Risk‐preferring rats make worse decisions and show increased incubation of craving after cocaine self‐administration
Abstract
Maladaptive decision‐making may play an integral role in the development and maintenance of an addiction. Substance‐dependent individuals make riskier choices on the Iowa Gambling Task, and these deficits persist during withdrawal and are predictive of relapse. However, it is unclear from clinical studies whether this cognitive impairment is a cause or consequence of drug use. We trained male Long‐Evans rats on the rat Gambling Task, a rodent analogue of the Iowa Gambling Task, to determine how choice preference influenced, and was influenced by, cocaine self‐administration, withdrawal and incubation of craving. Rats that exhibited a preference for the risky, disadvantageous options at baseline were uniquely and adversely affected by cocaine self‐administration. Risky choice was exacerbated in these rats when decision‐making was assessed during the same diurnal period as cocaine self‐administration, whereas the choice pattern of optimal decision‐makers was unaffected. This decision‐making deficit was maintained during 30 days of withdrawal and correlated with greater cue‐induced incubation of craving. Risk‐preferring rats also made more drug‐seeking responses during cocaine self‐administration. These data demonstrate that poor decision‐making prior to contact with addictive drugs is associated with a pro‐addictive behavioural phenotype, characterized by further increased risky choice and heightened responding for drug both during cocaine self‐administration and withdrawal. Such findings indicate that the elevated risky decision‐making observed in substance‐dependent populations is not merely circumstantial, but makes an important contribution to addiction vulnerability and severity that can now be effectively modelled in laboratory rats.
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Risk-preferring animals in the rodent gambling task make more drug-seeking responses and show greater cue-induced incubation of craving after cocaine self-administration.
“While the majority of animals learn to choose the safe and advantageous options, a small proportion tend to be more risk-preferring, and these risk-preferring animals make more drug-seeking responses and show greater cue-induced incubation of craving after cocaine self-administration (Ferland & Winstanley, 2016).”
From Cued for Risk: Evidence for an Incentive Sensitization Framework to Explain the Interplay between Stress and Anxiety, Substance Abuse, and Reward Uncertainty in Disordered Gambling Behavior (2019) · cites this paper as Ferland & Winstanley, 2016
Cites
Insensitivity to future consequences following damage to human prefrontal cortex
Bechara, A., Damasio, A. R., Damasio, H., & Anderson, S. W. (1994) · Cognition · doi:10.1016/0010-0277(94)90018-3 · Cited by 6,128 · see citing works
Goldstein, R. Z., & Volkow, N. D. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.10.1642 · Cited by 2,667 · see citing works
Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective
Bechara, A. (2005) · Nature Neuroscience · doi:10.1038/nn1584 · Cited by 2,149 · cited 1× · see citing works
“Indeed, dependent populations perform poorly on laboratory-based cost/benefit decision-making tasks(Bechara 2005; Bolla et al. 2003; Rogers et al. 1999; Verdejo-Garcia & Bechara 2009).”
BackgroundDifferent contributions of the human amygdala and ventromedial prefrontal cortex to decision-making
Bechara, A., Damasio, H., Damasio, A. R., & Lee, G. P. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-13-05473.1999 · Cited by 2,001 · see citing works
Bechara, A., Dolan, S. L., Denburg, N. L., Hindes, A. R., Anderson, S. W., & Nathan, P. E. (2001) · Neuropsychologia · doi:10.1016/s0028-3932(00)00136-6 · Cited by 1,168 · see citing works
Rogers, R. (1999) · Neuropsychopharmacology · doi:10.1016/s0893-133x(98)00091-8 · Cited by 1,101 · see citing works
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 1,003 · see citing works
High Impulsivity Predicts the Switch to Compulsive Cocaine-Taking
Belin, D., Mar, A. C., Dalley, J. W., Robbins, T. W., & Everitt, B. J. (2008) · Science · doi:10.1126/science.1158136 · Cited by 989 · see citing works
Drug abusers show impaired performance in a laboratory test of decision making
Grant, S. (2000) · Neuropsychologia · doi:10.1016/s0028-3932(99)00158-x · Cited by 625 · see citing works
Orbitofrontal cortex dysfunction in abstinent cocaine abusers performing a decision-making task
Bolla, K. I., Eldreth, D. A., London, E. D., Kiehl, K. A., Mouratidis, M., Contoreggi, C. S., Matochik, J. A., Kurian, V., Cadet, J. L., Kimes, A. S., et al. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00113-7 · Cited by 578 · see citing works
Risky Business: Emotion, Decision-Making, and Addiction
Bechara, A. (2004) · Journal of Gambling Studies · doi:10.1023/a:1021223113233 · Cited by 500 · see citing works
Goudriaan, A., Oosterlaan, J., de Beurs, E., & van den Brink, W. (2005) · Brain research. Cognitive brain research · doi:10.1016/j.cogbrainres.2005.01.017 · Cited by 473 · see citing works
Perry, J. L., Larson, E. B., German, J. P., Madden, G. J., & Carroll, M. E. (2005) · Psychopharmacology · doi:10.1007/s00213-004-1994-4 · Cited by 388 · see citing works
Zeeb, F. D., Robbins, T. W., & Winstanley, C. A. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.62 · Cited by 384 · see citing works
Self-citationNeural substrates of faulty decision-making in abstinent marijuana users
Bolla, K. I., Eldreth, D. A., Matochik, J. A., & Cadet, J. L. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.02.012 · Cited by 378 · see citing works
A somatic marker theory of addiction
Verdejo‐García, A., & Bechara, A. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.07.035 · Cited by 359 · see citing works
Ma, Y.-Y., Lee, B. R., Wang, X., Guo, C., Liu, L., Cui, R., Lan, Y., Balcita-Pedicino, J. J., Wolf, M. E., Sesack, S. R., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.08.023 · Cited by 344 · see citing works
Cognitive impulsivity in cocaine and heroin polysubstance abusers
Verdejo‐García, A., Perales, J. C., & Pérez-Garcı́a, M. (2006) · Addictive Behaviors · doi:10.1016/j.addbeh.2006.06.032 · Cited by 302 · see citing works
Lee, B. R., Ma, Y., Huang, Y. H., Wang, X., Otaka, M., Ishikawa, M., Neumann, P. A., Graziane, N., Brown, T. E., Beroun, A., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3533 · Cited by 297 · see citing works
Effects of Length of Abstinence on Decision-Making and Craving in Methamphetamine Abusers
Wang, G., Shi, J., Chen, N., Xu, L., Li, J., Li, P., Sun, Y., & Lu, L. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068791 · Cited by 261 · see citing works
Decision making and binge drinking: a longitudinal study
Goudriaan, A. E., Grekin, E. R., & Sher, K. J. (2007) · Alcoholism: Clinical and Experimental Research · doi:10.1111/j.1530-0277.2007.00378.x · Cited by 257 · see citing works
High Impulsivity Predicts Relapse to Cocaine-Seeking After Punishment-Induced Abstinence
Economidou, D., Pelloux, Y., Robbins, T. W., Dalley, J. W., & Everitt, B. J. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.12.008 · Cited by 234 · see citing works
The impact of orbitofrontal dysfunction on cocaine addiction
Lucantonio, F., Stalnaker, T. A., Shaham, Y., Niv, Y., & Schoenbaum, G. M. (2012) · Nature Neuroscience · doi:10.1038/nn.3014 · Cited by 210 · see citing works
Perry, J. L., Nelson, S. E., & Carroll, M. E. (2008) · Experimental and Clinical Psychopharmacology · doi:10.1037/1064-1297.16.2.165 · Cited by 200 · see citing works
Basolateral Amygdala Lesions Abolish Orbitofrontal-Dependent Reversal Impairments
Stalnaker, T. A., Franz, T. M., Singh, T., & Schoenbaum, G. M. (2007) · Neuron · doi:10.1016/j.neuron.2007.02.014 · Cited by 178 · see citing works
Robinson, E. S. J., Eagle, D. M., Economidou, D., Theobald, D. E. H., Mar, A. C., Murphy, E. R., Robbins, T. W., & Dalley, J. W. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.09.021 · Cited by 178 · see citing works
Zeeb, F. D., & Winstanley, C. A. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5597-10.2011 · Cited by 157 · see citing works
Self-citationNeural substrates of cognitive inflexibility after chronic cocaine exposure
Stalnaker, T. A., Takahashi, Y. K., Roesch, M. R., & Schoenbaum, G. M. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.07.019 · Cited by 151 · see citing works
Calu, D. J., Stalnaker, T. A., Franz, T. M., Singh, T., Shaham, Y., & Schoenbaum, G. M. (2007) · Learning & Memory · doi:10.1101/lm.534807 · Cited by 146 · see citing works
Besson, M., Belin, D., McNamara, R., Theobald, D. E., Castel, A., Beckett, V. L., Crittenden, B. M., Newman, A. H., Everitt, B. J., Robbins, T. W., et al. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.162 · Cited by 143 · see citing works
Mendez, I. A., Simon, N. W., Hart, N., Mitchell, M. R., Nation, J. R., Wellman, P. J., & Setlow, B. (2010) · Behavioral Neuroscience · doi:10.1037/a0020458 · Cited by 135 · see citing works
Context and repetition in word learning
Horst, J. S. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00149 · Cited by 129 · see citing works
González, R., Bechara, A., & Martin, E. M. (2006) · Journal of Clinical and Experimental Neuropsychology · doi:10.1080/13803390600582446 · Cited by 121 · see citing works
Zeeb, F. D., & Winstanley, C. A. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3971-12.2013 · Cited by 120 · see citing works
Self-citationUnpredictable saccharin reinforcement enhances locomotor responding to amphetamine
Singer, B. F., Scott-Railton, J., & Vezina, P. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.09.003 · Cited by 117 · see citing works
Adolescent Risk Taking, Cocaine Self-Administration, and Striatal Dopamine Signaling
Mitchell, M. R., Weiss, V. G., Beas, B. S., Morgan, D., Bizon, J. L., & Setlow, B. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.295 · Cited by 113 · see citing works
Zack, M., Featherstone, R. E., Mathewson, S., & Fletcher, P. J. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00036 · Cited by 108 · see citing works
Broos, N., Diergaarde, L., Schoffelmeer, A. N. M., Pattij, T., & Vries, T. J. D. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.323 · Cited by 96 · see citing works
Winstanley, C. A., Bachtell, R. K., Theobald, D. E. H., Laali, S., Green, T. A., Kumar, A., Chakravarty, S., Self, D. W., & Nestler, E. J. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn094 · Cited by 89 · see citing works
Self-citationParallel Roles for Dopamine in Pathological Gambling and Psychostimulant Addiction
Zack, M. H., & Poulos, C. X. (2009) · Current Drug Abuse Reviews · doi:10.2174/1874473710902010011 · Cited by 84 · see citing works
Affective Decision-Making Is Predictive of Three-Month Relapse in Polysubstance-Dependent Alcoholics
de Wilde, B., Verdéjo-Garcia, A., Sabbe, B., Hulstijn, W., & Dom, G. (2012) · European Addiction Research · doi:10.1159/000339290 · Cited by 67 · see citing works
Cervantes, M. C., Laughlin, R. E., & Jentsch, J. D. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3135-4 · Cited by 55 · see citing works
Stevens, L., Espinosa, P. B., Crunelle, C. L., Vergara‐Moragues, E., Roeyers, H., Lozano, O. M., Dom, G., González‐Sáiz, F., Vanderplasschen, W., Verdejo‐García, A., et al. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00149 · Cited by 55 · see citing works
Barrus, M. M., Hosking, J. G., Zeeb, F. D., Tremblay, M., & Winstanley, C. A. (2015) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.140045 · Cited by 55 · see citing works
Self-citationPaine, T. A., Asinof, S. K., Diehl, G. W., Frackman, A., & Leffler, J. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.01.018 · Cited by 53 · see citing works
Cocaine-induced decision-making deficits are mediated by miscoding in basolateral amygdala
Stalnaker, T. A., Roesch, M. R., Franz, T. M., Calu, D. J., Singh, T., & Schoenbaum, G. M. (2007) · Nature Neuroscience · doi:10.1038/nn1931 · Cited by 53 · see citing works
Mitchell, M. R., Weiss, V. G., Ouimet, D. J., Fuchs, R. A., Morgan, D., & Setlow, B. (2014) · Behavioral Neuroscience · doi:10.1037/a0036742 · Cited by 50 · see citing works
Wang, G.-B., Zhang, X.-L., Zhao, L.-Y., Sun, L.-L., Wu, P., Lu, L., & Shi, J. (2012) · Psychopharmacology · doi:10.1007/s00213-011-2617-5 · Cited by 46 · see citing works
Tremblay, M., Cocker, P. J., Hosking, J. G., Zeeb, F. D., Rogers, R. D., & Winstanley, C. A. (2014) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-014-0271-1 · Cited by 42 · see citing works
Self-citationPotenza, M. N. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.152 · Cited by 42 · see citing works
Duka, T., Crombag, H. S., & Stephens, D. (2010) · Journal of Psychopharmacology · doi:10.1177/0269881110388324 · Cited by 35 · see citing works
Responsibility and Choice in Addiction
Committee on Addictions of the Group for the Advancement of Psychiatry (2002) · Psychiatric Services · doi:10.1176/appi.ps.53.6.707 · Cited by 22 · see citing works
Broos, N., Loonstra, R., van Mourik, Y., Schetters, D., Schoffelmeer, A. N. M., Pattij, T., & Vries, T. J. D. (2014) · Addiction Biology · doi:10.1111/adb.12168 · Cited by 21 · see citing works
Tse, M., Cantor, A., & Floresco, S. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1810-11.2011 · Cited by 20 · see citing works
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Hellberg, S. N., Russell, T. I., & Robinson, M. J. F. (2019) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-018-00662-3 · Cited by 65 · see citing works
Addiction, cognitive decline and therapy: Seeking ways to escape a vicious cycle
Perry, C. J., & Lawrence, A. J. (2017) · Genes, Brain and Behavior · doi:10.1111/gbb.12325 · Cited by 60 · see citing works
Ahmed, S. H. (2018) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.07.005 · Cited by 39 · see citing works
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- Authors
- Ferland, J. N., & Winstanley, C. A.
- Affiliations
- University of British Columbia (CA)
- Corresponding author
- Ferland, Jacqueline‐Marie N.
- Venue
- Addiction Biology
- Publisher
- Wiley
- Published
- 2016-03-22
- Volume
- 22
- Issue
- 4
- Pages
- 991-1001
- ISSN
- 1355-6215 (ISSN-L)
- 1369-1600
- OpenAlex
- W2309365610
- Cited by
- 72
- References
- 54
- Citations by year
- 2026: 5 · 2025: 4 · 2024: 5 · 2023: 5 · 2022: 4 · 2021: 9 · 2020: 6 · 2019: 12 · 2018: 11 · 2017: 7 · 2016: 3
- FWCI
- 6.17
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Addiction Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Michael Smith Health Research BC
- Canadian Institutes of Health Research
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Health Sciences › Medicine › Epidemiology › Substance Abuse Treatment and Outcomes
- Keywords
- risk preferences, risky decision making, cocaine self-administration, cocaine withdrawal, cue-induced craving, drug-seeking behavior, addiction vulnerability, relapse
- MeSH terms
- Animals, Behavior, Animal, Cocaine, Decision Making, Disease Models, Animal, Male, Risk, Self Administration, Dopamine Uptake Inhibitors, Cocaine-Related Disorders, Rats, Long-Evans, Rats, Craving
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