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Operant Social Reward Decreases Incubation of Heroin Craving in Male and Female Rats
Open accessAbstract
Background We recently reported that operant social choice-induced voluntary abstinence prevents incubation of methamphetamine craving. Here, we determined whether social choice-induced voluntary abstinence would prevent incubation of heroin craving. We also introduce a fully automatic social reward self-administration model that eliminates the intense workload and rat-human interaction of the original semiautomatic model.Methods In experiment 1, we trained male and female rats for social self-administration (6 days) and then for heroin self-administration (12 days). Next, we assessed relapse to heroin seeking after 1 and 15 abstinence days. Between tests, the rats underwent either forced or social choice-induced abstinence. In experiment 2, we developed a fully automatic social self-administration procedure by introducing a screen between the self-administration chamber and the social-peer chamber; the screen allows physical contact but prevents rats from crossing chambers. Next, we compared incubation of craving in rats with a history of standard (no-screen) or automatic (screen) social self-administration and social choice-induced abstinence.Results The time-dependent increase in heroin seeking after cessation of drug self-administration (incubation of craving) was lower after social choice-induced abstinence than after forced abstinence. There were no differences in social self-administration, social choice-induced abstinence, and incubation of craving in rats trained in the standard semiautomatic procedure versus the novel fully automatic procedure.Conclusions Our study demonstrates the protective effect of rewarding social interaction on heroin self-administration and incubation of heroin craving and introduces a fully automatic social self-administration and choice procedure to investigate the role of volitional social interaction in drug addiction and other psychiatric disorders.
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“the opportunity to socialize reduces drug seeking for both methamphetamine and heroin [145,146].”
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Citations
Cites
The reinstatement model of drug relapse: history, methodology and major findings
Shaham, Y., Shalev, U., Lu, L., de Wit, H., & Stewart, J. (2003) · Psychopharmacology · doi:10.1007/s00213-002-1224-x · Cited by 1,615
Self-citationThe Neuroscience of Natural Rewards: Relevance to Addictive Drugs
Kelley, A. E., & Berridge, K. C. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03306.2002 · Cited by 1,505
Drug Overdose Deaths in the United States, 1999–2020
Hedegaard, H., Miniño, A., Spencer, M. R., & Warner, M. (2021) · doi:10.15620/cdc:112340 · Cited by 1,283
Dole, V. P. (1965) · JAMA · doi:10.1001/jama.1965.03090080008002 · Cited by 1,240
Transition from Moderate to Excessive Drug Intake: Change in Hedonic Set Point
Ahmed, S. H., & Koob, G. F. (1998) · Science · doi:10.1126/science.282.5387.298 · Cited by 1,186
Evidence for Addiction-like Behavior in the Rat
Deroche-Gamonet, V., Belin, D., & Piazza, P. V. (2004) · Science · doi:10.1126/science.1099020 · Cited by 1,135
Incubation of cocaine craving after withdrawal
Grimm, J. W., Hope, B. T., Wise, R. A., & Shaham, Y. (2001) · Nature · doi:10.1038/35084134 · Cited by 1,031
Self-citationNeurobiology of relapse to heroin and cocaine seeking: a review
Shalev, U., Grimm, J. W., & Shaham, Y. (2002) · Pharmacological Reviews · doi:10.1124/pr.54.1.1 · Cited by 880
Self-citationPeciña, S., & Berridge, K. C. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2329-05.2005 · Cited by 671
Neurobiology of the incubation of drug craving
Pickens, C. L., Airavaara, M., Theberge, F. R. M., Fanous, S., Hope, B. T., & Shaham, Y. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.06.001 · Cited by 657
Self-citationBrain circuitry and the reinstatement of cocaine-seeking behavior
Kalivas, P., & McFarland, K. (2003) · Psychopharmacology · doi:10.1007/s00213-003-1393-2 · Cited by 613
A community-reinforcement approach to alcoholism
Hunt, G. M., & Azrin, N. H. (1973) · Behaviour Research and Therapy · doi:10.1016/0005-7967(73)90072-7 · Cited by 596
Heroin and cocaine intravenous self-administration in rats: Mediation by separate neural systems
Ettenberg, A., Pettit, H. O., Bloom, F. E., & Koob, G. F. (1982) · Psychopharmacology · doi:10.1007/bf00428151 · Cited by 563
A behavioral approach to achieving initial cocaine abstinence
Higgins, S. T., Delaney, D. D., Budney, A. J., Bickel, W. K., Hughes, J. R., Foerg, F. E., & Fenwick, J. W. (1991) · American Journal of Psychiatry · doi:10.1176/ajp.148.9.1218 · Cited by 553
Endogenous opioids and social behavior
Panksepp, J., Herman, B. H., Vilberg, T., Bishop, P., & DeEskinazi, F. G. (1980) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(80)90036-6 · Cited by 531
Opiate versus psychostimulant addiction: the differences do matter
Badiani, A., Belin, D., Epstein, D. H., Calu, D. J., & Shaham, Y. (2011) · Nature reviews. Neuroscience · doi:10.1038/nrn3104 · Cited by 491
Self-citationBossert, J. M., Marchant, N. J., Calu, D. J., & Shaham, Y. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3120-y · Cited by 453
Self-citationSynaptic mechanisms underlying persistent cocaine craving
Wolf, M. E. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.39 · Cited by 397
Clinical Implications of Reinforcement as a Determinant of Substance Use Disorders
Higgins, S. T., Heil, S. H., & Lussier, J. P. (2004) · Annual Review of Psychology · doi:10.1146/annurev.psych.55.090902.142033 · Cited by 393
Mello, N. K. (1996) · Neuropsychopharmacology · doi:10.1016/0893-133x(95)00274-h · Cited by 391
Improvements in the community-reinforcement approach to alcoholism
Azrin, N. H. (1976) · Behaviour Research and Therapy · doi:10.1016/0005-7967(76)90021-8 · Cited by 371
Volitional social interaction prevents drug addiction in rat models
Venniro, M., Zhang, M., Caprioli, D., Hoots, J. K., Golden, S. A., Heins, C., Morales, M., Epstein, D. H., & Shaham, Y. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0246-6 · Cited by 342
Self-citationAnimal models of drug relapse and craving
Vènniro, M., Caprioli, D., & Shaham, Y. (2015) · Progress in brain research · doi:10.1016/bs.pbr.2015.08.004 · Cited by 331
Self-citationThe neurobiology of social play and its rewarding value in rats
Vanderschuren, L. J. M. J., Achterberg, E. J. M., & Trezza, V. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.025 · Cited by 329
Opioids, Reward and Addiction: An Encounter of Biology, Psychology, and Medicine
van Ree, J. M., Gerrits, M. A. F. M., & Vanderschuren, L. J. M. J. (1999) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01405-4 · Cited by 301
Time to connect: bringing social context into addiction neuroscience
Heilig, M., Epstein, D. H., Nader, M. A., & Shaham, Y. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.67 · Cited by 298
Self-citationShalev, U., Morales, M., Hope, B. T., Yap, J. J., & Shaham, Y. (2001) · Psychopharmacology · doi:10.1007/s002130100748 · Cited by 290
Self-citationNeurobiology of relapse to heroin and cocaine seeking: An update and clinical implications
Bossert, J. M., Ghitza, U. E., Lü, L., Epstein, D. H., & Shaham, Y. (2005) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.09.030 · Cited by 271
Self-citationNucleus Accumbens μ-Opioid Receptors Mediate Social Reward
Trezza, V., Damsteegt, R., Achterberg, E. J. M., & Vanderschuren, L. J. M. J. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.5492-10.2011 · Cited by 263
Ahmed, S. H. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.04.005 · Cited by 250
Johnson, Z. V., & Young, L. J. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.034 · Cited by 242
Incubation of Cue-Induced Cigarette Craving During Abstinence in Human Smokers
Bedi, G., Preston, K. L., Epstein, D. H., Heishman, S. J., Marrone, G. F., Shaham, Y., & de Wit, H. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.07.014 · Cited by 237
Self-citationThe US Opioid Crisis: Current Federal and State Legal Issues
Soelberg, C. D., Re, B., Vivier, D. D., Meyer, J. E., & Ramachandran, B. K. (2017) · Anesthesia & Analgesia · doi:10.1213/ane.0000000000002403 · Cited by 215
Incubation of Cue-Induced Craving in Adults Addicted to Cocaine Measured by Electroencephalography
Parvaz, M. A., Moeller, S. J., & Goldstein, R. Z. (2016) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2016.2181 · Cited by 212
Opioids and consummatory behavior
Levine, A. S., Morley, J. E., Gosnell, B. A., Billington, C. J., & Bartness, T. J. (1985) · Brain Research Bulletin · doi:10.1016/0361-9230(85)90116-9 · Cited by 180
Circuit and Synaptic Plasticity Mechanisms of Drug Relapse
Dong, Y., Taylor, J. R., Wolf, M. E., & Shaham, Y. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1821-17.2017 · Cited by 180
Self-citationThe Motivation to Self-Administer is Increased After a History of Spiking Brain Levels of Cocaine
Zimmer, B. A., Oleson, E. B., & Roberts, D. C. S. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.37 · Cited by 170
Lü, L., Grimm, J. W., Dempsey, J., & Shaham, Y. (2004) · Psychopharmacology · doi:10.1007/s00213-004-1860-4 · Cited by 168
Self-citationIndividual Differences and Social Influences on the Neurobehavioral Pharmacology of Abused Drugs
Bardo, M. T., Neisewander, J. L., & Kelly, T. H. (2013) · Pharmacological Reviews · doi:10.1124/pr.111.005124 · Cited by 167
The Central Amygdala Nucleus is Critical for Incubation of Methamphetamine Craving
Li, X., Zeric, T., Kambhampati, S., Bossert, J. M., & Shaham, Y. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.320 · Cited by 163
Self-citationVenniro, M., Caprioli, D., Zhang, M., Whitaker, L. R., Zhang, S., Warren, B. L., Cifani, C., Marchant, N. J., Yizhar, O., Bossert, J. M., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.024 · Cited by 162
Self-citationVènniro, M., Zhang, M. H., Shaham, Y., & Caprioli, D. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.287 · Cited by 152
Self-citationInsights from Preclinical Choice Models on Treating Drug Addiction
Banks, M. L., & Negus, S. S. (2016) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2016.11.002 · Cited by 151
Caprioli, D., Vènniro, M., Zhang, M. H., Bossert, J. M., Warren, B. L., Hope, B. T., & Shaham, Y. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3091-16.2016 · Cited by 149
Self-citationCaprioli, D., Venniro, M., Zeric, T., Li, X., Adhikary, S., Madangopal, R., Marchant, N. J., Lucantonio, F., Schoenbaum, G., Bossert, J. M., et al. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.02.018 · Cited by 145
Self-citationRole of Orbitofrontal Cortex Neuronal Ensembles in the Expression of Incubation of Heroin Craving
Fanous, S., Goldart, E. M., Theberge, F. R. M., Bossert, J. M., Shaham, Y., & Hope, B. T. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1914-12.2012 · Cited by 140
Self-citationDrug Overdose Deaths in the United States, 1999-2016.
Hedegaard, H. B., Warner, M., & Miniño, A. (2017) · PubMed · Cited by 135
Oxytocin, vasopressin, and the motivational forces that drive social behaviors
Caldwell, H. K., & Albers, H. E. (2015) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2015_390 · Cited by 129
Theberge, F. R., Li, X., Kambhampati, S., Pickens, C. L., St. Laurent, R., Bossert, J. M., Baumann, M. H., Hutchinson, M. R., Rice, K. C., Watkins, L. R., et al. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.12.019 · Cited by 119
Self-citationLü, L., Wang, X., Wu, P., Xu, C., Zhao, M., Morales, M., Harvey, B. K., Hoffer, B. J., & Shaham, Y. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.02.009 · Cited by 114
Self-citationEffects of environmental enrichment on the incubation of cocaine craving
Chauvet, C., Goldberg, S. R., Jaber, M., & Solinas, M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.05.014 · Cited by 100
Bossert, J. M., Adhikary, S., Laurent, R. S., Marchant, N. J., Wang, H.-L., Morales, M., & Shaham, Y. (2015) · Psychopharmacology · doi:10.1007/s00213-015-4060-5 · Cited by 99
Self-citationCaprioli, D., Celentano, M., Dubla, A., Lucantonio, F., Nencini, P., & Badiani, A. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.12.009 · Cited by 94
Kristjánsson, Á. L., Sigfúsdóttir, I. D., Þórlindsson, Þ., Mann, M. J., Sigfússon, J., & Allegrante, J. P. (2015) · Addiction · doi:10.1111/add.13248 · Cited by 90
Maintenance of reinforcement to address the chronic nature of drug addiction
Silverman, K., DeFulio, A., & Sigurdsson, S. O. (2012) · Preventive Medicine · doi:10.1016/j.ypmed.2012.03.013 · Cited by 85
Caprioli, D., Zeric, T., Thorndike, E. B., & Vènniro, M. (2015) · Addiction Biology · doi:10.1111/adb.12220 · Cited by 80
Prefrontal Cortical Opioids and Dysregulated Motivation: A Network Hypothesis
Baldo, B. A. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.03.004 · Cited by 76
Trying to make sense of rodents' drug choice behavior
Ahmed, S. H. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.09.027 · Cited by 74
Thiel, K. J., Painter, M. R., Pentkowski, N. S., Mitroi, D., Crawford, C. A., & Neisewander, J. L. (2011) · Addiction Biology · doi:10.1111/j.1369-1600.2011.00358.x · Cited by 72
Contingency management: an evidence‐based component of methamphetamine use disorder treatments
Roll, J. M. (2007) · Addiction · doi:10.1111/j.1360-0443.2006.01774.x · Cited by 68
Airavaara, M., Pickens, C. L., Stern, A. L., Wihbey, K. A., Harvey, B. K., Bossert, J. M., Liu, Q., Hoffer, B. J., & Shaham, Y. (2010) · Addiction Biology · doi:10.1111/j.1369-1600.2010.00281.x · Cited by 66
Self-citationSubstance-specific environmental influences on drug use and drug preference in animals and humans
Badiani, A. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.03.010 · Cited by 62
Aklin, W., Wong, C. J., Hampton, J., Svikis, D., Stitzer, M., Bigelow, G., & Silverman, K. (2014) · Journal of Substance Abuse Treatment · doi:10.1016/j.jsat.2014.06.013 · Cited by 60
Abstinence reinforcement maintenance contingency and one-year follow-up.
Preston, K., Umbricht, A., & Epstein, D. (2002) · Drug and Alcohol Dependence · doi:10.1016/s0376-8716(02)00023-6 · Cited by 52
Pirro, S. D., Galati, G., Pizzamiglio, L., & Badiani, A. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0019-18.2018 · Cited by 48
Nader, M. A., & Banks, M. L. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.05.044 · Cited by 45
Grimm, J. W., Barnes, J. L., Koerber, J., Glueck, E., Ginder, D. E., Hyde, J., & Eaton, L. (2015) · Brain Structure and Function · doi:10.1007/s00429-015-1074-z · Cited by 44
Science-Based Actions Can Help Address the Opioid Crisis
Epstein, D. H., Heilig, M., & Shaham, Y. (2018) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2018.06.002 · Cited by 42 · cited 5×
“Research on neural substrates of drug reward, withdrawal, and relapse has yet to be translated into an advancement in addiction treatment (1, 2).”
BackgroundMethodInfluentialSelf-citationTranslational Research on Incubation of Cocaine Craving
Li, X., Vènniro, M., & Shaham, Y. (2016) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2016.2110 · Cited by 41
Self-citationNovel models of drug relapse and craving after voluntary abstinence
Vènniro, M., Caprioli, D., & Shaham, Y. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0196-4 · Cited by 38
Self-citationCommunity Reinforcement Approach and Contingency Management Interventions for Substance Abuse
Stitzer, M. L., Jones, H. E., Tuten, M., & Wong, C. J. (2011) · doi:10.1002/9780470979952.ch23 · Cited by 24
Dunn, K., Defulio, A., Everly, J. J., Donlin, W. D., Aklin, W., Nuzzo, P. A., Leoutsakos, J., Umbricht, A., Fingerhood, M. I., Bigelow, G., et al. (2014) · Psychology of Addictive Behaviors · doi:10.1037/adb0000010 · Cited by 22
Does human language limit translatability of clinical and preclinical addiction research?
de Wit, H., Epstein, D. H., & Preston, K. L. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0095-8 · Cited by 20
Heroin versus cocaine: opposite choice as a function of context but not of drug history in the rat
Luca, M. T. D., Montanari, C., Meringolo, M., Contu, L., Celentano, M., & Badiani, A. (2018) · Psychopharmacology · doi:10.1007/s00213-018-5115-1 · Cited by 19
Anorectic specificity as measured in a choice paradigm in rhesus monkeys
Corwin, R. L., & Schuster, C. R. (1993) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(93)90096-c · Cited by 9
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Metadata
- Authors
- Venniro, M., Russell, T. I., Zhang, M., & Shaham, Y.
- Affiliations
- National Institutes of Health (US)
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2019-12
- Volume
- 86
- Issue
- 11
- Pages
- 848-856
- ISSN
- 0006-3223 (ISSN-L)
- PMC
- PMC8383184
- OpenAlex
- W2947439413
- Cited by
- 127
- References
- 75
- Citations by year
- 2026: 6 · 2025: 16 · 2024: 16 · 2023: 13 · 2022: 28 · 2021: 25 · 2020: 21 · 2019: 2
- FWCI
- 9.07
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Drug Abuse
- National Institutes of Health
- National Alliance for Research
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Health Sciences › Medicine › Epidemiology › Substance Abuse Treatment and Outcomes
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Opioid Use Disorder Treatment
- Keywords
- heroin craving, incubation of craving, social reward, heroin self-administration, relapse, sex differences, drug addiction, social interaction
- MeSH terms
- Animals, Behavior, Animal, Choice Behavior, Heroin, Extinction, Psychological, Feeding Behavior, Female, Male, Methamphetamine, Reward, Self Administration, Social Behavior, Rats, Sprague-Dawley, Rats, Drug-Seeking Behavior, Craving
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