Animals, Vol. 15, No. 4, 1981, pp. 309-312. doi:10.1258/002367781780953040
J. P. Garner, S. M. Weisker, B. Dufour and J. A. Mench, “Barbering (fur and Whisker Trimming) by Laboratory Mice as a Model of Human Trichotillomania and Obsessive-Compulsive Spectrum Disorders,” Comparative Medicine, Vol. 54, No. 2, 2004, pp. 216-224.
A. V. Kalueff, A. Minasyan, T. Keisala, Z. H. Shah and P. Tuohimaa, “Hair Barbering in Mice: Implications for Neurobehavioural Research,” Behavioural Processes, Vol. 71, No. 1, 2006, pp. 8-15. doi:10.1016/j.beproc.2005.09.004
S. Y. Long, “Hair-Nibbling and Whisker-Trimming as Indicators of Social Hierarchy in Mice,” Animal Behaviour, Vol. 20, No. 1, 1972, pp. 10-12. doi:10.1016/S0003-3472(72)80167-2
H. K. Caldwell, O. E. Dike, E. L. Stevenson, K. Storck and W. S. Young III, “Social Dominance in Male Vasopressin 1b Receptor Knockout Mice,” Hormones and Behavior, Vol. 58, No. 2, 2010, pp. 257-263. doi:10.1016/j.yhbeh.2010.03.008
J. Uhrich, “The Social Hierarchy in Albino Mice,” Journal of Comparative Psychology, Vol. 25, No. 2, 1938, pp. 373-413. doi:10.1037/h0056350
T. E. McGill, “Sexual Behaviour in Three Inbred Strains of Mice,” Behaviour, Vol. 19, No. 4, 1962, pp. 341-350. doi:10.1163/156853962X00087
D. W. Mosig and D. A. Dewsbury, “Studies of the Copulatory Behaviour of House Mice (Mus musculus),” Behavioral Biology, Vol. 16, No. 4, 1976, pp. 463-473. doi:10.1016/S0091-6773(76)91635-7
E. F. Rissman, A. H. Early, J. A. Taylor, K. S. Korach and D. B. Lubahn, “Estrogen Receptors Are Essential for Female Sexual Receptivity,” Endocrinology, Vol. 138, No. 1, 1997, pp. 507-510. doi:10.1210/en.138.1.507
C. Cohen-Salmon, M. Carlier, P. Roubertoux, J. Jouhaneau, C. Semal and M. Paillette, “Differences in Patterns of Pup Care in Mice V—Pup Ultrasonic Emissions and Pup Care Behaviour,” Physiology & Behavior, Vol. 35, No. 2, 1985, pp. 167-174. doi:10.1016/0031-9384(85)90331-2
K. Nishimori, L. J. Young, Q. Guo, Z. Wang, T. R. Insel and M. M. Matzuk, “Oxytocin Is Required for Nursing but Is Not Essential for Parturition or Reproductive Behaviour,” Proceedings of the National Academy of Sciences of USA, Vol. 93, No. 21, 1996, pp. 11699-11704. doi:10.1073/pnas.93.21.11699
R. M. J. Deacon, L. L. Cholerton, K. Talbot, R. NairRoberts, D. J. Sanderson and C. Romberg, “Age-Dependent and -Independent Behavioural Deficits in Tg2576 Mice,” Behavioural Brain Research, Vol. 189, No. 1, 2008, pp. 126-138. doi:10.1016/j.bbr.2007.12.024
R. Deacon, “Assessing Burrowing, Nest Construction, and Hoarding in Mice,” Journal of Visualized Experiments, Vol. 59, 2012, e2607.
E. Giacalone, M. Tansella, L. Valzelli and S. Garattini, “Brain Serotonin Metabolism in Isolated Aggressive Mice,” Biochemical Pharmacology, Vol. 17, No. 7, 1968, pp. 1315-1327. doi:10.1016/0006-2952(68)90069-5
J. P. Scott, “Agonistic Behaviour of Mice and Rats: A Review,” American Zoologist, Vol. 6, No. 4, 1966, pp. 683-701.
J. N. Crawley and R. Paylor, “A Proposed Test Battery and Constellations of Specific Behavioural Paradigms to Investigate the Behavioural Phenotypes of Transgenic and Knockout Mice,” Hormones and Behavior, Vol. 31, No. 3, 1997, pp. 197-211. doi:10.1006/hbeh.1997.1382
J. N. Crawley, W. M. Schleidt and J. F. Contrera, Does social environment decrease propensity to fight in male mice? Behavioral Biology, Vol. 15, No. 1, 1975, pp. 73-83. doi:10.1016/S0091-6773(75)92105-7
K. A. Miczek, E. Weerts, M. Haney and J. Tidey, “Neurobiological Mechanisms Controlling Aggression: Preclinical Developments for Pharmacotherapeutic Interventions,” Neuroscience & Biobehavioral Reviews, Vol. 18, No. 1, 1994, pp. 97-110. doi:10.1016/0149-7634(94)90040-X
S. E. Jones and P. F. Brain, “Performances of Inbred and Outbred Laboratory Mice in Putative Tests of Aggression,” Behavior Genetics, Vol. 17, No. 1, 1987, pp. 87-96. doi:10.1007/BF01066013
P. Moretti, J. A. Bouwknecht, R. Teague, R. Paylor and H. Y. Zoghbi, “Abnormalities of Social Interactions and Home-Cage Behaviour in a Mouse Model of Rett Syndrome,” Human Molecular Genetics, Vol. 14, No. 2, 2005, pp. 205-220. doi:10.1093/hmg/ddi016
R. J. Nelson, G. E. Demas, P. L. Huang, M. C. Fishman, V. L. Dawson and T. M. Dawson, “Behavioural Abnormalities in Male Mice Lacking Neuronal Nitric Oxide Synthase,” Nature, Vol. 378, 1995, pp. 383-386. doi:10.1038/378383a0
R. Avitsur, S. G. Kinsey, K. Bidor, M. T. Bailey, D. A. Padgett and J. F. Sheridan, “Subordinate Social Status Modulates the Vulnerability to the Immunological Effects of Social Stress,” Psychoneuroendocrinology, Vol. 32, No. 8-10, 2007, pp. 1097-1105. doi:10.1016/j.psyneuen.2007.09.005
R. Avitsur, J. L. Stark and J. F. Sheridan, “Social Stress Induces Glucocorticoid Resistance in Subordinate Animals,” Hormones and Behavior, Vol. 39, No. 4, 2001, pp. 247-257. doi:10.1006/hbeh.2001.1653
R. C. La Barba, J. Martini and J. White, “The Effect of Maternal-Separation on the Growth of Ehrlich Carcinoma in the Balb-c Mouse,” Psychosomatic Medicine, Vol. 31, No. 2, 1969, pp. 129-133.
R. D. Romeo, A. Mueller, H. M. Sisti, S. Ogawa, B. S. McEwen and W. G. Brake, “Anxiety and Fear Behaviours in Adult Male and Female C57BL/6 Mice Are Modulated by Maternal Separation,” Hormones and Behavior, Vol. 43, No. 5, 2003, pp. 561-567. doi:10.1016/S0018-506X(03)00063-1
J. H. Van Heerden, V. Russell, A. Korff, D. J. Stein and N. Illing, “Evaluating the Behavioural Consequences of Early Maternal Separation in Adult C57BL/6 Mice: The Importance of Time,” Behavioural Brain Research, Vol. 207, No. 2, 2010, pp. 332-342. doi:10.1016/j.bbr.2009.10.015
J. B. Panksepp and G. P Lahvis, “Social Reward among Juvenile Mice,” Genes, Brain and Behavior, Vol. 6,No. 7, 2007, pp. 661-671. doi:10.1111/j.1601-183X.2006.00295.x
C. Rondinini, A. Venerosi, I. Branchi, G. Calamandrei and E. Alleva, “Long-Term Effects of Prenatal 3’-Azido3’-Deoxythymidine (AZT) Exposure on Intermale Aggressive Behaviour of Mice,” Psychopharmacology, Vol. 45, No. 3, 1999, pp. 317-323. doi:10.1007/s002130051064
L. J. Keeling and H. W. Gonyou, “Social Behaviour in Farm Animals,” CABI Publishing, London, 2001. doi:10.1079/9780851993973.0000
M. L. Terranova and G. Laviola, “Delta-Opioid Modulation of Social Interactions in Juvenile Mice Weaned at Different Ages,” Physiology & Behavior, Vol. 73, No. 3, 2001, pp. 393-400. doi:10.1016/S0031-9384(01)00447-4
T. Miyakawa, M. Yamada, A. Duttaroy and J. Wess, “Hyperactivity and Intact Hippocampus-Dependent Learning in Mice Lacking the M1 Muscarinic Acetylcholine Receptor,” Journal of Neuroscience, Vol. 21, No. 14, 2001, pp. 5239-5250.
T. Ishihama, Y. Ago, N. Shintani, H. Hashimoto, A. Baba and K. Takuma, “Environmental Factors during Early Developmental Period Influence Psychobehavioural Abnormalities in Adult PACAP-Deficient Mice,” Behavioural Brain Research, Vol. 209, No. 2, 2010, pp. 274-280. doi:10.1016/j.bbr.2010.02.009
C. M. Spencer, O. Alekseyenko, E. Serysheva, L. YuvaPaylor and R. Paylor, “Altered Anxiety-Related and Social Behaviours in the Fmr1 Knockout Mouse Model of Fragile X Syndrome,” Genes, Brain and Behavior, Vol. 4, No. 7, 2005, pp. 420-430. doi:10.1111/j.1601-183X.2005.00123.x
M. A. Mines, C. J. Yuskaitis, M. K. King, E. Beurel and R. S. Jope, “GSK3 Influences Social Preference and Anxiety-Related Behaviours during Social Interaction in a Mouse Model of Fragile X Syndrome and Autism,” PLoS One, Vol. 5, No. 3, 2010, e9706. doi:10.1371/journal.pone.0009706
L. H. Turner, C. E. Lim and S. C. Heinrichs, “Antisocial and Seizure Susceptibility Phenotypes in an Animal Model of Epilepsy Are Normalized by Impairment of Brain Corticotropin-Releasing Factor,” Epilepsy & Behavior, Vol. 10, No. 1, 2007, pp. 8-15. doi:10.1016/j.yebeh.2006.08.013
A. Siegmund and C. T. Wotjak, “A Mouse Model of Posttraumatic Stress Disorder That Distinguishes between Conditioned and Sensitised Fear,” Journal of Psychiatric Research, Vol. 41, No. 10, 2007, pp. 848-860. doi:10.1016/j.jpsychires.2006.07.017
C. Zanettini, V. Carola, L. Lo Iacono, A. Moles, C. Gross and F. R. D’Amato, “Postnatal Handling Reverses Social Anxiety in Serotonin Receptor 1A Knockout Mice,” Genes, Brain and Behavior, Vol. 9, No. 1, 2010, pp. 26-32. doi:10.1111/j.1601-183X.2009.00531.x
H. Tsunekawa, Y. Noda, M. Miyazaki, F. Yoneda, T. Nabeshima and D. Wang, “Effects of (R)-(-)-1-(benzofuran-2-yl)-2-propylaminopentane Hydrochloride [(-)-BPAP] in Animal Models of Mood Disorders,” Behavioural Brain Research, Vol. 189, No. 1, 2008, pp. 107-116. doi:10.1016/j.bbr.2007.12.016
D. K. Pandey, R. Mahesh, A. A. Kumar, V. S. Rao, M. Arjun and R. Rajkumar, “A Novel 5-HT(2A) Receptor Antagonist Exhibits Antidepressant-Like Effects in a Battery of Rodent Behavioural Assays: Approaching EarlyOnset Antidepressants,” Pharmacology Biochemistry and Behavior, Vol. 94, No. 3, 2010, pp. 363-373. doi:10.1016/j.pbb.2009.09.018
M. Filali and R. Lalonde, “Age-Related Cognitive Decline and Nesting Behaviour in an APPswe/PS1 Bigenic Model of Alzheimer’s Disease,” Brain Research, Vol. 2009, pp. 1292:93-99. doi:10.1016/j.brainres.2009.07.066
M. Filali, R. Lalonde and S. Rivest, “Anomalies in Social Behaviors and Exploratory Activities in an APPswe/PS1 Mouse Model of Alzheimer’s Disease,” Physiology & Behavior, Vol. 104, No. 5, 2011, pp. 880-885. doi:10.1016/j.physbeh.2011.05.023
M. Filali and R. Lalonde, “The Effects of Subchronic D-Serine on Left-Right Discrimination Learning, Social Interaction, and Exploratory Activity in APPswe/PS1 Mice,” European Journal of Pharmacology, 2012, in Press.
S. Pietropaolo, P. Delage, F. Lebreton, W. E. Crusio and Y. H. Cho, “Early Development of Social Deficits in APP and APP-PS1 Mice,” Neurobiology of Aging, Vol. 33, No. 1002, 2012, pp. e17-e27.
S. S. Moy, J. J. Nadler, N. B. Young, R. J. Nonneman, S. K. Segall and G. M. Andrade, “Social Approach and Repetitive Behaviour in Eleven Inbred Mouse Strains,” Behavioural Brain Research, Vol. 191, No. 1, 2008, pp. 118-129. doi:10.1016/j.bbr.2008.03.015
C. L. Yochum, P. Bhattacharya, L. Patti, O. Mirochnitchenko and G. C. Wagner, “Animal Model of Autism Using GSTM1 Knockout Mice and Early Post-Natal Sodium Valproate Treatment,” Behavioural Brain Research, Vol. 210, No. 2, 2010, pp. 202-210. doi:10.1016/j.bbr.2010.02.032
K. Karelina, G. J. Norman, N. Zhang and A. C. DeVries, “Social Contact Influences Histological and Behavioural Outcomes Following Cerebral Ischemia,” Experimental Neurology, Vol. 220, No. 2, 2009, pp. 276-282. doi:10.1016/j.expneurol.2009.08.022
J. B. Williams, D. Pang, B. Delgado, M. Kocherginsky, M. Tretiakova and T. Krausz, “A Model of Gene-Environment Interaction Reveals Altered Mammary Gland Gene Expression and Increased Tumor Growth Following Social Isolation,” Cancer Prevention Research, Vol. 2, 2009, pp. 850-861. doi:10.1158/1940-6207.CAPR-08-0238
V. J. Bolivar, S. R. Walters and J. L. Phoenix, “Assessing Autism-Like Behaviour in Mice: Variations in Social Interactions among Inbred Strains,” Behavioural Brain Research, Vol. 176, No. 1, 2007, pp. 21-26. doi:10.1016/j.bbr.2006.09.007
J. M. Ho, J. H. Murray, G. E. Demas and J. L. Goodson, “Vasopressin Cell Groups Exhibit Strongly Divergent Responses to Copulation and Male-Male Interactions in Mice,” Hormones and Behavior, Vol. 58, No. 3, 2010, pp. 368-377. doi:10.1016/j.yhbeh.2010.03.021
C. E. Kovacsics and T. D. Gould, “Shock-induced Aggression in Mice Is Modified by Lithium,” Pharmacology Biochemistry and Behavio, Vol. 94, No. 3, 2010, pp. 380-386. doi:10.1016/j.pbb.2009.09.020
V. M. Linck, A. L. da Silva, M. Figueiró, E. B. Caram?o, P. R. H. Moreno and E. Elisabetsky, “Effects of Inhaled Linalool in Anxiety, Social Interaction and Aggressive Behaviour in Mice,” Phytomedicine, Vol. 17, 2010, pp. 679-683. doi:10.1016/j.phymed.2009.10.002
J. L. Gariépy, P. L. Gendreau, R. B. Cairns and M. H. Lewis, “D1 Dopamine Receptors and the Reversal of Isolation-Induced Behaviours in Mice,” Behavioural Brain Research, Vol. 95, No. 1, 1998, pp. 103-111. doi:10.1016/S0166-4328(97)00215-5
T. Miyakawa, L. M. Leiter, D. J. Gerber, R. R. Gainetdinov, T. D. Sotnikova and H. Zeng, “Conditional Calcineurin Knockout Mice Exhibit Multiple Abnormal Behaviours Related to Schizophrenia,” Proceedings of the National Academy of Sciences of USA, Vol. 100, No. 15, 2003, pp. 8987-8992. doi:10.1073/pnas.1432926100
Z. Callaerts-Vegh, T. Beckers, S. M. Ball, F. Baeyens, P. F. Callaerts and J. F. Cryan, “Concomitant Deficits in Working Memory and Fear Extinction Are Functionally Dissociated from Reduced Anxiety in Metabotropic Glutamate Receptor 7-Deficient Mice,” Journal of Neuroscience, Vol. 26, No. 24, 2006, pp. 6573-6582. doi:10.1523/JNEUROSCI.1497-06.2006
T. Maekawa, S. Kim, D. Nakai, C. Makino, T. Takagi and H. Ogura, “Social Isolation Stress Induces ATF-7 Phosphorylation and Impairs Silencing of the 5-HT 5B Receptor Gene,” EMBO Journal, Vol. 29, 2010, pp. 196-208. doi:10.1038/emboj.2009.318