A method for evaluating cocaine-induced social preference in rats
Main Article Content
Keywords
COCAINE, SOCIAL INTERACTIONS, CONDITIONED PLACE PREFERENCE
Abstract
Drug addicts are extremely sensitive to cues that predict drug availability and exposure to these cues can facilitate drug relapse. Cues vary in their nature but can include drug-associated paraphernalia, environmental contexts, and discrete conditioned stimuli (e.g., advertisements). One cue that has recently been heavily investigated is that of social interaction. To date, it has been demonstrated that when cocaine is conditioned with social interaction, place preference for cocaine significantly increases, suggesting that the presence of social interaction during a drug-associated “high” enhances the magnitude of drug reward. When social interaction is provided in a mutually exclusive, non-drug environment though, it can serve as a preventative stimulus towards cocaine seeking. What remains unknown is whether contact with rats associated with drug experience facilitates preferential social interactions for those rats. The first step in answering this question is to determine if rats can behaviorally discriminate between drug-associated and non-drug-associated conspecifics, much like humans can differentiate their “drug-friends” from their non-drug-using friends. Using a custom social interaction chamber, in which rats were able to interact with two distinct conspecifics via holes in a boundary wall, we demonstrate that rats exhibit more interactive and investigative behavior towards a partner that was consistently present during the drug-state, than a partner that was present when the rat was “sober”. It is our hope that this protocol will contribute to the development of models designed to study social cue-induced reinstatement, and related neural substrates, and will ultimately contribute to the treatment of substance use disorders.
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References
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25 Zernig, G., Kummer, K. K. & Prast, J. M. Dyadic social interaction as an alternative reward to cocaine. Frontiers in psychiatry 4, 100, doi:10.3389/fpsyt.2013.00100 (2013).
26 Zernig, G. & Pinheiro, B. S. Dyadic social interaction inhibits cocaine-conditioned place preference and the associated activation of the accumbens corridor. Behavioural pharmacology 26, 580-594, doi:10.1097/FBP.0000000000000167 (2015).
27 Kummer, K. et al. Conditioned place preference for social interaction in rats: contribution of sensory components. Frontiers in behavioral neuroscience 5, 80, doi:10.3389/fnbeh.2011.00080 (2011).
28 Volkow, N. D. et al. Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction. The Journal of neuroscience : the official journal of the Society for Neuroscience 26, 6583-6588, doi:10.1523/JNEUROSCI.1544-06.2006 (2006).
29 Kalivas, P. W. & Volkow, N. D. The neural basis of addiction: a pathology of motivation and choice. The American journal of psychiatry 162, 1403-1413, doi:10.1176/appi.ajp.162.8.1403 (2005).
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31 Brown, R. M., Short, J. L. & Lawrence, A. J. Identification of brain nuclei implicated in cocaine-primed reinstatement of conditioned place preference: a behaviour dissociable from sensitization. PloS one 5, e15889, doi:10.1371/journal.pone.0015889 (2010).
32 Beardsley, P. M. & Shelton, K. L. Prime-, stress-, and cue-induced reinstatement of extinguished drug-reinforced responding in rats: cocaine as the prototypical drug of abuse. Current protocols in neuroscience / editorial board, Jacqueline N. Crawley ... [et al.] Chapter 9, Unit 9 39, doi:10.1002/0471142301.ns0939s61 (2012).
33 McFarland, K., Lapish, C. C. & Kalivas, P. W. Prefrontal glutamate release into the core of the nucleus accumbens mediates cocaine-induced reinstatement of drug-seeking behavior. The Journal of neuroscience : the official journal of the Society for Neuroscience 23, 3531-3537 (2003).
34 Kummer, K. K. et al. Differences in social interaction- vs. cocaine reward in mouse vs. rat. Frontiers in behavioral neuroscience 8, 363, doi:10.3389/fnbeh.2014.00363 (2014).
35 Valjent, E. et al. Involvement of the extracellular signal-regulated kinase cascade for cocaine-rewarding properties. The Journal of neuroscience : the official journal of the Society for Neuroscience 20, 8701-8709 (2000).
36 Redila, V. A. & Chavkin, C. Stress-induced reinstatement of cocaine seeking is mediated by the kappa opioid system. Psychopharmacology 200, 59-70, doi:10.1007/s00213-008-1122-y (2008).
37 LaLumiere, R. T., Niehoff, K. E. & Kalivas, P. W. The infralimbic cortex regulates the consolidation of extinction after cocaine self-administration. Learn Mem 17, 168-175, doi:10.1101/lm.1576810 (2010).
38 Lubin, D. A., Meter, K. E., Walker, C. H. & Johns, J. M. Effects of chronic cocaine administration on aggressive behavior in virgin rats. Progress in neuro-psychopharmacology & biological psychiatry 25, 1421-1433 (2001).
2 Childress, A. R. et al. Limbic activation during cue-induced cocaine craving. The American journal of psychiatry 156, 11-18, doi:10.1176/ajp.156.1.11 (1999).
3 O'Brien, C. P., Childress, A. R., Ehrman, R. & Robbins, S. J. Conditioning factors in drug abuse: can they explain compulsion? Journal of psychopharmacology 12, 15-22 (1998).
4 Skinner, M. D. & Aubin, H. J. Craving's place in addiction theory: contributions of the major models. Neuroscience and biobehavioral reviews 34, 606-623, doi:10.1016/j.neubiorev.2009.11.024 (2010).
5 Tiffany, S. T. & Wray, J. M. The clinical significance of drug craving. Annals of the New York Academy of Sciences 1248, 1-17, doi:10.1111/j.1749-6632.2011.06298.x (2012).
6 Grimm, J. W., Hope, B. T., Wise, R. A. & Shaham, Y. Neuroadaptation. Incubation of cocaine craving after withdrawal. Nature 412, 141-142, doi:10.1038/35084134 (2001).
7 Lu, L., Grimm, J. W., Hope, B. T. & Shaham, Y. Incubation of cocaine craving after withdrawal: a review of preclinical data. Neuropharmacology 47 Suppl 1, 214-226, doi:10.1016/j.neuropharm.2004.06.027 (2004).
8 Ma, Y. Y. et al. Bidirectional modulation of incubation of cocaine craving by silent synapse-based remodeling of prefrontal cortex to accumbens projections. Neuron 83, 1453-1467, doi:10.1016/j.neuron.2014.08.023 (2014).
9 Volkow, N. D. et al. High levels of dopamine D2 receptors in unaffected members of alcoholic families: possible protective factors. Arch Gen Psychiatry 63, 999-1008, doi:10.1001/archpsyc.63.9.999 (2006).
10 Volkow, N. D. et al. Dopamine increases in striatum do not elicit craving in cocaine abusers unless they are coupled with cocaine cues. NeuroImage 39, 1266-1273, doi:10.1016/j.neuroimage.2007.09.059 (2008).
11 Epstein, D. H. et al. Real-time electronic diary reports of cue exposure and mood in the hours before cocaine and heroin craving and use. Archives of general psychiatry 66, 88-94, doi:10.1001/archgenpsychiatry.2008.509 (2009).
12 Havassy, B. E., Wasserman, D. A. & Hall, S. M. Social relationships and abstinence from cocaine in an American treatment sample. Addiction 90, 699-710 (1995).
13 Friedmann, P. D., Saitz, R. & Samet, J. H. Management of adults recovering from alcohol or other drug problems: relapse prevention in primary care. Jama 279, 1227-1231 (1998).
14 Fatseas, M. et al. Craving and substance use among patients with alcohol, tobacco, cannabis or heroin addiction: a comparison of substance- and person-specific cues. Addiction 110, 1035-1042, doi:10.1111/add.12882 (2015).
15 Ben-Ami Bartal, I., Decety, J. & Mason, P. Empathy and pro-social behavior in rats. Science 334, 1427-1430, doi:10.1126/science.1210789 (2011).
16 Varlinskaya, E. I., Spear, L. P. & Spear, N. E. Social behavior and social motivation in adolescent rats: role of housing conditions and partner's activity. Physiology & behavior 67, 475-482 (1999).
17 Panksepp, J. The ontogeny of play in rats. Developmental psychobiology 14, 327-332, doi:10.1002/dev.420140405 (1981).
18 Panksepp, J. & Beatty, W. W. Social deprivation and play in rats. Behavioral and neural biology 30, 197-206 (1980).
19 Douglas, L. A., Varlinskaya, E. I. & Spear, L. P. Rewarding properties of social interactions in adolescent and adult male and female rats: impact of social versus isolate housing of subjects and partners. Developmental psychobiology 45, 153-162, doi:10.1002/dev.20025 (2004).
20 Thiel, K. J., Okun, A. C. & Neisewander, J. L. Social reward-conditioned place preference: a model revealing an interaction between cocaine and social context rewards in rats. Drug and alcohol dependence 96, 202-212, doi:10.1016/j.drugalcdep.2008.02.013 (2008).
21 Yates, J. R., Beckmann, J. S., Meyer, A. C. & Bardo, M. T. Concurrent choice for social interaction and amphetamine using conditioned place preference in rats: effects of age and housing condition. Drug and alcohol dependence 129, 240-246, doi:10.1016/j.drugalcdep.2013.02.024 (2013).
22 Peartree, N. A. et al. Limited physical contact through a mesh barrier is sufficient for social reward-conditioned place preference in adolescent male rats. Physiology & behavior 105, 749-756, doi:10.1016/j.physbeh.2011.10.001 (2012).
23 Fritz, M. et al. Differential effects of accumbens core vs. shell lesions in a rat concurrent conditioned place preference paradigm for cocaine vs. social interaction. PloS one 6, e26761, doi:10.1371/journal.pone.0026761 (2011).
24 Grotewold, S. K., Wall, V. L., Goodell, D. J., Hayter, C. & Bland, S. T. Effects of cocaine combined with a social cue on conditioned place preference and nucleus accumbens monoamines after isolation rearing in rats. Psychopharmacology 231, 3041-3053, doi:10.1007/s00213-014-3470-0 (2014).
25 Zernig, G., Kummer, K. K. & Prast, J. M. Dyadic social interaction as an alternative reward to cocaine. Frontiers in psychiatry 4, 100, doi:10.3389/fpsyt.2013.00100 (2013).
26 Zernig, G. & Pinheiro, B. S. Dyadic social interaction inhibits cocaine-conditioned place preference and the associated activation of the accumbens corridor. Behavioural pharmacology 26, 580-594, doi:10.1097/FBP.0000000000000167 (2015).
27 Kummer, K. et al. Conditioned place preference for social interaction in rats: contribution of sensory components. Frontiers in behavioral neuroscience 5, 80, doi:10.3389/fnbeh.2011.00080 (2011).
28 Volkow, N. D. et al. Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction. The Journal of neuroscience : the official journal of the Society for Neuroscience 26, 6583-6588, doi:10.1523/JNEUROSCI.1544-06.2006 (2006).
29 Kalivas, P. W. & Volkow, N. D. The neural basis of addiction: a pathology of motivation and choice. The American journal of psychiatry 162, 1403-1413, doi:10.1176/appi.ajp.162.8.1403 (2005).
30 Graziane, N. M., Polter, A. M., Briand, L. A., Pierce, R. C. & Kauer, J. A. Kappa opioid receptors regulate stress-induced cocaine seeking and synaptic plasticity. Neuron 77, 942-954, doi:10.1016/j.neuron.2012.12.034 (2013).
31 Brown, R. M., Short, J. L. & Lawrence, A. J. Identification of brain nuclei implicated in cocaine-primed reinstatement of conditioned place preference: a behaviour dissociable from sensitization. PloS one 5, e15889, doi:10.1371/journal.pone.0015889 (2010).
32 Beardsley, P. M. & Shelton, K. L. Prime-, stress-, and cue-induced reinstatement of extinguished drug-reinforced responding in rats: cocaine as the prototypical drug of abuse. Current protocols in neuroscience / editorial board, Jacqueline N. Crawley ... [et al.] Chapter 9, Unit 9 39, doi:10.1002/0471142301.ns0939s61 (2012).
33 McFarland, K., Lapish, C. C. & Kalivas, P. W. Prefrontal glutamate release into the core of the nucleus accumbens mediates cocaine-induced reinstatement of drug-seeking behavior. The Journal of neuroscience : the official journal of the Society for Neuroscience 23, 3531-3537 (2003).
34 Kummer, K. K. et al. Differences in social interaction- vs. cocaine reward in mouse vs. rat. Frontiers in behavioral neuroscience 8, 363, doi:10.3389/fnbeh.2014.00363 (2014).
35 Valjent, E. et al. Involvement of the extracellular signal-regulated kinase cascade for cocaine-rewarding properties. The Journal of neuroscience : the official journal of the Society for Neuroscience 20, 8701-8709 (2000).
36 Redila, V. A. & Chavkin, C. Stress-induced reinstatement of cocaine seeking is mediated by the kappa opioid system. Psychopharmacology 200, 59-70, doi:10.1007/s00213-008-1122-y (2008).
37 LaLumiere, R. T., Niehoff, K. E. & Kalivas, P. W. The infralimbic cortex regulates the consolidation of extinction after cocaine self-administration. Learn Mem 17, 168-175, doi:10.1101/lm.1576810 (2010).
38 Lubin, D. A., Meter, K. E., Walker, C. H. & Johns, J. M. Effects of chronic cocaine administration on aggressive behavior in virgin rats. Progress in neuro-psychopharmacology & biological psychiatry 25, 1421-1433 (2001).
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Mar 7, 2017
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Dingess PM, Deters MJ, Darling RA, Yarborough EA, Brown TE. A method for evaluating cocaine-induced social preference in rats. J Biol Methods [Internet]. 2017 Mar. 7 [cited 2024 Apr. 24];4(1):e66. Available from: https://jbmethods.org/index.php/jbm/article/view/145
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Author Biography
Travis E. Brown, University of Wyoming
Assistant Professor of Neuroscience
