Social approach behaviors are similar on conventional versus reverse lighting cycles, and in replications across cohorts, in BTBR T+ tf/J, C57BL/6J, and vasopressin receptor 1B mutant mice
Open accessAbstract
Mice are a nocturnal species, whose social behaviors occur primarily during the dark phase of the circadian cycle. However, laboratory rodents are frequently tested during their light phase, for practical reasons. We investigated the question of whether light phase testing presents a methodological pitfall for investigating mouse social approach behaviors. Three lines of mice were systematically compared. One cohort of each line was raised in a conventional lighting schedule and tested during the light phase, under white light illumination; another cohort was raised in a reverse lighting schedule and tested during their dark phase, under dim red light. Male C57BL/6J (B6) displayed high levels of sociability in our three-chambered automated social approach task when tested in either phase. BTBR T+ tf/J (BTBR) displayed low levels of sociability in either phase. Five cohorts of vasopressin receptor subtype 1b (Avpr1b) null mutants, heterozygotes, and wildtype littermate controls were tested in the same social approach paradigm: three in the dark phase and two in the light phase. All three genotypes displayed normal sociability in four out of the five replications. In the juvenile play test, testing phase had no effect on play soliciting behaviors in Avpr1b mice, but had modest effects on nose sniff and huddling. Taken together, these findings indicate that testing phase is not a crucial factor for studying some forms of social approach in juvenile and adult mice.
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BTBR T+tf/J mice display behavioral phenotypes relevant to all three diagnostic symptoms of autism.
“BTBR T+tf/J (BTBR) is a commercially available inbred strain of mouse that displays behavioral phenotypes relevant to all three diagnostic symptoms of autism (60–62, 64, 66, 68–70, 72, 74–78).”
From Negative allosteric modulation of the mGluR5 receptor reduces repetitive behaviors and rescues social deficits in mouse models of autism (2012) · cites this paper as [74]
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Cites
Coordination of circadian timing in mammals
Reppert, S. M., & Weaver, D. R. (2002) · Nature · doi:10.1038/nature00965 · Cited by 4,379 · see citing works
Genetics of Mouse Behavior: Interactions with Laboratory Environment
Crabbe, J. C., Wahlsten, D., & Dudek, B. C. (1999) · Science · doi:10.1126/science.284.5420.1670 · Cited by 1,666 · see citing works
Moy, S. S., Nadler, J. J., Perez, A., Barbaro, R. P., Johns, J. M., Magnuson, T. R., Piven, J., & Crawley, J. N. (2004) · Genes, Brain and Behavior · doi:10.1111/j.1601-1848.2004.00076.x · Cited by 1,545 · see citing works
(2000) · Cited by 919 · see citing works
Autism‐like behavioral phenotypes in BTBR T+tf/J mice
McFarlane, H. G., Kusek, G. K., Yang, M., Phoenix, J. L., Bolivar, V. J., & Crawley, J. N. (2008) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2007.00330.x · Cited by 812 · see citing works
Self-citationMouse behavioral tasks relevant to autism: Phenotypes of 10 inbred strains
MOY, S., NADLER, J., YOUNG, N., PEREZ, A., HOLLOWAY, L., BARBARO, R., BARBARO, J., WILSON, L., THREADGILL, D., & LAUDER, J. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.07.030 · Cited by 776 · see citing works
Automated apparatus for quantitation of social approach behaviors in mice
Nadler, J. J., Moy, S. S., Dold, G., Trang, D., Simmons, N., Perez, A., Young, N. B., Barbaro, R. P., Piven, J., Magnuson, T. R., et al. (2004) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2004.00071.x · Cited by 775 · see citing works
Mouse genetics: concepts and applications
(1995) · Choice Reviews Online · doi:10.5860/choice.33-2135 · Cited by 757 · see citing works
A review of 25 years of the social interaction test
File, S. E., & Seth, P. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01273-1 · Cited by 744 · see citing works
Cryan, J. F., & Mombereau, C. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001457 · Cited by 616 · see citing works
Designing mouse behavioral tasks relevant to autistic‐like behaviors
Crawley, J. N. (2004) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/mrdd.20039 · Cited by 520 · see citing works
Different data from different labs: Lessons from studies of gene–environment interaction
Wahłsten, D., Metten, P., Phillips, T. J., Boehm, S. L., Burkhart‐Kasch, S., Dorow, J. D., Doerksen, S., Downing, C., Fogarty, J., Rodd‐Henricks, K., et al. (2002) · Journal of Neurobiology · doi:10.1002/neu.10173 · Cited by 495 · see citing works
Social influences on mammalian circadian rhythms: animal and human studies
Mistlberger, R. E., & Skene, D. J. (2004) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1017/s1464793103006353 · Cited by 402 · see citing works
Vasopressin V1b receptor knockout reduces aggressive behavior in male mice
Wersinger, S. R., Ginns, E. I., O'Carroll, A.-M., Lolait, S. J., & Young III, W. S. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001195 · Cited by 397 · see citing works
An Efficient SNP System for Mouse Genome Scanning and Elucidating Strain RelationshipsPreprint
Petkov, P. M., Ding, Y., Cassell, M. A., Zhang, W., Wagner, G., Sargent, E. E., Asquith, S., Crew, V., Johnson, K. A., Robinson, P. S., et al. (2004) · Genome Research · doi:10.1101/gr.2825804 · Cited by 338 · see citing works
Oxytocin, vasopressin and pair bonding: implications for autism
Hammock, E. A. D., & Young, L. J. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1939 · Cited by 289 · see citing works
Assessing autism-like behavior in mice: Variations in social interactions among inbred strains
BOLIVAR, V, WALTERS, S., & PHOENIX, J. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.09.007 · Cited by 264 · see citing works
Social reward among juvenile mice
Panksepp, J. B., & Lahvis, G. P. (2007) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2006.00295.x · Cited by 248 · see citing works
Leahy, A., Xiong, J., Kuhnert, F., & Stuhlmann, H. (1999) · Journal of Experimental Zoology · doi:10.1002/(sici)1097-010x(19990615)284:1 · Cited by 243 · see citing works
Crawley, J. N., Chen, T., Puri, A., Washburn, R., Sullivan, T. L., Hill, J. M., Young, N. B., Nadler, J. J., Moy, S. S., Young, L. J., et al. (2007) · Neuropeptides · doi:10.1016/j.npep.2007.02.002 · Cited by 232 · see citing works
Evolution of circadian organization in vertebrates
Menaker, M., Moreira, L. F. S., & Tosini, G. (1997) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x1997000300003 · Cited by 171 · see citing works
Ontogeny of amicable social behavior in the mouse: Gender differences and ongoing isolation outcomes
Terranova, M. L., Laviola, G., & Alleva, E. (1993) · Developmental Psychobiology · doi:10.1002/dev.420260805 · Cited by 160 · see citing works
Refining rodent husbandry: the mouse: Report of the Rodent Refinement Working Party
Jennings, M., Batchelor, G. R., Brain, P. F., Dick, A., Elliott, H., Francis, R. J., Hubrecht, R. C., Hurst, J. L., Morton, D. B., Peters, A. G., et al. (1998) · Laboratory Animals · doi:10.1258/002367798780559301 · Cited by 144 · see citing works
Wang, Z., Young, L. J., Vries, G. J. D., & Insel, T. R. (1999) · Progress in brain research · doi:10.1016/s0079-6123(08)61589-7 · Cited by 132 · see citing works
Wersinger, S. R., Kelliher, K. R., Zufall, F., Lolait, S. J., O’Carroll, A., & Young, W. S. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.07.004 · Cited by 132 · see citing works
Wersinger, S. R., Caldwell, H. K., Christiansen, M., & Young, W. S. (2006) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2006.00294.x · Cited by 130 · see citing works
A description of the ontogeny of mouse agonistic behavior.
Terranova, M. L., Giovanni Laviola, A., Acetis, L. D., & Alleva, E. (1998) · Journal of comparative psychology · doi:10.1037/0735-7036.112.1.3 · Cited by 107 · see citing works
Variability of diurnality in laboratory rodents
Refinetti, R. (2006) · Journal of Comparative Physiology A · doi:10.1007/s00359-006-0093-x · Cited by 104 · see citing works
Effects of light or dark phase testing on behavioural and cognitive performance in DBA mice
Roedel, A., Storch, C., Holsboer, F., & Ohl, F. (2006) · Laboratory Animals · doi:10.1258/002367706778476343 · Cited by 101 · see citing works
Varying responses to the rat forced-swim test under diurnal and nocturnal conditions
Kelliher, P., Connor, T. J., Harkin, A., Sánchez, C., Kelly, J. P., & Leonard, B. E. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(00)00213-4 · Cited by 91 · see citing works
ARAKAWA, H., BLANCHARD, D., & BLANCHARD, R. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.07.027 · Cited by 86 · see citing works
Scoring of Social Interactions and Play in Mice During Adolescence
Terranova, M. L., & Giovanni Laviola, A. (2005) · Current Protocols in Toxicology · doi:10.1002/0471140856.tx1310s26 · Cited by 86 · see citing works
Nocturnality and species survival.
Daily, G. C., & Ehrlich, P. R. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.21.11709 · Cited by 83 · see citing works
Vasopressin/oxytocin and aggression
Ferris, C. F. (2005) · Novartis Foundation symposium · doi:10.1002/0470010703.ch13 · Cited by 76 · see citing works
Beyond the Suprachiasmatic Nucleus
Mrosovsky, N. (2003) · Chronobiology International · doi:10.1081/cbi-120017811 · Cited by 74 · see citing works
The dark phase improves genetic discrimination for some high throughput mouse behavioral phenotyping
Hossain, S. M., Wong, B. K. Y., & Simpson, E. M. (2004) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2004.00069.x · Cited by 73 · see citing works
Vasopressin and pair-bond formation: genes to brain to behavior.
Nair, H. P., & Young, L. J. (2006) · Physiology · doi:10.1152/physiol.00049.2005 · Cited by 68 · see citing works
Locomotor activity rhythm in inbred strains of mice: implications for behavioural studies
Kopp, C. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00289-3 · Cited by 67 · see citing works
The use of sodium lamps to brightly illuminate mouse houses during their dark phases
McLennan, I. S., & Taylor-Jeffs, J. (2004) · Laboratory Animals · doi:10.1258/0023677041958927 · Cited by 66 · see citing works
Analysis of Behavior in Laboratory Rodents
Whishaw, I. Q., Haun, F., & Kolb, B. E. (1999) · Springer eBooks · doi:10.1007/978-3-642-58552-4_44 · Cited by 64 · see citing works
Nocturnal Activity in a Diurnal Rodent (Arvicanthis Niloticus): The Importance of Masking
Redlin, U., & Mrosovsky, N. (2004) · Journal of Biological Rhythms · doi:10.1177/0748730403260371 · Cited by 62 · see citing works
Low amplitude entrainment of mice and the impact of circadian phase on behavior tests
Beeler, J. A., Prendergast, B. J., & Zhuang, X. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.01.037 · Cited by 59 · see citing works
Daily activity patterns of a nocturnal and a diurnal rodent in a seminatural environment
REFINETTI, R. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.03.015 · Cited by 55 · see citing works
A mouse model of early social interactions after prenatal drug exposure: a genetic investigation
Giovanni Laviola, A., Terranova, M. L., Sedowofia, K., Clayton, R. M., & Manning, A. (1994) · Psychopharmacology · doi:10.1007/bf02245214 · Cited by 26 · see citing works
(2007) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2007.00355.x · Cited by 12 · see citing works
Saline drinking and naloxone: Lightcycle dependent effects on social behaviour in male mice
Paterson, A. T., & Vickers, C. (1984) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(84)80029-5 · Cited by 11 · see citing works
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Behavioural phenotyping assays for mouse models of autism
Silverman, J. L., Yang, M., Lord, C., & Crawley, J. N. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2851 · Cited by 1,462 · see citing works
Self-citationAutomated Three‐Chambered Social Approach Task for Mice
Yang, M., Silverman, J. L., & Crawley, J. N. (2011) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0826s56 · Cited by 598 · see citing works
Self-citationUnusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism
Scattoni, M. L., Gandhy, S. U., Ricceri, L., & Crawley, J. N. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003067 · Cited by 550 · see citing works
Behavioral phenotyping strategies for mutant mice
Crawley, J. N. (2008) · Neuron · doi:10.1016/j.neuron.2008.03.001 · Cited by 439 · see citing works
Silverman, J. L., Tolu, S. S., Barkan, C. L., & Crawley, J. N. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.201 · Cited by 438 · see citing works
Silverman, J. L., Smith, D. G., Rizzo, S. J. S., Karras, M. N., Turner, S. M., Tolu, S. S., Bryce, D. K., Smith, D. L., Fonseca, K., Ring, R. H., et al. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3003501 · Cited by 251 · see citing works
Shirvalkar, P. R., Rapp, P. R., & Shapiro, M. L. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911184107 · Cited by 235 · see citing works
Han, S., Tai, C., Jones, C. J., Scheuer, T., & Catterall, W. A. (2014) · Neuron · doi:10.1016/j.neuron.2014.01.016 · Cited by 231 · see citing works
Sociability and motor functions in Shank1 mutant mice
Silverman, J. L., Turner, S. M., Barkan, C. L., Tolu, S. S., Saxena, R., Hung, A. Y., Sheng, M., & Crawley, J. N. (2011) · Brain Research · doi:10.1016/j.brainres.2010.09.026 · Cited by 218 · see citing works
Silverman, J. L., Pride, M. C., Hayes, J. E., Puhger, K. R., Butler-Struben, H. M., Baker, S., & Crawley, J. N. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.66 · Cited by 215 · see citing works
Reduced scent marking and ultrasonic vocalizations in the BTBR T+tf/J mouse model of autism
Wöhr, M., Roullet, F. I., & Crawley, J. N. (2011) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2010.00582.x · Cited by 169 · see citing works
Motor and cognitive stereotypies in the BTBR T+tf/J mouse model of autism
Pearson, B. L., Pobbe, R. L. H., Defensor, E. B., Oasay, L., Bolivar, V. J., Blanchard, D. C., & Blanchard, R. J. (2011) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2010.00659.x · Cited by 171 · see citing works
The BTBR T+tf/J mouse model for autism spectrum disorders–in search of biomarkers
Meyza, K. Z., Defensor, E. B., Jensen, A. L., Corley, M. J., Pearson, B. L., Pobbe, R. L. H., Bolivar, V. J., Blanchard, D. C., & Blanchard, R. J. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.07.021 · Cited by 147 · see citing works
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Silverman, J. L., Yang, M., Turner, S. M., Katz, A. M., Bell, D. B., Koenig, J. I., & Crawley, J. N. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.09.059 · Cited by 146 · see citing works
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Ellegood, J., Babineau, B. A., Henkelman, R. M., Lerch, J. P., & Crawley, J. N. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2012.12.029 · Cited by 135 · see citing works
Dodero, L., Damiano, M., Galbusera, A., Bifone, A., Tsaftsaris, S. A., Scattoni, M. L., & Gozzi, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076655 · Cited by 116 · see citing works
Postnatal lesion evidence against a primary role for the corpus callosum in mouse sociability
Yang, M., Clarke, A. M., & Crawley, J. N. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06714.x · Cited by 117 · see citing works
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Yang, M., Abrams, D. N., Zhang, J. Y., Weber, M. D., Katz, A. M., Clarke, A. M., Silverman, J. L., & Crawley, J. N. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.12.025 · Cited by 112 · see citing works
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Yang, M., Perry, K., Weber, M. D., Katz, A. M., & Crawley, J. N. (2011) · Autism Research · doi:10.1002/aur.163 · Cited by 106 · see citing works
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Curley, J. P., Rock, V., Moynihan, A. M., Bateson, P., Keverne, E. B., & Champagne, F. A. (2010) · Behavior Genetics · doi:10.1007/s10519-010-9334-4 · Cited by 46 · see citing works
Williams Avram, S. K., Lee, H.-J., Fastman, J., Cymerblit-Sabba, A., Smith, A., Vincent, M., Song, J., Granovetter, M. C., Lee, S.-H., Cilz, N. I., et al. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00218 · Cited by 22 · see citing works
- Authors
- Yang, M.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Yang, Mu
- ORCID
- Yang, Mu
- Venue
- Frontiers in Behavioral Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2007
- Volume
- 1
- Pages
- 1-1
- ISSN
- 1662-5153 (ISSN-L)
- PMC
- PMC2525856
- OpenAlex
- W2093081094
- Cited by
- 124
- References
- 46
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 1 · 2023: 5 · 2022: 4 · 2021: 4 · 2020: 3 · 2019: 5 · 2018: 6 · 2017: 6 · 2016: 2 · 2015: 10 · 2014: 9 · 2013: 9 · 2012: 16
- FWCI
- 11.48
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Digital Kenyon (Kenyon College) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health
- National Institute of Mental Health (Z01MH002179, Z01-MH-002498, Z01MH002498)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Keywords
- social approach behavior, sociability, circadian rhythm, BTBR T+tf/J mice, C57BL/6J mice, huddling
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