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Stereotypic mice are aggressed by their cage-mates, and tend to be poor demonstrators in social learning tasks

Published online by Cambridge University Press:  01 January 2023

L Harper
Affiliation:
Department of Animal Biosciences, University of Guelph, Guelph, ON N1G 2W1, Canada
E Choleris
Affiliation:
Department of Animal Biosciences, University of Guelph, Guelph, ON N1G 2W1, Canada
K Ervin
Affiliation:
Department of Psychology, University of Guelph, Guelph, ON, Canada
C Fureix
Affiliation:
Department of Animal Biosciences, University of Guelph, Guelph, ON N1G 2W1, Canada Department of Molecular & Cellular Biology, University of Guelph, Guelph, ON, Canada
K Reynold
Affiliation:
Department of Animal Husbandry, University of Bristol, Langford, UK
M Walker
Affiliation:
Department of Animal Biosciences, University of Guelph, Guelph, ON N1G 2W1, Canada
G Mason*
Affiliation:
Department of Animal Biosciences, University of Guelph, Guelph, ON N1G 2W1, Canada
*
* Contact for correspondence and requests for reprints: gmason@uoguelph.ca

Abstract

Stereotypic behaviours (SBs) are linked with behavioural inflexibility and resemble symptoms of autism, suggesting that stereotypic animals could have autistic-like social impairments. SBs are also common in caged mice. We therefore hypothesised relationships between stereotypic and social behaviours, predicting that highly stereotypic mice would give/receive more agonism and be less effective in social learning tasks. Experiment One used C57BL/6 and DBA/2 mice in non-enriched or enriched housing (15 cages each); Experiment Two, more cages (six non-enriched, 44 enriched) plus a third strain (BALB/c). Across both experiments, enrichment reduced SB and agonism (aggression, plus ‘displacements’ where one mouse supplants another at a resource). These effects appeared related: housing effects on agonism became negligible when SB was statistically controlled for, and, at least in enriched cages, SB covaried with receiving aggression. In Experiment Three, 20 DBAs varying in SB from Experiment Two acted as demonstrators in a ‘social transmission of food preferences’ task. They were fed a novel flavour (shatavari powder), then each mingled with a familiar but flavour-naïve C57 observer. Observers were subsequently offered two novel flavours: shatavari or marjoram. Those spontaneously choosing more shatavari (n = 10) tended to have had less stereotypic demonstrators than the other ten observer mice. Overall, highly stereotypic mice thus received more agonism — an effect with obvious welfare implications that can be reduced with enrichment — and seemed potentially less effective at inducing flavour preferences in conspecifics. Such effects are consistent with social impairment, suggesting that reducing SB may perhaps enhance interactions between conspecifics.

Type
Research Article
Copyright
© 2015 Universities Federation for Animal Welfare

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References

Akre, AKM, Bakken, M, Hovland, AL, Palme, R and Mason, G 2011 Clustered environmental enrichments induce more aggression and stereotypic behavior than do dispersed enrich-ments in female mice. Applied Animal Behaviour Science 131: 145152. http://dx.doi.org/10.1016/j.applanim.2011.01.010CrossRefGoogle Scholar
Bartolomucci, A, Palanza, P, Sacerdote, P, Panerai, AE, Sgoifo, A, Dantzer, R and Parmigiani, S 2005 Social factors and individual vulnerability to chronic stress exposure. Neuroscience & Biobehavioral Reviews 29: 6781. http://dx.doi.org/10.1016/j.neubiorev.2004.06.009CrossRefGoogle ScholarPubMed
Campbell, DLM, Dallaire, JA and Mason, GJ 2013 Environmentally enriched rearing environments reduce repetitive perseveration in caged mink, but increase spontaneous alteration. Behavioural Brain Research 239: 177187. http://dx.doi.org/10.1016/j.bbr.2012.11.004CrossRefGoogle Scholar
Choleris, E, Clipperton-Allen, AE, Gray, DG, Diaz-Gonzalez, S and Welsman, RG 2011 Differential effects of dopamine receptor D1-type and D2-type antagonists and phase of the estrous cycle on social learning of food preferences, feeding, and social interactions in mice. Neuropsychopharmacology 36:16891702. http://dx.doi.org/10.1038/npp.2011.50CrossRefGoogle ScholarPubMed
Choleris, E, Guo, C, Liu, H, Mainardi, M and Valsecchi, P 1997 The effect of demonstrator age and number on duration of socially-induced food preferences in house mouse (Mus domesti-cus). Behavioural Processes 41: 6977. http://dx.doi.org/10.1016/S 0376-6357(97)00029-6CrossRefGoogle Scholar
Clipperton, AE, Spinato, JM, Chernets, C, Pfaff, DW and Choleris, E 2008 Differential effects of estrogen receptor alpha and beta specific agonists on social learning of food preferences in female mice. Neuropsychopharmacology 33: 23622375. http://dx.doi.org/10.1038/sj.npp.1301625CrossRefGoogle ScholarPubMed
Clipperton-Allen, AE, Almey, A, Melichercik, A, Allen, CP and Choleris, E 2011 Effects of an estrogen receptor alpha ago-nist on agonistic behaviour in intact and gonadectomized male and female mice. Psychoneuroendocrinology 36: 981995. http://dx.doi.or g/10.1016/j.psyneuen.2010.12.010CrossRefGoogle ScholarPubMed
Dallaire, JA, Meagher, RK, Díez-León, M, Garner, JP and Mason, GJ 2011 Recurrent perseveration correlates with abnor-mal repetitive locomotion in mink but is not reduced by environ-mental enrichment. Behavioural Brain Research 224: 213222. http://dx.doi.org/10.1016/j.bbr.2011.03.061CrossRefGoogle Scholar
Díez-León, M, Bowman, J, Bursian, S, Filion, H, Galicia, D, Kanefsky, J, Napolitano, A, Palme, R, Schulte-Hostedde, A, Scribner, K and Mason, GJ 2013 Environmentally enriched male mink gain more copulations than stereotypic, barren-reared competi-tors. PLoS One 8: 111. http://dx.doi.org/10.1371/journal.pone.0080494CrossRefGoogle Scholar
Díez-León, M and Mason, GJ Effects of environmental enrich-ment on aspects of maternal behavior, and infant growth and sur-vival, in a model carnivore species, the American mink (Neovison vison). Zoo Biology, in pressGoogle Scholar
Doncaster, CP and Davey, AJH 2007 Analysis of Variance and Covariance. How to Choose and Construct Models for the Life Sciences. Cambridge University Press: Cambridge, UK. http://dx.doi.org/10.1017/CBO9780511611377CrossRefGoogle Scholar
Galef, BG 2001 Social influences on food choices of Norway rats and mate choices of Japanese quail. International Journal of Comparative Psychology 14: 124CrossRefGoogle Scholar
Galef, BG, Rudolf, B, Whiskin, EE, Choleris, E, Mainardi, M and Valsecchi, P 1998 Familiarity and relatedness: effects on social learning about foods by Norway rats and Mongolian gerbils. Animal Learning & Behavior 26: 448454. http://dx.doi.org/10.3758/BF03199238CrossRefGoogle Scholar
Galef, BG and Wigmore, SW 1983 Transfer of information concerning distant food: a laboratory investigation of the ‘infor-mation-centre’ hypothesis. Animal Behaviour 31: 748758. http://dx.doi.org/10.1016/S0003-3472(83)80232-2CrossRefGoogle Scholar
Garner, JP and Mason, GJ 2002 Evidence for a relationship between cage stereotypies and behavioural disinhibition in labora-tory rodents. Behavioural Brain Research 136: 8392. http://dx.doi.org/10.1016/S0166-4328(02)00111-0CrossRefGoogle Scholar
Garner, JP, Thogerson, CM, Dufour, BD, Würbel, H, Murray, JD and Mench, JA 2011 Reverse-translational biomark-er validation of Abnormal Repetitive Behaviours in mice: An illus-tration of the 4P's modelling approach. Behavioural Brain Research 219: 189196. http://dx.doi.org/10.1016/j.bbr.2011.01.002CrossRefGoogle Scholar
Grafen, A and Hails, R 2002 Modern Statistics for the Life Sciences. Oxford University Press: New York, USAGoogle Scholar
Grant, EC and Mackintosh, JH 1963 A comparison of the social postures of some common laboratory rodents. Behaviour 21: 246259. http://dx.doi.org/10.1163/156853963X00185Google Scholar
Honess, PE and Marin, CM 2006 Enrichment and aggression in primates. Neuroscience and Biobehavioural Reviews 30: 413436. http://dx.doi.org/10.1016/j.neubiorev.2005.05.002CrossRefGoogle ScholarPubMed
Jones, MA, Mason, GJ and Pillay, N 2011 Correlates of birth origin effects on the development of stereotypic behaviour in striped mice Rhabdomys. Animal Behaviour 82: 149159. http://dx.doi.org/10.1016/j.anbehav.2011.04.010CrossRefGoogle Scholar
Kavaliers, M, Choleris, E and Colwell, DD 2001 Learning from others to cope with biting flies: Social learning of fear-induced con-ditioned analgesia and active avoidance. Behavioural Neuroscience 115:661674. http://dx.doi.org/10.1037/0735-7044.115.3.661CrossRefGoogle Scholar
Kavaliers, M, Colwell, DD and Choleris, E 2005 Kinship, famil-iarity and social status modulate social learning about “micropreda-tors” (biting flies) in deer mice. Behavioural Ecology and Sociobiology 58: 6071. http://dx.doi.org/10.1007/s00265-004-0896-0CrossRefGoogle Scholar
Lam, KSL, Bodfish, JW and Piven, J 2008 Evidence for three subtypes of repetitive behaviour in autism that differ in familiality and association with other symptoms. The Journal of Child Psychology and Psychiatry 49: 11931200. http://dx.doi.org/10.1111/j.1469-7610.2008.01944.xCrossRefGoogle ScholarPubMed
Lopez, BR, Lincoln, AJ, Ozonoff, S and Lai, Z 2005 Examining the relationship between executive function and restricted, repet-itive symptoms of autistic disorder. Journal of Autism and Developmental Disorders 35: 445460. http://dx.doi.org/10.1007/s10803-005-5035-xCrossRefGoogle ScholarPubMed
Lumley, LA, Charles, RF, Charles, RC, Hebert, MA, Morton, DM and Meyerhoff, JL 2000 Effects of social defeat and of diazepam on behaviour in a resident-intruder test in male DBA/2 mice. Pharmacology, Biochemistry and Behaviour 67: 433447. http://dx.doi.org/10.1016/S0091-3057(00)00382-8CrossRefGoogle Scholar
Márquez-Arias, A, Santillán-Doherty, AM, Arenas-Rosas, RV, Gasca-Matías, MP and Muñoz-Delgado, J 2010 Environmental enrichment for captive stumptail macaques (Macaca arctoides). Journal of Medical Primatology 39: 3240. http://dx.doi.org/10.1111/j.1600-0684.2009.00392.xCrossRefGoogle ScholarPubMed
Martin, P and Bateson, PPG 1993 Measuring Behaviour: An Introductory Guide. Cambridge University Press: Cambridge, UK. http://dx.doi.org/10.1017/CBO9781139168342CrossRefGoogle Scholar
Mason, GJ and Latham, NR 2004 Can't stop, won't stop: is stereo-typy a reliable animal welfare indicator? Animal Welfare 13: 5769Google Scholar
McEvoy, RE, Rogers, SJ and Pennington, BF 1993 Executive function and social communication deficits in young autistic chil-dren. Journal of Child Psychology and Psychiatry 34: 563578. http://dx.doi.org/10.1111/j.1469-7610.1993.tb01036.xCrossRefGoogle Scholar
Meagher, RK and Mason, GJ 2012 Environmental enrichment reduces signs of boredom in caged mink. PLoS One 7: 110. http://dx.doi.org/10.1371/journal.pone.0049180CrossRefGoogle ScholarPubMed
Memari, AH, Ziaee, V, Shayestehfar, M, Ghanouni, P, Mansournia, MA and Moshayedi, P 2013 Cognitive flexibil-ity impairments in children with autism spectrum disorders: Links to age, gender and child outcomes. Research in Developmental Disabilities 34: 32183225. http://dx.doi.org/10.1016/j.ridd.2013.06.033CrossRefGoogle Scholar
Morley-Fletcher, S, Rea, M, Maccari, S and Laviola, G 2003 Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactiv-ity in rats. European Journal of Neuroscience 18: 33673374. http://dx.doi.org/10.1111/j.1460-9568.2003.03070.xCrossRefGoogle ScholarPubMed
National Centre for the Replacement, Refinement, and Reduction of Animals in Research (NC3Rs) 2015 The 3Rs. https://www.nc3rs.org.uk/the-3rs#What%20are%20the%203Rs?Google Scholar
Papini, MR 2003 Comparative psychology of surprising non-reward. Brain, Behavior and Evolution 62: 8395. http://dx.doi.org/10.1159/000072439CrossRefGoogle Scholar
Patterson, PH 2011 Modeling autistic features in animals. Pediatric Research 69: 34R40R. http://dx.doi.org/10.1203/PD R.0b013e318212b80fCrossRefGoogle ScholarPubMed
Rasch, D and Guiard, V 2004 The robustness of parametric sta-tistical methods. Psychology Science 46: 175208Google Scholar
Rodriguiz, RM, Chu, R, Caron, MG and Wetsel, WC 2004 Aberrant responses in social interaction of dopamine transporter knockout mice. Behavioural Brain Research 148: 185198. http://dx.doi.org/10.1016/S0166-4328(03)00187-6CrossRefGoogle ScholarPubMed
Ryan, BC, Young, NB, Moy, SS and Crawley, JN 2008 Olfactory cues are sufficient to elicit social approach behaviours but not social transmission of food preference in C57BL/6J mice. Behavioural Brain Research 193: 235242. http://dx.doi.org/10.1016/j.bbr.2008.06.002CrossRefGoogle Scholar
Rymer, T, Schradin, C and Pillay, N 2008 Social transmission of information about novel food in two populations of the African striped mouse, Rhabdomys pumilio. Animal Behaviour 76: 1297-1303. http://dx.doi.org/10.1016/j.anbehav.2008.06.014CrossRefGoogle Scholar
Schaefer, AL, Salomons, MO, Tong, AKW, Sather, AP and Lepage, P 1990 The effect of environment enrichment on aggression in newly weaned pigs. Applied Animal Behaviour Science 27: 4152. http://dx.doi.org/10.1016/0168-1591(90)90006-YCrossRefGoogle Scholar
Silverman, JL, Yang, M, Lord, C and Crawley, JN 2010 Behavioural phenotyping assays for mouse models of autism. Nature Reviews Neuroscience 11: 490502. http://dx.doi.org/10.1038/nrn2851CrossRefGoogle ScholarPubMed
Simpson, J and Kelly, JP 2011 The impact of environmental enrichment in laboratory rats. Behavioural and neurochemical aspects. Behavioural Brain Research 222: 246264. http://dx.doi.org/10.1016/j.bbr.2011.04.002CrossRefGoogle ScholarPubMed
Sørenson, G 1987 Stereotyped behaviour, hyperaggressiveness and “tyrannic” hierarchy induced in bank voles (Clethrionomys glareolus) by a restricted cage milieu. Progress in Neuropsychopharmacology and Biological Psychiatry 11: 921. http://dx.doi.org/10.1016/0278-5846(87)90027-3CrossRefGoogle Scholar
Tanimura, Y, King, MA, Williams, DK and Lewis, MH 2011 Development of repetitive behaviour in a mouse model: Roles of indirect and striosomal basal ganglia pathways. International Journal of Developmental Neuroscience 29: 461467. http://dx.doi.org/10.1016/j.ijdevneu.2011.02.004CrossRefGoogle Scholar
Tanimura, Y, Yang, MC and Lewis, MH 2008 Procedural learning and cognitive flexibility in a mouse model of restricted, repetitive behaviour. Behavioural Brain Research 189: 250256. http://dx.doi.org/10.1016/j.bbr.2008.01.001CrossRefGoogle Scholar
Tilly, SC, Dallaire, J and Mason, GJ 2010 Middle-aged mice with enrichment-resistant stereotypic behaviour show reduced moti-vation for enrichment. Animal Behaviour 80: 363373. http://dx.doi.org/10.1016/j.anbehav.2010.06.008CrossRefGoogle Scholar
Turner, PV, Wozniak, L, Batista, L, Ovari, J, Clipperton-Allen, AE, Hammermueller, J, Ingrao, JN, Bienzle, D and Choleris, E Long term provision of environmental resources alters behaviour but not physiology or neuroanatomy of male and female BALB/c and C57BL/6 mice. The Journal of the American Association for Laboratory Animal Science, in pressGoogle Scholar
Valsecchi, P, Choleris, E, Moles, A, Guo, C and Mainardi, M 1996 Kinship and familiarity as factors affecting social transfer of food preferences in adult Mongolian gerbils (Meriones unguicula-tus). Journal of Comparative Psychology 110: 243251. http://dx.doi.org/10.1037/0735-7036.110.3.243CrossRefGoogle Scholar
Valsecchi, P and Galef, BG 1989 Social influences on the food preferences of house mice (Mus musculus). The International Journal of Comparative Psychology 2: 245256CrossRefGoogle Scholar
Valsecchi, P, Mainardi, M, Sgoifo, A and Taticchi, A 1989 Maternal influences on food preferences in weanling mice Mus domesticus. Behavioural Processes 19: 155166. http://dx.doi.org/10.1016/0376-6357(89)90038-7CrossRefGoogle ScholarPubMed
Van Loo, PLP, Kruitwagen, CLJJ, Koolhaas, JM, Van de Weerd, HA, Van Zutphen, LFM and Baumans, V 2002 Influence of cage enrichment on aggressive behaviour and physio-logical parameters in male mice. Applied Animal Behaviour Science 76: 6581. http://dx.doi.org/10.1016/S0168-1591(01)00200-3CrossRefGoogle Scholar
Walker, M, Fureix, C, Palme, R and Mason, G 2013 Co-housing rodents with different coat colours as a simple, non-Invasive means of individual identification: Validating mixed-strain housing for C57BL/6 and DBA/2 mice. PLoS One 8(10): e77541. http://dx.doi.org/10.1371/journal.pone.0077541CrossRefGoogle ScholarPubMed
Warne, MC 1947 A time analysis of certain aspects of the behav-ior of small groups of caged mice. Journal of Comparative and Physiological Psychology 40: 371. http://dx.doi.org/10.1037/h0060816CrossRefGoogle Scholar
Whitaker, J, Moy, SS, Godfrey, V, Nielsen, J, Bellinger, D and Bradfield, J 2009 Effects of cage size and enrichment on repro-ductive performance and behaviour in C57BL/6Tac mice. Lab Animal 38: 2434. http://dx.doi.org/10.1038/laban0109-24CrossRefGoogle Scholar