Extended Heroin Access Increases Heroin Choices Over a Potent Nondrug Alternative
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Epidemiological research shows that the proportion of drug users who become addicted to heroin is higher than to cocaine. Here we tested whether this difference could be due to a difference in the addiction liability between the two drugs. Addiction liability was assessed under a discrete-trials choice procedure by measuring the proportion of rats that prefer the drug over a potent alternative reward (ie, water sweetened with saccharin). Previous research on choice between self-administration of i.v. cocaine or sweet water showed that the proportion of cocaine-preferring rats remains relatively low and invariable (ie, 15%), even after extended drug access and regardless of past drug consumption (ie, total drug use before choice testing). By contrast, the present study shows that under similar choice conditions, the proportion of heroin-preferring rats considerably increases with extended heroin access (6-9 h per day for several weeks) and with past heroin consumption, from 11 to 51% at the highest past drug consumption level. At this level, the proportion of drug-preferring rats was about three times higher with heroin than with cocaine (51% vs 15%). This increase in the rate of heroin preference after extended heroin access persisted even after recovery from acute heroin withdrawal. Overall, these findings show that choice procedures are uniquely sensitive to different drugs and suggest that heroin is more addictive than cocaine. This higher addiction liability may contribute to explain why more drug users become addicted to heroin than to cocaine in epidemiological studies.
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In rodent studies, choice procedures are resistant to disruption, and a large proportion of rats continue to select a sweet solution rather than the drug even after clear establishment of dependence.
“In rodent studies, choice procedures are notoriously resistant to disruption, and a large proportion of rats continue to select a sweet solution (e.g., saccharin) rather than the drug even after the clear establishment of dependence (Lenoir et al., 2013;Ahmed, 2018).”
From Drug Addiction: Hyperkatifeia/Negative Reinforcement as a Framework for Medications Development (2021) · cites this paper as Lenoir et al., 2013
The Results (page unavailable) show that 8 of 20 rats with extended heroin access still preferred saccharin, and the Discussion describes markers of dependence in that group. But extended access also increased heroin preference from 25% to 60%, so describing the choice procedure as resistant to disruption without that qualification overstates this paper's finding. (LLM, conf=0.86)
Experimental — accuracy not yet measuredIn animal models, animals extensively trained to self-administer drugs will readily forego the drug if offered a potent non-drug alternative.
“The critical role of alternative reinforcers was elegantly brought into modern neuroscience by Ahmed et al., who showed that rats extensively trained to self-administer cocaine would readily forego the drug if offered a sweet solution as an alternative [103].This was later also found to be the case for heroin [103], methamphetamine [104] and alcohol [105].”
From Addiction as a brain disease revised: why it still matters, and the need for consilience (2021) · cites this paper as [103]
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Cites
Drug Addiction, Dysregulation of Reward, and Allostasis
Koob, G. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(00)00195-0 · Cited by 2,953 · see citing works
Drugs of abuse: anatomy, pharmacology and function of reward pathways
Koob, G. F. (1992) · Trends in Pharmacological Sciences · doi:10.1016/0165-6147(92)90060-j · Cited by 2,070 · see citing works
Avena, N. M., Rada, P., & Hoebel, B. G. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.04.019 · Cited by 1,358 · see citing works
Richardson, N. R., & Roberts, D. C. S. (1996) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(95)00153-0 · Cited by 1,357 · see citing works
Anthony, J. C., Warner, L. A., & Kessler, R. C. (1994) · Experimental and Clinical Psychopharmacology · doi:10.1037/1064-1297.2.3.244 · Cited by 1,341 · see citing works
A Role for Brain Stress Systems in Addiction
Koob, G. F. (2008) · Neuron · doi:10.1016/j.neuron.2008.06.012 · Cited by 1,056 · see citing works
Stress-induced obesity and the emotional nervous system
Dallman, M. F. (2010) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2009.10.004 · Cited by 814 · see citing works
Self-administration of psychoactive substances by the monkey
Deneau, G. A., Yanagita, T., & Seevers, M. H. (1969) · Psychopharmacology · doi:10.1007/bf00405254 · Cited by 811 · see citing works
Berridge, K. C. (2003) · Brain and Cognition · doi:10.1016/s0278-2626(03)00014-9 · Cited by 694 · see citing works
Intense Sweetness Surpasses Cocaine Reward
Lenoir, M., Serre, F., Cantin, L., & Ahmed, S. H. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000698 · Cited by 608 · see citing works
Self-citationHeroin 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 · see citing works
Evidence That Intermittent, Excessive Sugar Intake Causes Endogenous Opioid Dependence
Colantuoni, C., Rada, P. V., McCarthy, J., Patten, C. S., Avena, N. M., Chadeayne, A., & Hoebel, B. G. (2002) · Obesity Research · doi:10.1038/oby.2002.66 · Cited by 544 · see citing works
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 466 · see citing works
Disentangling pleasure from incentive salience and learning signals in brain reward circuitry
Smith, K. S., Berridge, K. C., & Aldridge, J. W. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1101920108 · Cited by 464 · see citing works
Smith, K. S., & Berridge, K. C. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4205-06.2007 · Cited by 450 · see citing works
Hedonic Hot Spots in the Brain
Peciña, S., Smith, K. S., & Berridge, K. C. (2006) · The Neuroscientist · doi:10.1177/1073858406293154 · Cited by 441 · see citing works
Arnold, J. M., & Roberts, D. C. S. (1997) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(96)00445-5 · Cited by 390 · see citing works
Common cellular and molecular mechanisms in obesity and drug addiction
Kenny, P. J. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3105 · Cited by 382 · see citing works
Persistent Increase in the Motivation to Take Heroin in Rats with a History of Drug Escalation
Ahmed, S. H. (2000) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00133-5 · Cited by 361 · see citing works
Self-citationEveritt, B. J., & Robbins, T. W. (2000) · Psychopharmacology · doi:10.1007/s002130000566 · Cited by 306 · see citing works
Conditioned Withdrawal Drives Heroin Consumption and Decreases Reward Sensitivity
Kenny, P. J., Chen, S. A., Kitamura, O., Markou, A., & Koob, G. F. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0740-06.2006 · Cited by 268 · see citing works
Arroyo, M., Markou, A., Robbins, T. W., & Everitt, B. J. (1998) · Psychopharmacology · doi:10.1007/s002130050774 · Cited by 251 · see citing works
Ahmed, S. H. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.04.005 · Cited by 240 · see citing works
Self-citationCiraulo, D. A. (2003) · JAMA · doi:10.1001/jama.289.23.3175-b · Cited by 232 · see citing works
Shaham, Y., Rajabi, H., & Stewart, J. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-05-01957.1996 · Cited by 218 · see citing works
The role of withdrawal in heroin addiction: enhances reward or promotes avoidance?
Hutcheson, D. M., Everitt, B. J., Robbins, T. W., & Dickinson, A. (2001) · Nature Neuroscience · doi:10.1038/nn0901-943 · Cited by 205 · see citing works
The science of making drug-addicted animals
Ahmed, S. H. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.014 · Cited by 197 · see citing works
Self-citationOpiate agonists microinjected into the nucleus accumbens enhance sucrose drinking in rats
Zhang, M., & Kelley, A. E. (1997) · Psychopharmacology · doi:10.1007/s002130050355 · Cited by 191 · see citing works
Cocaine Is Low on the Value Ladder of Rats: Possible Evidence for Resilience to Addiction
Cantin, L., Lenoir, M., Augier, E., Vanhille, N., Dubreucq, S., Serre, F., Vouillac‐Mendoza, C., & Ahmed, S. H. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011592 · Cited by 190 · see citing works
Self-citationBDNF is a negative modulator of morphine action
Koo, J. W., Mazei-Robison, M. S., Chaudhury, D., Juarez, B., LaPlant, Q., Ferguson, D., Feng, J., Sun, H., Scobie, K. N., Damez-Werno, D., et al. (2012) · Science · doi:10.1126/science.1222265 · Cited by 189 · see citing works
Animal model for investigating the anxiogenic effects of self-administered cocaine
Ettenberg, A., & Geist, T. D. (1991) · Psychopharmacology · doi:10.1007/bf02244244 · Cited by 181 · see citing works
Recent advances in the genetic epidemiology and molecular genetics of substance use disorders
Kendler, K. S., Chen, X., Dick, D., Maes, H., Gillespie, N., Neale, M. C., & Riley, B. (2012) · Nature Neuroscience · doi:10.1038/nn.3018 · Cited by 179 · see citing works
Dissociation of Psychomotor Sensitization from Compulsive Cocaine Consumption
Ahmed, S. H., & Cador, M. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300834 · Cited by 158 · see citing works
Self-citationOpponent process properties of self-administered cocaine
Ettenberg, A. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2003.11.009 · Cited by 149 · see citing works
Parker, L. A., Maier, S., Rennie, M., & Crebolder, J. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.6.999 · Cited by 142 · see citing works
Models of relative reinforcing efficacy of drugs and their predictive utility
Katz, J. L. (1990) · Behavioural Pharmacology · doi:10.1097/00008877-199000140-00003 · Cited by 137 · see citing works
Self‐administration of cocaine, cannabis and heroin in the human laboratory: benefits and pitfalls
Haney, M. (2008) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00121.x · Cited by 134 · see citing works
Martínez, D., Slifstein, M., Narendran, R., Foltin, R. W., Broft, A. I., Hwang, D., Perez, A. Y., Abi‐Dargham, A., Fischman, M. W., Kleber, H. D., et al. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.235 · Cited by 129 · see citing works
Negus, S. S. (2006) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.105.095380 · Cited by 128 · see citing works
Parker, L. A., Maier, S., Rennie, M., et al. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.6.999 · Cited by 126 · see citing works
Sex Differences in Selecting Between Food and Cocaine Reinforcement are Mediated by Estrogen
Kerstetter, K. A., Ballis, M. A., Duffin-Lutgen, S., Carr, A. E., Behrens, A. M., & Kippin, T. E. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.99 · Cited by 119 · see citing works
Lenoir, M., & Ahmed, S. H. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301083 · Cited by 110 · see citing works
Self-citationMorphine Tolerance in Genetically Selected Rats Induced by Chronically Elevated Saccharin Intake
Lieblich, I., Cohen, E., Ganchrow, J. R., Blass, E. M., & Bergmann, F. (1983) · Science · doi:10.1126/science.6879185 · Cited by 108 · see citing works
Tolerance and cross-tolerance to cocaine and d-amphetamine.
Woolverton, W. L., Kandel, D. A., & Schuster, C. R. (1978) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)31260-7 · Cited by 102 · see citing works
Yanagita, T. (1973) · Bulletin on narcotics · Cited by 100 · see citing works
Epidemiology of Drug Dependence
Anthony, J. C., & Helzer, J. E. (2002) · Wiley eBooks · doi:10.1002/0471234311.ch20 · Cited by 97 · see citing works
Chen, S. A., O'Dell, L. E., Hoefer, M. E., Greenwell, T. N., Zorrilla, E. P., & Koob, G. F. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301008 · Cited by 97 · see citing works
Supply of a Nondrug Substitute Reduces Escalated Heroin Consumption
Lenoir, M., & Ahmed, S. H. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301602 · Cited by 96 · see citing works
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 · see citing works
Ettenberg, A., & Geist, T. D. (1993) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(93)90298-8 · Cited by 91 · see citing works
Conditioned preferences in the rat with an unnatural need state: Morphine withdrawal.
Parker, L. F., Failor, A., & Weidman, K. (1973) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0033921 · Cited by 87 · see citing works
Escalation patterns of varying periods of heroin access
Vendruscolo, L. F., Schlosburg, J. E., Misra, K., Chen, S. A., Greenwell, T. N., & Koob, G. F. (2011) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.03.004 · Cited by 79 · see citing works
Negus, S. S., & Rice, K. C. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.127 · Cited by 70 · cited 5× · see citing works
“Both conditioned and unconditioned heroin or morphine withdrawal has previously been demonstrated to increase responding for heroin in rats (Shaham et al, 1996; Kenny et al, 2006) and heroin choices in monkeys, especially at the lowest doses of heroin tested (Negus, 2006; Negus and Rice, 2009).”
BackgroundResultInfluentialWard, S. J., Morgan, D., & Roberts, D. C. S. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300560 · Cited by 68 · see citing works
Central enhancement of taste pleasure by intraventricular morphine.
Peciña, S., & Berridge, K. C. (1995) · PubMed · Cited by 63 · see citing works
Animal models for assessing drugs of abuse
Brady, J. V. (1991) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80089-2 · Cited by 53 · see citing works
(2011) · Wiley eBooks · doi:10.1002/9781118023150 · Cited by 52 · see citing works
Diazepam promotes choice of abstinence in cocaine self‐administering rats
Augier, E., Vouillac‐Mendoza, C., & Ahmed, S. H. (2011) · Addiction Biology · doi:10.1111/j.1369-1600.2011.00368.x · Cited by 47 · see citing works
Self-citationWalsh, S., Donny, E. C., Nuzzo, P. A., Umbricht, A., & Bigelow, G. (2009) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2009.07.011 · Cited by 46 · see citing works
Alderson, H. L., Robbins, T. W., & Everitt, B. J. (2000) · Psychopharmacology · doi:10.1007/s002130000429 · Cited by 43 · see citing works
Banks, M. L., & Negus, S. S. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.154 · Cited by 38 · see citing works
Influence of sweet tasting solutions on opioid withdrawal
Jain, R., Mukherjee, K., & Singh, R. (2004) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2004.08.003 · Cited by 35 · see citing works
Drug specificity in extended access cocaine and heroin self‐administration
Lenoir, M., Guillem, K., Koob, G. F., & Ahmed, S. H. (2011) · Addiction Biology · doi:10.1111/j.1369-1600.2011.00385.x · Cited by 30 · see citing works
Self-citationIntake of and preference for sweet solutions are attenuated in morphine-withdrawn rats.
Lieblich, I., Yirmiya, R., & Liebeskind, J. C. (1991) · Behavioral Neuroscience · doi:10.1037//0735-7044.105.6.965 · Cited by 29 · see citing works
Chronic opioid exposure produces increased heroin self-administration in rats
Walker, J. R., Chen, S. A., Moffitt, H., Inturrisi, C. E., & Koob, G. F. (2003) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(03)00094-7 · Cited by 28 · see citing works
Sj, C. (1982) · PubMed · Cited by 28 · see citing works
Intake of and preference for sweet solutions are attenuated in morphine-withdrawn rats.
Lieblich, I., Yirmiya, R., & Liebeskind, J. C. (1991) · Behavioral Neuroscience · doi:10.1037/0735-7044.105.6.965 · Cited by 25 · see citing works
Negus, S. S., & Banks, M. L. (2011) · doi:10.1002/9781118023150.ch11 · Cited by 21 · see citing works
Indicated Preference for Drugs of Abuse
Kliner, D. J., & Pickens, R. W. (1982) · International Journal of the Addictions · doi:10.3109/10826088209064057 · Cited by 10 · see citing works
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Volkow, N. D., Michaelides, M., & Baler, R. (2019) · Physiological Reviews · doi:10.1152/physrev.00014.2018 · Cited by 863 · see citing works
Drug Addiction: Hyperkatifeia/Negative Reinforcement as a Framework for Medications Development
Koob, G. F. (2021) · Pharmacological Reviews · doi:10.1124/pharmrev.120.000083 · Cited by 337 · see citing works
Hogarth, L. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0600-8 · Cited by 281 · see citing works
Food addiction: a valid concept?
Fletcher, P. C., & Kenny, P. J. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0203-9 · Cited by 224 · see citing works
Improving translation of animal models of addiction and relapse by reverse translation
Venniro, M., Banks, M. L., Heilig, M., Epstein, D. H., & Shaham, Y. (2020) · Nature Reviews Neuroscience · doi:10.1038/s41583-020-0378-z · Cited by 212 · see citing works
Imaging addiction: D2 receptors and dopamine signaling in the striatum as biomarkers for impulsivity
Trifilieff, P., & Martinez, D. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.06.031 · Cited by 171 · see citing works
Vènniro, M., Zhang, M. H., Shaham, Y., & Caprioli, D. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.287 · Cited by 147 · see citing works
Insights 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 144 · see citing works
Neurobiology of addiction versus drug use driven by lack of choice
Ahmed, S. H., Lenoir, M., & Guillem, K. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.01.028 · Cited by 135 · see citing works
Self-citationRelapse to opioid seeking in rat models: behavior, pharmacology and circuits
Reiner, D. J., Fredriksson, I., Lofaro, O. M., Bossert, J. M., & Shaham, Y. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0234-2 · Cited by 131 · see citing works
Sex differences in opioid reinforcement under a fentanyl vs. food choice procedure in rats
Townsend, E. A., Negus, S. S., Caine, S. B., Thomsen, M., & Banks, M. L. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0356-1 · Cited by 101 · see citing works
Animal Models of Drug Relapse and Craving after Voluntary Abstinence: A Review
Fredriksson, I., Vènniro, M., Reiner, D. J., Chow, J. J., Bossert, J. M., & Shaham, Y. (2021) · Pharmacological Reviews · doi:10.1124/pharmrev.120.000191 · Cited by 99 · see citing works
Perry, A. N., Westenbroek, C., & Becker, J. B. (2013) · PLoS ONE · doi:10.1371/journal.pone.0079465 · Cited by 95 · see citing works
Compulsive Addiction-like Aggressive Behavior in Mice
Golden, S. A., Heins, C., Vènniro, M., Caprioli, D., Zhang, M. H., Epstein, D. H., & Shaham, Y. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.03.004 · Cited by 93 · see citing works
Consolidating the Circuit Model for Addiction
Lüscher, C., & Janak, P. H. (2021) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-092920-123905 · Cited by 88 · see citing works
George, O., Koob, G. F., & Vendruscolo, L. F. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3623-1 · Cited by 84 · see citing works
Non-pharmacological factors that determine drug use and addiction
Ahmed, S. H., Badiani, A., Miczek, K. A., & Müller, C. P. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.08.015 · Cited by 82 · see citing works
Self-citationSchmeichel, B. E., Barbier, E., Misra, K. K., Contet, C., Schlosburg, J. E., Grigoriadis, D., Williams, J. P., Karlsson, C., Pitcairn, C., Heilig, M., et al. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.293 · Cited by 79 · see citing works
Drug versus sweet reward: greater attraction to and preference for sweet versus drug cues
Madsen, H. B., & Ahmed, S. H. (2014) · Addiction Biology · doi:10.1111/adb.12134 · Cited by 79 · see citing works
Self-citationSign-tracking predicts increased choice of cocaine over food in rats
Tunstall, B. J., & Kearns, D. N. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.12.034 · Cited by 76 · see citing works
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 · see citing works
Self-citationReiner, D. J., Lofaro, O. M., Applebey, S. V., Korah, H. E., Vènniro, M., Cifani, C., Bossert, J. M., & Shaham, Y. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.2693-19.2020 · Cited by 70 · see citing works
Modeling the development of drug addiction in male and female animals
Lynch, W. J. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.06.006 · Cited by 70 · see citing works
Townsend, E. A., Blake, S., Faunce, K. E., Hwang, C. S., Natori, Y., Zhou, B., Bremer, P. T., Janda, K. D., & Banks, M. L. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0385-9 · Cited by 68 · see citing works
Vandaele, Y., Cantin, L., Serre, F., Vouillac‐Mendoza, C., & Ahmed, S. H. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.195 · Cited by 63 · see citing works
Self-citationPunishment models of addictive behavior
Vanderschuren, L. J. M. J., Minnaard, A. M., Smeets, J. A. S., & Lesscher, H. M. B. (2016) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2016.10.007 · Cited by 60 · see citing works
Drugs of abuse hijack a mesolimbic pathway that processes homeostatic need
Tan, B., Browne, C. J., Nöbauer, T., Vaziri, A., Friedman, J. M., & Nestler, E. J. (2024) · Science · doi:10.1126/science.adk6742 · Cited by 57 · see citing works
Townsend, E. A., Schwienteck, K. L., Robinson, H. L., Lawson, S. T., & Banks, M. L. (2021) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2021.109110 · Cited by 56 · see citing works
Zhang, Y., Mayer-Blackwell, B., Schlussman, S. D., Randesi, M., Butelman, E. R., Ho, A., Ott, J., & Kreek, M. J. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3306-3 · Cited by 52 · see citing works
Canchy, L., Girardeau, P., Durand, A., Vouillac‐Mendoza, C., & Ahmed, S. H. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0786-9 · Cited by 51 · see citing works
Self-citationTownsend, E. A., Kim, R. K., Robinson, H. L., Marsh, S. A., Banks, M. L., & Hamilton, P. J. (2021) · Biological Psychiatry Global Open Science · doi:10.1016/j.bpsgos.2021.04.009 · Cited by 49 · see citing works
A Choice‐Based Screening Method for Compulsive Drug Users in Rats
Lenoir, M., Augier, E., Vouillac‐Mendoza, C., & Ahmed, S. H. (2013) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0944s64 · Cited by 48 · see citing works
Self-citationAarde, S. M., Huang, P.-K., Dickerson, T. J., & Taffe, M. A. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3819-4 · Cited by 47 · see citing works
de Guglielmo, G., Kallupi, M., Sedighim, S., Newman, A. H., & George, O. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00292 · Cited by 46 · see citing works
Essential values of cocaine and non‐drug alternatives predict the choice between them
Kearns, D. N., Kim, J. S., Tunstall, B. J., & Silberberg, A. M. (2016) · Addiction Biology · doi:10.1111/adb.12450 · Cited by 43 · see citing works
Imperio, C. G., McFalls, A. J., Hadad, N., Blanco-Berdugo, L., Masser, D. R., Colechio, E. M., Coffey, A. A., Bixler, G. V., Stanford, D. R., Vrana, K. E., et al. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.06.037 · Cited by 43 · 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
Self-citationUrbanik, L. A., Acharya, N., & Grigson, P. S. (2022) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2022.08.023 · Cited by 38 · see citing works
Negus, S. S., & Banks, M. L. (2018) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.04.006 · Cited by 34 · see citing works
Panlilio, L. V., Secci, M. E., Schindler, C. W., & Bradberry, C. W. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4726-2 · Cited by 34 · see citing works
Exercise decreases speedball self-administration
Lacy, R. T., Strickland, J. C., Brophy, M. K., Witte, M. A., & Smith, M. A. (2014) · Life Sciences · doi:10.1016/j.lfs.2014.08.005 · Cited by 34 · see citing works
Targeting the subthalamic nucleus in a preclinical model of alcohol use disorder
Pelloux, Y., & Baunez, C. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4618-5 · Cited by 34 · see citing works
Drug specificity in drug versus food choice in male rats.
Tunstall, B. J., Riley, A. L., & Kearns, D. N. (2014) · Experimental and Clinical Psychopharmacology · doi:10.1037/a0037019 · Cited by 33 · see citing works
Imperio, C. G., McFalls, A. J., Colechio, E. M., Masser, D. R., Vrana, K. E., Grigson, P. S., & Freeman, W. M. (2015) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2015.12.005 · Cited by 31 · see citing works
A common limiter circuit for opioid choice and relapse identified in a rodent addiction model
Heinsbroek, J. A., Giannotti, G., Mandel, M. R., Josey, M., Aston‐Jones, G., James, M. H., & Peters, J. (2021) · Nature Communications · doi:10.1038/s41467-021-25080-x · Cited by 30 · see citing works
Corticosteroid sensitization drives opioid addiction
Carmack, S. A., Vendruscolo, J. C. M., McGinn, M. A., Miranda-Barrientos, J. A., Repunte‐Canonigo, V., Bossé, G. D., Mercatelli, D., Giorgi, F. M., Fu, Y., Hinrich, A. J., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01501-1 · Cited by 29 · see citing works
Heroin and saccharin demand and preference in rats
Schwartz, L. P., Kim, J. S., Silberberg, A. M., & Kearns, D. N. (2017) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2017.04.031 · Cited by 29 · see citing works
Effects of alcohol dependence on discrete choice between alcohol and saccharin
Russo, M., Funk, D. R., Loughlin, A., Coen, K. M., & Lê, A. D. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0101-1 · Cited by 29 · see citing works
Animal Models of the Behavioral Symptoms of Substance Use DisordersPreprint
Vanderschuren, L. J. M. J., & Ahmed, S. H. (2020) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a040287 · Cited by 28 · see citing works
Self-citationImperio, C. G., & Grigson, P. S. (2015) · Behavioral Neuroscience · doi:10.1037/bne0000069 · Cited by 27 · see citing works
Augier, E. (2021) · Alcohol and Alcoholism · doi:10.1093/alcalc/agab003 · Cited by 27 · see citing works
Remifentanil-food choice follows predictions of relative subjective value
Chow, J. J., & Beckmann, J. S. (2020) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2020.108369 · Cited by 26 · see citing works
Wistar rats choose alcohol over social interaction in a discrete-choice model
Augier, G., Schwabl, V., Lguensat, A., Atudorei, M., Iyere, O. C., Solander, S. E., & Augier, E. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01526-8 · Cited by 26 · see citing works
Concurrent access to nicotine and sucrose in rats
Panlilio, L. V., Hogarth, L., & Shoaib, M. C. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3787-8 · Cited by 26 · see citing works
Sedighim, S., Carrette, L. L. G., Vènniro, M., Shaham, Y., de Guglielmo, G., & George, O. (2021) · Psychopharmacology · doi:10.1007/s00213-021-05961-1 · Cited by 25 · see citing works
Medications Development for Treatment of Opioid Use DisorderPreprint
Townsend, E. A., Negus, S. S., & Banks, M. L. (2020) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a039263 · Cited by 25 · see citing works
Choice between delayed food and immediate oxycodone in rats
Secci, M. E., Factor, J., Schindler, C. W., & Panlilio, L. V. (2016) · Psychopharmacology · doi:10.1007/s00213-016-4429-0 · Cited by 22 · see citing works
Neuronal representation of individual heroin choices in the orbitofrontal cortex
Guillem, K., Brenot, V., Durand, A., & Ahmed, S. H. (2017) · Addiction Biology · doi:10.1111/adb.12536 · Cited by 22 · see citing works
Self-citationThe effects of heroin administration and drug cues on impulsivity
Jones, J. D., Vadhan, N. P., Luba, R. R., & Comer, S. D. (2016) · Journal of Clinical and Experimental Neuropsychology · doi:10.1080/13803395.2016.1156652 · Cited by 22 · see citing works
Augier, E., Dulman, R. S., Singley, E., & Heilig, M. A. (2017) · Journal of Visualized Experiments · doi:10.3791/53305 · Cited by 22 · see citing works
Strickland, J. C., Stoops, W. W., Banks, M. L., & Gipson, C. D. (2022) · Journal of the Experimental Analysis of Behavior · doi:10.1002/jeab.757 · Cited by 21 · see citing works
de Guglielmo, G., Carrette, L. L. G., Kallupi, M., Brennan, M., Boomhower, B., Maturin, L., Conlisk, D., Sedighim, S., Tieu, L., Fannon, M. J., et al. (2023) · eLife · doi:10.7554/elife.90422.3 · Cited by 20 · see citing works
Insights into the Neurobiology of Craving in Opioid Use Disorder
Lueptow, L. M., Shashkova, E., Miller, M. G., Evans, C. J., & Cahill, C. M. (2020) · Current anesthesiology reports · doi:10.1007/s40140-020-00420-7 · Cited by 19 · see citing works
Pre-trial cocaine biases choice toward cocaine through suppression of the nondrug option
Freese, L., Durand, A., Guillem, K., & Ahmed, S. H. (2018) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2018.07.010 · Cited by 17 · see citing works
Self-citationHardy, L., Parker, S., Hartley, L., & Hogarth, L. (2018) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000421 · Cited by 17 · see citing works
Misdeed of the need: towards computational accounts of transition to addiction
Keramati, M., Ahmed, S. H., & Gutkin, B. S. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.08.014 · Cited by 17 · see citing works
Self-citation“A Walk on the Wild Side” of Addiction
Ahmed, S. H. (2018) · Routledge eBooks · doi:10.4324/9781315689197-17 · Cited by 14 · see citing works
Self-citationAlaux‐Cantin, S., Alarcon, R., Audegond, C., O'Brien, E. S., Martinetti, M. P., Ahmed, S. H., Nalpas, B., Perney, P., & Naassïla, M. (2021) · Addiction Biology · doi:10.1111/adb.13023 · Cited by 13 · see citing works
Self-citationExposure to sucrose during periods of withdrawal does not reduce cocaine-seeking behavior in rats
Nicolas, C., Lafay‐Chebassier, C., & Solinas, M. (2016) · Scientific Reports · doi:10.1038/srep23272 · Cited by 13 · see citing works
The effect of economy type on heroin and saccharin essential value.
Gunawan, T., Tripoli, C. S., Silberberg, A. M., & Kearns, D. N. (2019) · Experimental and Clinical Psychopharmacology · doi:10.1037/pha0000277 · Cited by 13 · see citing works
Heroin choice depends on income level and economy type
Gunawan, T., Hachiga, Y., Tripoli, C. S., Silberberg, A. M., & Kearns, D. N. (2020) · Psychopharmacology · doi:10.1007/s00213-020-05471-6 · Cited by 12 · see citing works
Kallupi, M., de Guglielmo, G., Carrette, L. L. G., Simpson, S., Kononoff, J., Kimbrough, A., Smith, L., Shankar, K., Avelar, A., Conlisk, D., et al. (2026) · Neuropsychopharmacology · doi:10.1038/s41386-026-02348-8 · Cited by 11 · see citing works
Onge, C. M. S., Taylor, K. M., Marcus, M. M., & Townsend, E. A. (2022) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2022.173473 · Cited by 11 · see citing works
Cocaine and heroin interact differently with nondrug reinforcers in a choice situation.
Beasley, M. M., Amantini, S., Gunawan, T., Silberberg, A. M., & Kearns, D. N. (2023) · Experimental and Clinical Psychopharmacology · doi:10.1037/pha0000674 · Cited by 10 · see citing works
Quantifying value-based determinants of drug and non-drug decision dynamics
Smith, A. P., & Beckmann, J. S. (2021) · Psychopharmacology · doi:10.1007/s00213-021-05830-x · Cited by 9 · see citing works
Kim, J. S., & Kearns, D. N. (2019) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2019.172744 · Cited by 9 · see citing works
Carey, L. M., Maguire, D. R., & France, C. P. (2023) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2023.109787 · Cited by 9 · see citing works
A Review of Behavioral Economic Manipulations Affecting Drug versus Nondrug Choice in Rats
Kearns, D. N. (2025) · Perspectives on Behavior Science · doi:10.1007/s40614-025-00445-5 · Cited by 8 · see citing works
Choosing between cocaine and sucrose under the influence: testing the effect of cocaine tolerance
Vandaele, Y., & Ahmed, S. H. (2021) · Psychopharmacology · doi:10.1007/s00213-021-05987-5 · Cited by 8 · see citing works
Self-citationEarly avoidance of a heroin-paired taste-cue and subsequent addiction-like behavior in rats
Jenney, C. B., Petko, J., Ebersole, B., Njatcha, C. V. N., Uzamere, T. O., Alexander, D. N., Grigson, P. S., & Levenson, R. G. (2015) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2015.10.008 · Cited by 8 · see citing works
Probing the decision-making mechanisms underlying choice between drug and nondrug rewards in rats
Vandaele, Y., Lenoir, M., Vouillac‐Mendoza, C., Guillem, K., & Ahmed, S. H. (2021) · eLife · doi:10.7554/elife.64993 · Cited by 7 · see citing works
Self-citationNeural circuits controlling choice behavior in opioid addiction
Chang, V. N., & Peters, J. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109407 · Cited by 7 · see citing works
Cocaine falls into oblivion during volitional initiation of choice trials
Vandaele, Y., Augier, E., Vouillac‐Mendoza, C., & Ahmed, S. H. (2022) · Addiction Biology · doi:10.1111/adb.13235 · Cited by 7 · see citing works
Self-citationScarlata, M., Keeley, R. J., Carmack, S., P-J, T., Vendruscolo, J. C. M., Lu, H., Koob, G. F., Vendruscolo, L. F., & Stein, E. A. (2021) · Addiction Neuroscience · doi:10.1016/j.addicn.2021.100002 · Cited by 5 · see citing works
Nall, R. W., Chalhoub, R., & Kalivas, P. W. (2022) · Journal of the Experimental Analysis of Behavior · doi:10.1002/jeab.752 · Cited by 5 · see citing works
Luo, Y., Huang, D., Guo, C., & Ma, Y. (2020) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13469 · Cited by 4 · see citing works
Paronis, C. A. (2013) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e328364c006 · Cited by 3 · see citing works
Neurobiological theories of addiction
Koob, G. F., Arends, M. A., McCracken, M. L., & Moal, M. L. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-816863-9.00003-0 · Cited by 3 · see citing works
Kim, S., Huang, Y., Singla, U., Hu, A., Kalra, S., Morgan, A. A., Sichel, B. C., Othman, D. N., & Carrette, L. L. G. (2025) · NPP—Digital Psychiatry and Neuroscience · doi:10.1038/s44277-025-00046-9 · Cited by 2 · see citing works
Samaha, A. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-00836-z · Cited by 2 · see citing works
Mile high on heroin: Lessons on the opioid epidemic from the Mile High City
Peters, J. (2022) · BioEssays · doi:10.1002/bies.202100297 · Cited by 2 · see citing works
Khoo, S. Y. (2020) · Journal for Reproducibility in Neuroscience · doi:10.31885/jrn.1.2020.1318 · Cited by 2 · see citing works
Shab, G., Fultz, E. K., Page, A., Coelho, M. A., Brewin, L. W., Stailey, N., Brown, C. N., Bryant, C. D., Kippin, T. E., & Szumlinski, K. K. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112959 · Cited by 2 · see citing works
Koob, G. F., Arends, M. A., McCracken, M. L., & Moal, M. L. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-816863-9.00002-9 · Cited by 2 · see citing works
Stull, S. W., Epstein, D. H., Gersz, M., Mondry, L., & Lanza, S. T. (2026) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2026.113154 · Cited by 1 · see citing works
LOSS OF CONTROL OVER SUBSTANCE USE
Minnaard, A. M. (2020) · doi:10.33540/163 · Cited by 1 · see citing works
de Guglielmo, G., Carrette, L. L. G., Kallupi, M., Brennan, M., Boomhower, B., Maturin, L., Conlisk, D., Sedighim, S., Tieu, L., Fannon, M. J., et al. (2023) · eLife · doi:10.7554/elife.90422.1 · Cited by 1 · see citing works
Tunstall, B. J., & Kearns, D. N. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-803750-8.00041-5
Neurobehavioral Measurements of Natural and Opioid Reward Value
Smith, A. P. (2019) · UKnowledge (University of Kentucky) · doi:10.13023/etd.2019.316
- Authors
- Lenoir, M., Cantin, L., Vanhille, N., Serre, F., & Ahmed, S. H.
- Affiliations
- Université de Bordeaux (FR)
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Ahmed, Serge H
- Venue
- Neuropsychopharmacology
- Published
- 2013-01-15
- Volume
- 38
- Issue
- 7
- Pages
- 1209-1220
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC3656363
- OpenAlex
- W2020320083
- Cited by
- 114
- References
- 68
- Citations by year
- 2026: 5 · 2025: 2 · 2024: 3 · 2023: 5 · 2022: 11 · 2021: 14 · 2020: 19 · 2019: 9 · 2018: 9 · 2017: 12 · 2016: 7 · 2015: 4 · 2014: 8 · 2013: 6
- FWCI
- 4.09
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neuropsychopharmacology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Agence Nationale de la Recherche
- Fondation pour la Recherche Médicale
- Centre National de la Recherche Scientifique
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Opioid Use Disorder Treatment
- Health Sciences › Medicine › Epidemiology › Substance Abuse Treatment and Outcomes
- Keywords
- heroin, cocaine, addiction liability, drug preference, self-administration, heroin withdrawal, relapse
- MeSH terms
- Animals, Choice Behavior, Cocaine, Conditioning, Operant, Heroin, Dose-Response Relationship, Drug, Male, Narcotics, Reward, Saccharin, Self Administration, Behavior, Addictive, Dopamine Uptake Inhibitors, Rats
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