Destruction of dopamine in the nucleus accumbens selectively attenuates cocaine but not heroin self-administration in rats
Abstract
The hypothesis that separate neural systems mediate the reinforcing properties of opioid and psychomotor stimulant drugs was tested by examining the role of mesolimbic dopamine (DA) neurons in maintaining intravenous heroin and cocaine self-administration. After local destruction of the DA terminals in the nucleus accumbens (NAcc) with 6-hydroxydopamine (6-OHDA), rats trained to self-administer cocaine and heroin on alternate days were observed for changes in their drug-seeking behaviors. Postlesion responding for cocaine showed a time-dependent decrease or extinction, whereas heroin self-administration showed a time-dependent recovery. By the fifth trial postlesion, heroin self-administration had recovered to 76% of prelesion baseline levels, but cocaine self-administration had dropped to 30% of prelesion baseline rates. Thus, selective lesions of the DA terminals in the nucleus accumbens significantly attenuate cocaine but not heroin self-administration. These data support the hypothesis that independent neural substrates are responsible for the reinforcing actions of these two drugs.
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Lesion or inactivation of the mesolimbic DA system in the VTA or NAc decreases cocaine, amphetamine, heroin, and nicotine self-administration in rats.
“In addition, lesion or inactivation of the mesolimbic DA system in the VTA [137,138] or in the NAc [139-143] decreases cocaine, amphetamine, heroin, and nicotine self-administration in rats.”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [141]
Cites
The rat brain: A stereotaxic atlas of the forebrain and lower parts of the brain stem
König, J. F. R., & Klippel, R. (1986) · Medical Entomology and Zoology · Cited by 4,134 · see citing works
The Rat Brain. A Stereotaxic Atlas
König, B. F. R., Klippel, R., & Zeman, W. (1964) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-196410000-00012 · Cited by 1,003 · 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
Roberts, D. C. S., Koob, G. F., Klonoff, P., & Fibiger, H. C. (1980) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(80)90166-5 · Cited by 730 · see citing works
Self-citationOn the role of ascending catecholaminergic systems in intravenous self-administration of cocaine
Roberts, D. C. S., Corcoran, M. E., & Fibiger, H. C. (1977) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(77)90084-3 · Cited by 728 · see citing works
DETERMINATION OF CATECHOLAMINES IN RAT BRAIN PARTS BY REVERSE‐PHASE ION‐PAIR LIQUID CHROMATOGRAPHY
Felice, L. J., Felice, J. D., & Kissinger, P. T. (1978) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1978.tb06573.x · Cited by 582 · see citing works
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 · see citing works
Self-citationYokel, R. A., & Wise, R. A. (1975) · Science · doi:10.1126/science.1114313 · Cited by 545 · see citing works
Intracranial self-administration of morphine into the ventral tegmental area in rats
Bozarth, M. A., & Wise, R. A. (1981) · Life Sciences · doi:10.1016/0024-3205(81)90148-x · Cited by 503 · see citing works
Self Administration of and Behavioral Dependence on Drugs
Schuster, C. R., & Thompson, T. I. (1969) · Annual Review of Pharmacology · doi:10.1146/annurev.pa.09.040169.002411 · Cited by 492 · see citing works
de Wit, H., & Wise, R. A. (1977) · Canadian Journal of Psychology / Revue canadienne de psychologie · doi:10.1037/h0081662 · Cited by 491 · see citing works
Lyness, W. H., Friedle, N. M., & Moore, K. E. (1979) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(79)90040-6 · Cited by 457 · see citing works
Attenuation of intravenous amphetamine reinforcement by central dopamine blockade in rats
Yokel, R. A., & Wise, R. A. (1976) · Psychopharmacology · doi:10.1007/bf00496868 · Cited by 369 · see citing works
Handbook of psychopharmacology, vol. 16
Woolf, C. J. (1985) · Pain · doi:10.1016/0304-3959(85)90237-4 · Cited by 366 · see citing works
Reinforcing effects of morphine microinjection into the ventral tegmental area
Phillips, A. G., & LePiane, F. G. (1980) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(80)90460-8 · Cited by 339 · see citing works
Heroin reward is dependent on a dopaminergic substrate
Bozarth, M. A., & Wise, R. A. (1981) · Life Sciences · doi:10.1016/0024-3205(81)90519-1 · Cited by 334 · see citing works
Attenuation of heroin reward in rats by disruption of the mesolimbic dopamine system
Spyraki, C., Fibiger, H. C., & Phillips, A. G. (1983) · Psychopharmacology · doi:10.1007/bf00427827 · Cited by 308 · see citing works
Self-administration of d-amphetamine by rats
Pickens, R. W., & Harris, W. C. (1968) · Psychopharmacology · doi:10.1007/bf00401545 · Cited by 296 · see citing works
Drug reinstatement of heroin-reinforced responding in the rat
de Wit, H., & Stewart, J. (1983) · Psychopharmacology · doi:10.1007/bf00433012 · Cited by 270 · see citing works
Spyraki, C., Fibiger, H. C., & Phillips, A. G. (1982) · Brain Research · doi:10.1016/0006-8993(82)90686-2 · Cited by 242 · see citing works
Fibiger, H. C., Carter, D. A., & Phillips, A. G. (1976) · Psychopharmacology · doi:10.1007/bf00428696 · Cited by 225 · see citing works
The dopamine synapse and the notion of ‘pleasure centers’ in the brain
Wise, R. A. (1980) · Trends in Neurosciences · doi:10.1016/0166-2236(80)90035-1 · Cited by 178 · see citing works
Long-term Intravenous Infusion
Weeks, J. R. (1972) · Elsevier eBooks · doi:10.1016/b978-0-12-512302-0.50010-9 · Cited by 172 · see citing works
SELF-ADMINISTRATION OF OPTICAL ISOMERS OF AMPHETAMINE AND METHYLAMPHETAMINE BY RATS
Yokel, R. A., & Pickens, R. W. (1973) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)29645-8 · Cited by 161 · see citing works
Reinforcement Properties of Morphine, Cocaine, and SPA as a Function of Unit Dose
Woods, J. H., & Schuster, C. R. (1968) · International Journal of the Addictions · doi:10.3109/10826086809042898 · Cited by 151 · see citing works
Joyce, E. M., Koob, G. F., Strecker, R. E., Iversen, S. D., & Bloom, F. E. (1981) · Brain Research · doi:10.1016/0006-8993(81)90784-8 · Cited by 139 · see citing works
Self-citationBlockade of intravenous amphetamine euphoria in man
Jônsson, L.-E., Änggård, E., & Gunne, L. (1971) · Clinical Pharmacology & Therapeutics · doi:10.1002/cpt1971126889 · Cited by 139 · see citing works
Robbins, T. W., Roberts, D. C. S., & Koob, G. F. (1983) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)33532-9 · Cited by 125 · see citing works
Self-citationNALORPHINE-INDUCED CHANGES IN MORPHINE SELF-ADMINISTRATION IN RHESUS MONKEYS
Goldberg, S. R., Woods, J. H., & Schuster, C. R. (1971) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)28806-1 · Cited by 104 · see citing works
Effect of haloperidol on (+)-amphetamine self-administration
Davis, W. M., & Smith, S. G. (1975) · Journal of Pharmacy and Pharmacology · doi:10.1111/j.2042-7158.1975.tb09502.x · Cited by 95 · see citing works
Drug Self-Administration: An Analysis of the Reinforcing Effects of Drugs
Pickens, R. W., Meisch, R. A., & Thompson, T. I. (1978) · Springer eBooks · doi:10.1007/978-1-4684-3186-5_1 · Cited by 71 · see citing works
Depression of Morphine-seeking Behaviour by Dopamine Inhibition
Schwartz, A. S., & Marchok, P. L. (1974) · Nature · doi:10.1038/248257a0 · Cited by 68 · see citing works
Chemical Interactions in Methamphetamine Reinforcement
Pickens, R. W., Meisch, R. A., & Dougherty, J. A. (1968) · Psychological Reports · doi:10.2466/pr0.1968.23.3f.1267 · Cited by 65 · see citing works
Changes in morphine self-administration in rats induced by prostaglandin E1 and naloxone
Weeks, J. R., & Collins, R. J. (1976) · Prostaglandins · doi:10.1016/s0090-6980(76)80003-2 · Cited by 53 · see citing works
Stimulant self-administration by animals: some comparisons with opiate self-administration.
Thompson, T. N., & Pickens, R. W. (1970) · PubMed · Cited by 48 · see citing works
A dose-response comparison between methadone and morphine self-administration
Werner, T. E., Smith, S. G., & Davis, W. M. (1976) · Psychopharmacology · doi:10.1007/bf00735825 · Cited by 28 · see citing works
Flagged first, then by citations
1 of the 37 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Di Chiara, G., & Imperato, A. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.14.5274 · Cited by 4,733 · see citing works
Bardo, M. T., & Hammer, R. P. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90226-e · Cited by 3,229 · see citing works
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
Self-citationA psychomotor stimulant theory of addiction.
Wise, R. A., & Bozarth, M. A. (1987) · Psychological Review · doi:10.1037/0033-295x.94.4.469 · Cited by 2,747 · see citing works
NEURAL MECHANISMS OF ADDICTION: The Role of Reward-Related Learning and Memory
Hyman, S. E., Malenka, R. C., & Nestler, E. J. (2006) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.113009 · Cited by 2,647 · 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
Self-citationCellular and molecular mechanisms of drug dependence
Koob, G. F., & Bloom, F. E. (1988) · Science · doi:10.1126/science.2903550 · Cited by 2,070 · see citing works
Self-citationIkemoto, S. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.004 · Cited by 1,477 · see citing works
Addiction and the brain antireward system
Koob, G. F., & Le Moal, M. (2008) · Annual Review of Psychology · doi:10.1146/annurev.psych.59.103006.093548 · Cited by 1,457 · see citing works
Self-citationIkemoto, S., & Panksepp, J. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00023-5 · Cited by 1,450 · see citing works
Nucleus accumbens D2/3 receptors predict trait impulsivity and cocaine reinforcement
Dalley, J. W., Fryer, T. D., Brichard, L., Robinson, E. S. J., Theobald, D. E. H., Lääne, K., Peña, Y., Murphy, E. R., Shah, Y., Probst, K., et al. (2007) · Science · doi:10.1126/science.1137073 · Cited by 1,188 · see citing works
Reward Processing by the Opioid System in the Brain
Le Merrer, J., Becker, J. A. J., Befort, K., & Kieffer, B. L. (2009) · Physiological Reviews · doi:10.1152/physrev.00005.2009 · Cited by 1,013 · see citing works
Nucleus accumbens shell and core dopamine: differential role in behavior and addiction
Di Chiara, G. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00286-3 · Cited by 996 · see citing works
The dopamine hypothesis of the reinforcing properties of cocaine
Kuhar, M. J., Ritz, M. C., & Boja, J. W. (1991) · Trends in Neurosciences · doi:10.1016/0166-2236(91)90141-g · Cited by 989 · see citing works
The dopamine hypothesis of reward: past and current status
Spanagel, R., & Weiss, F. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01447-2 · Cited by 967 · see citing works
depue, R. A., & morrone-strupinsky, J. V. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000063 · Cited by 958 · see citing works
Pierce, R. C., & Kumaresan, V. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.016 · Cited by 913 · see citing works
Reward, Motivation, and Reinforcement Learning
Dayan, P., & Balleine, B. W. (2002) · Neuron · doi:10.1016/s0896-6273(02)00963-7 · Cited by 855 · see citing works
The mesolimbic dopaminergic system is implicated in the reinforcing effects of nicotine
Corrigall, W. A., Franklin, K. B. J., Coen, K. M., & Clarke, P. B. S. (1992) · Psychopharmacology · doi:10.1007/bf02245149 · Cited by 829 · see citing works
Pennartz, C. M. A., Groenewegen, H. J., & LOPESDASILVA, F. (1994) · Progress in Neurobiology · doi:10.1016/0301-0082(94)90025-6 · Cited by 802 · see citing works
Neurobiological similarities in depression and drug dependence: a self-medication hypothesis
Markou, A. (1998) · Neuropsychopharmacology · doi:10.1016/s0893-133x(97)00113-9 · Cited by 767 · see citing works
Endogenous opioid systems and alcohol addiction
Herz, A. (1997) · Psychopharmacology · doi:10.1007/s002130050169 · Cited by 749 · see citing works
Role of dopamine in the behavioural actions of nicotine related to addiction
Chiara, G. D. (2000) · European Journal of Pharmacology · doi:10.1016/s0014-2999(00)00122-9 · Cited by 680 · see citing works
Swerdlow, N. R., & Koob, G. F. (1987) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00047488 · Cited by 674 · see citing works
Self-citationPsychobiology of novelty seeking and drug seeking behavior
Bardo, M. T., Donohew, R. L., & Harrington, N. G. (1996) · Behavioural Brain Research · doi:10.1016/0166-4328(95)00203-0 · Cited by 667 · see citing works
Relationship between subjective effects of cocaine and dopamine transporter occupancy
Volkow, N. D., Wang, G., Fischman, M. W., Foltin, R. W., Fowler, J. S., Abumrad, N. N., Vitkun, S. A., Logan, J., Gatley, S. J., Pappas, N. R., et al. (1997) · Nature · doi:10.1038/386827a0 · Cited by 646 · see citing works
The role of dopamine in drug abuse viewed from the perspective of its role in motivation
Chiara, G. D. (1995) · Drug and Alcohol Dependence · doi:10.1016/0376-8716(95)01118-i · Cited by 624 · see citing works
Neural Mechanisms of Drug Reinforcementa
Koob, G. F. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb25966.x · Cited by 607 · see citing works
Self-citationMcBride, W. J., Murphy, J. M., & Ikemoto, S. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00022-4 · Cited by 574 · see citing works
The neurobiology of drug addiction
Koob, G. F., & Nestler, E. J. (1997) · Journal of Neuropsychiatry · doi:10.1176/jnp.9.3.482 · Cited by 572 · see citing works
Self-citationMolecular Mechanisms of Drug Reinforcement and Addiction
Self, D. W., & Nestler, E. J. (1995) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.18.030195.002335 · Cited by 565 · see citing works
The neurobiology of social play behavior in rats
Vanderschuren, L. J. M. J., Niesink, R. J. M., & Van Pee, J. M. (1997) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(96)00020-6 · Cited by 559 · see citing works
Markou, A., Weiss, F., Gold, L. H., Caine, S. B., Schulteis, G., & Koob, G. F. (1993) · Psychopharmacology · doi:10.1007/bf02244907 · Cited by 551 · see citing works
Self-citationChiara, G. D., & North, R. A. (1992) · Trends in Pharmacological Sciences · doi:10.1016/0165-6147(92)90062-b · Cited by 538 · see citing works
Dopamine Signaling in reward-related behaviors
Baik, J. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00152 · Cited by 534 · see citing works
Terwilliger, R. Z., Beitner‐Johnson, D., Sevarino, K. A., Crain, S. M., & Nestler, E. J. (1991) · Brain Research · doi:10.1016/0006-8993(91)91111-d · Cited by 534 · see citing works
Cocaine self-administration in dopamine-transporter knockout mice
Rocha, B. A. G., Fumagalli, F., Gainetdinov, R. R., Jones, S. R., Ator, R., Giros, B., Miller, G. W., & Caron, M. G. (1998) · Nature Neuroscience · doi:10.1038/381 · Cited by 519 · see citing works
Differential control over cocaine-seeking behavior by nucleus accumbens core and shell
Ito, R., Robbins, T. W., & Everitt, B. J. (2004) · Nature Neuroscience · doi:10.1038/nn1217 · Cited by 501 · see citing works
Sora, I., Wichems, C. H., Takahashi, N., Li, X.-F., Zeng, Z., Revay, R. S., Lesch, K., Murphy, D. L., & Uhl, G. R. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.13.7699 · Cited by 501 · see citing works
The nucleus accumbens: a comprehensive review
Salgado, S., & Kaplitt, M. G. (2015) · Stereotactic and Functional Neurosurgery · doi:10.1159/000368279 · Cited by 489 · see citing works
Zahm, D. S. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00065-2 · Cited by 487 · see citing works
Ethanol increases the firing rate of dopamine neurons of the rat ventral tegmental area in vitro
Brodie, M. S., Shefner, S. A., & Dunwiddie, T. V. (1990) · Brain Research · doi:10.1016/0006-8993(90)91118-z · Cited by 485 · see citing works
The transition to compulsion in addiction
Lüscher, C., Robbins, T. W., & Everitt, B. J. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-0289-z · Cited by 475 · see citing works
Sora, I., Hall, F. S., Andrews, A. M., Itokawa, M., Li, X.-F., Wei, H.-B., Wichems, C. H., Lesch, K., Murphy, D. L., & Uhl, G. R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.091039298 · Cited by 474 · 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
Role of brain dopamine in food reward and reinforcement
Wise, R. A. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1854 · Cited by 436 · see citing works
Addictive drugs as reinforcers: multiple partial actions on memory systems
White, N. M. (1996) · Addiction · doi:10.1046/j.1360-0443.1996.9179212.x · Cited by 436 · see citing works
The role of reward pathways in the development of drug dependence
Wise, R. A. (1987) · Pharmacology & Therapeutics · doi:10.1016/0163-7258(87)90108-2 · Cited by 432 · see citing works
Absence of opiate rewarding effects in mice lacking dopamine D2 receptors
Maldonado, R. J., Saiardi, A., Valverde, O., Samad, T. A., Roques, B. P., & Borrelli, E. (1997) · Nature · doi:10.1038/41567 · Cited by 431 · see citing works
The neurocircuitry of addiction: an overview
Feltenstein, M. W., & See, R. E. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.51 · Cited by 421 · see citing works
Involvement of the dorsal striatum in cue-controlled cocaine seeking
Vanderschuren, L. J. M. J., Di Ciano, P., & Everitt, B. J. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.0925-05.2005 · Cited by 393 · see citing works
Electrophysiological Characterization of GABAergic Neurons in the Ventral Tegmental Area
Steffensen, S. C., Svingos, A. L., Pickel, V. M., & Henriksen, S. J. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-19-08003.1998 · Cited by 388 · see citing works
Pettit, H. O., & Justice, J. B. (1989) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(89)90291-8 · Cited by 375 · see citing works
Self-citationKreek, M. J., LaForge, K. S., & Butelman, E. R. (2002) · Nature Reviews Drug Discovery · doi:10.1038/nrd897 · Cited by 371 · 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
Neural substrates of opiate withdrawal
Koob, G. F., Maldonado, R. J., & Stinus, L. (1992) · Trends in Neurosciences · doi:10.1016/0166-2236(92)90171-4 · Cited by 356 · see citing works
Self-citationThere and Back Again: A Tale of Norepinephrine and Drug Addiction
Weinshenker, D., & Schroeder, J. P. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301263 · Cited by 347 · see citing works
The ventral pallidum: Subregion-specific functional anatomy and roles in motivated behaviors
Root, D. H., Meléndez, R. I., Záborszky, L., & Napier, T. C. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.03.005 · Cited by 343 · see citing works
Morphine reward in dopamine-deficient mice
Hnasko, T. S., Sotak, B. N., & Palmiter, R. D. (2005) · Nature · doi:10.1038/nature04172 · Cited by 338 · see citing works
Extinction-induced upregulation in AMPA receptors reduces cocaine-seeking behaviour
Sutton, M. A., Schmidt, E. F., Choi, K.-H., Schad, C. A., Whisler, K., Simmons, D. L., Karanian, D. A., Monteggia, L. M., Neve, R. L., & Self, D. W. (2003) · Nature · doi:10.1038/nature01249 · Cited by 322 · see citing works
Impérato, A., Puglisi‐Allegra, S., Casolini, P., & Angelucci, L. (1991) · Brain Research · doi:10.1016/0006-8993(91)90384-8 · Cited by 322 · see citing works
Taylor, J. R., & Robbins, T. W. (1986) · Psychopharmacology · doi:10.1007/bf00179197 · Cited by 317 · see citing works
Molecular alterations in the neostriatum of human cocaine addicts
Hurd, Y. L., & Herkenham, M. A. (1993) · Synapse · doi:10.1002/syn.890130408 · Cited by 316 · see citing works
Neurobiology of Addiction: Toward the Development of New Therapies
Koob, G. F. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06682.x · Cited by 314 · see citing works
Self-citationOpioids, 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 300 · see citing works
Dichter, G. S., Damiano, C. A., & Allen, J. A. (2012) · Journal of Neurodevelopmental Disorders · doi:10.1186/1866-1955-4-19 · Cited by 299 · see citing works
Addictive drugs as reinforcers: multiple partial actions on memory systems
WHITE, N. M. (1996) · Addiction · doi:10.1111/j.1360-0443.1996.tb03586.x · Cited by 439 · see citing works
Sufficiency of Mesolimbic Dopamine Neuron Stimulation for the Progression to Addiction
Pascoli, V., Terrier, J. E., Hiver, A., & Lüscher, C. (2015) · Neuron · doi:10.1016/j.neuron.2015.10.017 · Cited by 291 · see citing works
Brown, E., Robertson, G. S., & Fibiger, H. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-10-04112.1992 · Cited by 288 · see citing works
Opiate reward: Sites and substrates
Wise, R. A. (1989) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(89)80021-1 · Cited by 286 · see citing works
Caine, S. B., Heinrichs, S. C., Coffin, V. L., & Koob, G. F. (1995) · Brain Research · doi:10.1016/0006-8993(95)00598-k · Cited by 286 · see citing works
Self-citationDrug addiction: Pathways to the disease and pathophysiological perspectives
Moal, M. L., & Koob, G. F. (2006) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2006.10.006 · Cited by 284 · see citing works
Self-citationHemby, S. E., Co, C., Koves, T. R., Smith, J. E., & Dworkin, S. I. (1997) · Psychopharmacology · doi:10.1007/s002130050365 · Cited by 278 · see citing works
Localization of drug reward mechanisms by intracranial injections
Wise, R. A., & Hoffman, D. C. (1992) · Synapse · doi:10.1002/syn.890100307 · Cited by 276 · see citing works
Microinjection of cocaine into the nucleus accumbens elicits locomotor activation in the rat
Delfs, J. M., Schreiber, L., & Kelley, A. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-01-00303.1990 · Cited by 274 · see citing works
Grace, A. A. (1995) · Drug and Alcohol Dependence · doi:10.1016/0376-8716(94)01066-t · Cited by 272 · see citing works
The biological, social and clinical bases of drug addiction: commentary and debate
Altman, J. S., Everitt, B. J., Robbins, T. W., Glautier, S., Markou, A., Nutt, D., Oretti, R. G., & Phillips, G. D. (1996) · Psychopharmacology · doi:10.1007/bf02246016 · Cited by 270 · see citing works
Opponent process theory of motivation: Neurobiological evidence from studies of opiate dependence
Koob, G. F., Stinus, L., Moal, M. L., & Bloom, F. E. (1989) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(89)80022-3 · Cited by 268 · see citing works
Self-citationSwerdlow, N. R., Vaccarino, F. J., Amalric, M., & Koob, G. F. (1986) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(86)90261-3 · Cited by 259 · see citing works
Self-citationRole of Dopamine D1and D2Receptors in the Nucleus Accumbens in Mediating Reward
Ikemoto, S., Glazier, B. S., Murphy, J. M., & McBride, W. J. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-21-08580.1997 · Cited by 257 · see citing works
Neural substrates of conditioned-cued relapse to drug-seeking behavior
See, R. E. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00682-7 · Cited by 257 · see citing works
Fletcher, P. J. (2002) · Neuropsychopharmacology · doi:10.1016/s0893-133x(02)00342-1 · Cited by 251 · see citing works
Swerdlow, N. R., BRAFF, D. L., Masten, V. L., & Geyer, M. A. (1990) · Psychopharmacology · doi:10.1007/bf02244063 · Cited by 246 · see citing works
Dynamics of Neuronal Circuits in Addiction: Reward, Antireward, and Emotional Memory
Koob, G. F. (2009) · Pharmacopsychiatry · doi:10.1055/s-0029-1216356 · Cited by 244 · see citing works
Self-citationCervo, L., & SAMANIN, R. (1995) · Brain Research · doi:10.1016/0006-8993(94)01420-m · Cited by 239 · see citing works
Caine, S. B., Negus, S. S., Mello, N. K., Patel, S., Bristow, L., Kulagowski, J., Vallone, D., Saiardi, A., & Borrelli, E. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-07-02977.2002 · Cited by 234 · see citing works
Brain substrates for increased drug seeking during protracted withdrawal
Aston‐Jones, G., & Harris, G. C. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.06.020 · Cited by 233 · see citing works
Jones, G. H., Marsden, C. A., & Robbins, T. W. (1990) · Psychopharmacology · doi:10.1007/bf02244105 · Cited by 232 · see citing works
Effect of dose on cocaine self-administration behavior and dopamine levels in the nucleus accumbens
Pettit, H. O., & Justice, J. B. (1991) · Brain Research · doi:10.1016/0006-8993(91)90690-w · Cited by 225 · see citing works
Self-citationLoh, E. A., & Roberts, D. C. S. (1990) · Psychopharmacology · doi:10.1007/bf02244137 · Cited by 224 · see citing works
Opiate addiction and cocaine addiction: underlying molecular neurobiology and genetics
Kreek, M. J., Levran, O., Reed, B., Schlussman, S. D., Zhou, Y., & Butelman, E. R. (2012) · Journal of Clinical Investigation · doi:10.1172/jci60390 · Cited by 220 · see citing works
The ventral pallidum plays a role in mediating cocaine and heroin self-administration in the rat
Hubner, C. B., & Koob, G. F. (1990) · Brain Research · doi:10.1016/0006-8993(90)91112-t · Cited by 218 · see citing works
Self-citationIkemoto, S., & Panksepp, J. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.2.331 · Cited by 216 · see citing works
Spangler, R., Unterwald, E. M., & Kreek, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90133-a · Cited by 210 · see citing works
Mesocorticolimbic Dopamine Systems and Reward
Fibiger, H. C., & Phillips, A. G. (1988) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1988.tb42107.x · Cited by 206 · see citing works
Rassnick, S., Stinus, L., & Koob, G. F. (1993) · Brain Research · doi:10.1016/0006-8993(93)90004-7 · Cited by 205 · see citing works
Self-citationAnderson, S. M., & Pierce, R. C. (2005) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2004.12.004 · Cited by 200 · see citing works
Cocaine self-administration differentially alters mRNA expression of striatal peptides
Hurd, Y. L., Brown, E. E., Finlay, J. M., Fibiger, H. C., & Gerfen, C. R. (1992) · Molecular Brain Research · doi:10.1016/0169-328x(92)90058-j · Cited by 199 · see citing works
Hurd, Y. L., Weiss, F., Koob, G. F., And, N.-E., & Ungerstedt, U. (1989) · Brain Research · doi:10.1016/0006-8993(89)90422-8 · Cited by 198 · see citing works
Self-citationMcCance‐Katz, E. F., Price, L. H., McDougle, C. J., Kosten, T. R., Black, J. E., & Jatlow, P. I. (1993) · Psychopharmacology · doi:10.1007/bf02257405 · Cited by 195 · see citing works
- Authors
- Pettit, H. O., Ettenberg, A., Bloom, F. E., & Koob, G. F.
- Affiliations
- Texas Christian University (US)
- University of California, Santa Barbara (US)
- Scripps Clinic (US)
- ORCID
- Koob, George F.
- Venue
- Psychopharmacology
- Published
- 1984-10
- Volume
- 84
- Issue
- 2
- Pages
- 167-173
- ISSN
- 0033-3158 (ISSN-L)
- 1432-2072
- OpenAlex
- W1964909230
- Cited by
- 651
- References
- 37
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 7 · 2023: 9 · 2022: 15 · 2021: 6 · 2020: 13 · 2019: 16 · 2018: 10 · 2017: 9 · 2016: 11 · 2015: 13 · 2014: 15 · 2013: 15 · 2012: 17
- FWCI
- 5.74
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Psychopharmacology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- nucleus accumbens, dopamine, cocaine self-administration, heroin self-administration, 6-hydroxydopamine lesion, drug reinforcement, opioid reinforcement, drug-seeking behavior
- MeSH terms
- Animals, Cocaine, Heroin, Dopamine, Hydroxydopamines, Male, Norepinephrine, Nucleus Accumbens, Rats, Inbred Strains, Self Administration, Septal Nuclei, 3,4-Dihydroxyphenylacetic Acid, Oxidopamine, Rats
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