Absence of social conditioned place preference in BTBR T+tf/J mice: Relevance for social motivation testing in rodent models of autism
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A major goal of translation research in autism is to characterize the physiological and psychological processes underlying behavioral abnormalities. Since autism reflects impairments in social motivation, we modified the mouse three-chamber social approach apparatus for use as a social conditioned place preference arena. We paired one of two unique contexts with social interactions in juvenile mice for five or ten conditioning sessions in BTBR T+tf/J mice and a control strain with normal approach behaviors (C57BL/6J) since the BTBR T+tf/J inbred mouse strain displays a variety of behavioral alterations analogous to symptoms of autism spectrum disorders. While C57BL/6J mice formed a conditioned place preference to the context associated with social interactions, particularly those receiving ten days of conditioning, BTBR T+tf/J mice did not. Neither absence of social proximity nor avoidance due to high rates of autogrooming appeared to underlie the impaired positive incentive value of the unconditioned social stimulus in the BTBR T+tf/J strain. These data contribute to a growing body of evidence suggesting that the BTBR T+tf/J strain shows impairments in all diagnostic domains of autism including social motivation. Additionally, social conditioning testing might provide an important social motivation measure in other rodent models of neuropsychiatric disorders characterized by social abnormalities.
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BTBR mice are deficient in conditioned place preference to social interactions.
“BTBR mice were also reported to be deficient in conditioned place preference to social interactions.46”
From Enhancement of anandamide-mediated endocannabinoid signaling corrects autism-related social impairment (2016) · cites this paper as [46]
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Cites
Diagnostic and Statistical Manual of Mental Disorders
Williams, J. B. W., & First, M. B. (2013) · Oxford University Press eBooks · doi:10.1093/acrefore/9780199975839.013.104 · Cited by 109,841 · see citing works
The social motivation theory of autism
Chevallier, C., Kohls, G., Troiani, V., Brodkin, E. S., & Schultz, R. T. (2012) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2012.02.007 · Cited by 2,072 · see citing works
The American Psychiatric Association (APA)
Strentz, T. (2017) · CRC Press eBooks · doi:10.1201/9781315150581-3 · Cited by 1,855 · see citing works
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
Conditioned place preference: what does it add to our preclinical understanding of drug reward?
Bardo, M. T., & Bevins, R. A. (2000) · Psychopharmacology · doi:10.1007/s002130000569 · Cited by 1,233 · see citing works
Early behavioral intervention, brain plasticity, and the prevention of autism spectrum disorder
Dawson, G. (2008) · Development and Psychopathology · doi:10.1017/s0954579408000370 · Cited by 1,138 · 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
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
HOW THE BRAIN PROCESSES SOCIAL INFORMATION: Searching for the Social Brain
Insel, T. R., & Fernald, R. D. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144148 · Cited by 556 · see citing works
Mouse Behavioral Assays Relevant to the Symptoms of Autism*
Crawley, J. N. (2007) · Brain Pathology · doi:10.1111/j.1750-3639.2007.00096.x · Cited by 541 · see citing works
Dawson, G., Carver, L., Meltzoff, A. N., Panagiotides, H., McPartland, J., & Webb, S. J. (2002) · Child Development · doi:10.1111/1467-8624.00433 · Cited by 523 · 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
Douglas, L. A., Varlinskaya, E. I., & Spear, L. P. (2004) · Developmental Psychobiology · doi:10.1002/dev.20025 · Cited by 389 · see citing works
Panksepp, J. B., Jochman, K. A., Kim, J. U., Koy, J. J., Wilson, E. D., Chen, Q., Wilson, C. R., & Lahvis, G. P. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000351 · Cited by 295 · see citing works
Place conditioning reveals the rewarding aspect of social interaction in juvenile rats
Calcagnetti, D. J., & Schechter, M. D. (1992) · Physiology & Behavior · doi:10.1016/0031-9384(92)90101-7 · Cited by 284 · 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
Neurofunctional mechanisms in autism
Waterhouse, L., Fein, D., & Modahl, C. (1996) · Psychological Review · doi:10.1037/0033-295x.103.3.457 · Cited by 218 · see citing works
Amodeo, D. A., Jones, J. H., Sweeney, J. A., & Ragozzino, M. E. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.10.032 · Cited by 191 · see citing works
Paparelli, A., di Forti, M., Morrison, P., & Murray, R. (2010) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00001 · Cited by 176 · 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
Self-citationThiel, K. J., Okun, A. C., & Neisewander, J. L. (2008) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2008.02.013 · Cited by 164 · see citing works
Low stress reactivity and neuroendocrine factors in the BTBR T+tf/J mouse model of autism
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
Fritz, M., Rawas, R. E., Salti, A., Klement, S., Bardo, M. T., Kemmler, G., Dechant, G., Saria, A., & Zernig, G. (2011) · Addiction Biology · doi:10.1111/j.1369-1600.2010.00285.x · Cited by 117 · 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
Trezza, V., Damsteegt, R., & Vanderschuren, L. J. M. J. (2009) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2009.03.006 · Cited by 115 · see citing works
Low sociability in BTBR T+tf/J mice is independent of partner strain
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
Conditioned place preference for social interaction in rats: contribution of sensory components
Kummer, K. K., Klement, S., Eggart, V., Michael, J. M., Saria, A., & Zernig, G. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00080 · Cited by 69 · see citing works
Successful intermale aggression and conditioned place preference in mice
Martı́nez, M., Guillén‐Salazar, F., Salvador, A., & Simón, V. M. (1995) · Physiology & Behavior · doi:10.1016/0031-9384(95)00061-m · Cited by 65 · see citing works
MacPherson, P., McGaffigan, R., Wahłsten, D., & Nguyen, P. (2008) · Brain Research · doi:10.1016/j.brainres.2008.03.008 · Cited by 61 · see citing works
Pacey, L. K. K., Doss, L., Cifelli, C., van der Kooy, D., Heximer, S. P., & Hampson, D. R. (2011) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2010.12.005 · Cited by 46 · see citing works
SOCIAL REINFORCEMENT OF OPERANT BEHAVIOR IN RATS: A METHODOLOGICAL NOTE
Evans, M. J., Duvel, A. D., Funk, M. L. J., Lehman, B., Sparrow, J. E., Watson, N. T., & Neuringer, A. J. (1994) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1994.62-149 · Cited by 41 · see citing works
Social and sexual motivation in the mouse.
Matthews, T. J., Abdelbaky, P., & Pfaff, D. W. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.6.1628 · Cited by 32 · see citing works
Age-dependent and strain-dependent influences of morphine on mouse social investigation behavior
Kennedy, B. C., Panksepp, J. B., Wong, J. C., Krause, E. J., & Lahvis, G. P. (2011) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e328343d7dd · Cited by 30 · see citing works
Bell, M. R., Meerts, S. H., & Sisk, C. L. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.05.017 · Cited by 29 · see citing works
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Murugan, M., Jang, H. J., Park, M., Miller, E. M., Cox, J., Taliaferro, J. P., Parker, N. F., Bhave, V., Hur, H., Liang, Y., et al. (2017) · Cell · doi:10.1016/j.cell.2017.11.002 · Cited by 311 · 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
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
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
Kas, M. J., Glennon, J. C., Buitelaar, J., Ey, E., Biemans, B., Crawley, J., Ring, R. H., Lajonchere, C., Esclassan, F., Talpos, J., et al. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3268-5 · Cited by 132 · see citing works
Wei, D., Dinh, D., Lee, D., Li, D., Anguren, A., Moreno-Sanz, G., Gall, C. M., & Piomelli, D. (2016) · Cannabis and Cannabinoid Research · doi:10.1089/can.2015.0008 · Cited by 122 · see citing works
Inflammatory profiles in the BTBR mouse: how relevant are they to autism spectrum disorders?
Careaga, M., Schwartzer, J., & Ashwood, P. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.06.006 · Cited by 77 · see citing works
Modeling autism-relevant behavioral phenotypes in rats and mice: Do ‘autistic’ rodents exist?
Servadio, M., Vanderschuren, L. J. M. J., & Trezza, V. (2015) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000163 · Cited by 76 · see citing works
- Authors
- Pearson, B. L., Bettis, J. K., Meyza, K. Z., Yamamoto, L. Y., Blanchard, D. C., & Blanchard, R. J.
- Affiliations
- University of Hawaiʻi at Mānoa (US)
- Corresponding author
- Pearson, Brandon L.
- Venue
- Behavioural Brain Research
- Publisher
- Elsevier BV
- Published
- 2012-07
- Volume
- 233
- Issue
- 1
- Pages
- 99-104
- ISSN
- 0166-4328 (ISSN-L)
- PMC
- PMC3378798
- OpenAlex
- W2048377822
- Cited by
- 57
- References
- 34
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 4 · 2023: 3 · 2022: 2 · 2021: 5 · 2020: 4 · 2019: 3 · 2018: 3 · 2017: 3 · 2016: 5 · 2015: 10 · 2014: 6 · 2013: 3 · 2012: 2
- FWCI
- 3.44
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Licence
- Locations
- Behavioural Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (R01MH081845, MH081845)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- BTBR T+tf/J mice, social motivation, autism spectrum disorder, social interaction, autogrooming, C57BL/6J mice, social conditioning
- MeSH terms
- Age Factors, Analysis of Variance, Animals, Animals, Newborn, Autistic Disorder, Conditioning, Operant, Disease Models, Animal, Grooming, Mice, Inbred C57BL, Mice, Mutant Strains, Motivation, Social Behavior, Time Factors, Mice
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