The DOI matches its Crossref record; 269 of the 269 references it cites were found in a registry or an index.
Addictive drugs as reinforcers: multiple partial actions on memory systems
Abstract
This review applies some new experimental findings and theoretical ideas about how reinforcers act on the neural mechanisms of learning and memory to the problem of how addictive drugs affect behaviour. A basic assumption of this analysis is that all changes in behaviour, including those involved in drug addiction and the initiation of drug self-administration, require the storage of new information in the nervous system. Animal studies suggest that such information is processed in several (this review deals with three) more or less independent learning and memory systems in the mammalian brain. Reinforcers can interact with these systems in three ways: they activate neural substrates of observable approach or escape responses, they produce unobservable internal states that can be perceived as rewarding or aversive, and they modulate or enhance the information stored in each of the memory systems. It is suggested that each addictive drug maintains its own self-administration by mimicking some subset of these actions. Evidence supporting the notion of multiple memory systems and data on the actions of several drugs (amphetamine, cocaine, nicotine, alcohol and morphine) on these systems are briefly reviewed. The utility of the concept of "reward" for understanding the effects of drugs on behaviour is discussed. Evidence demonstrating actions of drugs on multiple neural substrates of reinforcement suggests that no single factor is likely to explain either addictive behaviour in general or self-administration in particular. Some of the findings on the development and maintenance of self-administration by animals of the five exemplar drugs are discussed in the context of these ideas.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Other frameworks that emphasize multiple parallel memory systems in the brain (e.g., Gruber & McDonald, 2012; McDonald & White, 1993; White, 1996) also allow behavioral flexibility.”
From Context, attention, and the switch between habit and goal-direction in behavior (2021) · cites this paper as White, 1996
Citations
Cites
Items 201–269 of 269
Facilitation of learning by reward of post-trial memory processes
Huston, J. P., Mondadori, C., & Waser, P. G. (1974) · Cellular and Molecular Life Sciences · doi:10.1007/bf01938996 · Cited by 51
Intraventricular self-administration of morphine in naive laboratory rats
Amit, Z., Brown, Z. W., & Sklar, L. S. (1976) · Psychopharmacology · doi:10.1007/bf00496864 · Cited by 51
Stewart, R. B., & Grupp, L. A. (1989) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(89)90175-5 · Cited by 50
Tomaz, C. A. B., Aguiar, M. S., & Nogueira, P. J. C. (1990) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80067-3 · Cited by 49
Rats learning to work for alcohol
Sinclair, J. D. (1974) · Nature · doi:10.1038/249590a0 · Cited by 49
Samson, H. H., Haraguchi, M., Tolliver, G. A., & Sadeghi, K. G. (1989) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(89)90395-x · Cited by 48
Hirsh, R., Leber, B. F., & Gillman, K. (1978) · Behavioral Biology · doi:10.1016/s0091-6773(78)92583-x · Cited by 48
Learning deficits induced by cholinergic blockade of the caudate nucleus as a function of experience
Prado-Alcalá, R. A., & Cobos-Zapiaín, G. (1977) · Brain Research · doi:10.1016/0006-8993(77)90797-1 · Cited by 45
Operationalizing and Measuring the Organizing Influence of Drugs on Behavior
White, N. M., Messier, C., & Carr, G. D. (1987) · Springer eBooks · doi:10.1007/978-1-4612-4812-5_28 · Cited by 44
Self-citationCharacteristics of Stimulant Drug Reinforcement
Pickens, R. W., & Thompson, T. I. (1971) · Springer eBooks · doi:10.1007/978-1-4757-0788-5_11 · Cited by 44
Comparative functions of the central noradrenergic, dopaminergic and cholinergic systems
Robbins, T. W. (1987) · Neuropharmacology · doi:10.1016/0028-3908(87)90067-0 · Cited by 42
Messing, R. B., Jensen, R. A., Vásquez, B. J., et al. (1981) · Elsevier eBooks · doi:10.1016/b978-0-12-474980-1.50026-x · Cited by 42
Castellano, C., Introini-Collison, I. B., Pavone, F., & McGaugh, J. L. (1989) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(89)90197-4 · Cited by 37
Nicotine conditions place preferences after intracerebral administration in rats
Iwamoto, E. T. (1990) · Psychopharmacology · doi:10.1007/bf02244415 · Cited by 35
Deminière, J.-M., Taghzouti, K., Tassin, J., Moal, M. L., & Simon, H. (1988) · Psychopharmacology · doi:10.1007/bf00176851 · Cited by 34
Jensen, R. A., Gilbert, D. G., Meliska, C. J., Landrum, T. A., & Szary, A. (1990) · Behavioral and Neural Biology · doi:10.1016/0163-1047(90)90310-3 · Cited by 34
Wood, P. L., & Rao, T. S. (1991) · Neuropharmacology · doi:10.1016/0028-3908(91)90066-k · Cited by 34
Effect of Ro 15-4513 on ethanol-induced conditioned place preference
Risinger, F. O., Malott, D. H., Riley, A. L., et al. (1992) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(92)90644-u · Cited by 33
Amphetamine conditioned cue preference and the neurobiology of drug-seeking
White, N. M., & Hiroi, N. (1993) · Seminars in Neuroscience · doi:10.1016/s1044-5765(05)80040-5 · Cited by 32
Self-citationLinseman, M. A. (1982) · Neuropharmacology · doi:10.1016/0028-3908(82)90101-0 · Cited by 32
Amphetamine-induced taste aversion demonstrated with operant behaviour
Stolerman, I. P., & D'Mello, G. D. (1978) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(78)90324-6 · Cited by 32
Effects of morphine on one-trial appetitive learning
White, N. M., Major, R., & Siegel, J. (1978) · Life Sciences · doi:10.1016/0024-3205(78)90564-7 · Cited by 32
Self-citationThe Hippocampus and the Expression of Knowledge
Hirsh, R., & Krajden, J. (1982) · Springer eBooks · doi:10.1007/978-1-4684-7890-7_7 · Cited by 31
Voluntary ethanol consumption in rats
Boyle, A. E., Smith, B. R., Spivak, K. J., et al. (1994) · Behavioural Pharmacology · doi:10.1097/00008877-199408000-00011 · Cited by 30
Garg, M., & HOLLAND, H. C. (1968) · International Journal of Neuropharmacology · doi:10.1016/0028-3908(68)90055-5 · Cited by 30
Nicotine-induced conditioned taste aversions are enhanced in rats with lesions of the area postrema
Ossenkopp, K., & Giugno, L. (1990) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(90)90266-k · Cited by 30
Pharmacologic determinants of tobacco self-administration by humans
Henningfield, J. E., & Goldberg, S. R. (1988) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(88)90449-2 · Cited by 29
Schedule-induction of nicotine self-administration
Slifer, B. L. (1983) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(83)90407-0 · Cited by 28
Faiman, C. P., de Erausquin, G. A., & Baratti, C. M. (1991) · Behavioral and Neural Biology · doi:10.1016/0163-1047(91)90592-e · Cited by 28
Avoidance learning enhanced by post-trial morphine injection
Staubli, U. V., & Huston, J. P. (1980) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(80)91860-9 · Cited by 28
Alcohol ingestion without oropharyngeal sensations
Amit, Z., & Stern, M. H. (1969) · Psychonomic Science · doi:10.3758/bf03336259 · Cited by 28
Posttrial treatment with ethanol enhances recall of prose narratives
Lamberty, G. J., Beckwith, B. E., Petros, T. V., & Ross, A. R. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90206-j · Cited by 28
Genetic models in the study of alcoholism and substance abuse mechanisms
George, F. R. (1993) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/0278-5846(93)90069-5 · Cited by 27
Improvement of learned behavior through cholinergic stimulation of the caudate nucleus
Prado-Alcalá, R. A., & Cobos-Zapiaín, G. (1979) · Neuroscience Letters · doi:10.1016/0304-3940(79)96157-3 · Cited by 27
Behavioral control by stimuli associated with acquisition of morphine self-administration
Smith, S. G., & Davis, W. M. (1973) · Behavioral Biology · doi:10.1016/s0091-6773(73)80139-7 · Cited by 26
Grecksch, G., Ott, T., & Matthies, H. J. G. (1978) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(78)90307-6 · Cited by 25
Chlorisondamine blocks acquisition of the conditioned taste aversion produced by (−)-nicotine
Reavill, C. A., Stolerman, I. P., Kumar, R. C., & Garcha, H. S. (1986) · Neuropharmacology · doi:10.1016/0028-3908(86)90204-2 · Cited by 25
Urrutia, A., & Gruol, D. L. (1992) · Brain Research · doi:10.1016/0006-8993(92)90365-g · Cited by 25
Dafny, N., Brown, M., Burks, T. F., et al. (1979) · Neuropharmacology · doi:10.1016/0028-3908(79)90075-3 · Cited by 25
Cocaine enhances retention of avoidance conditioning in rats
Janak, P. H., Keppel, G., & Martinez, J. L. (1992) · Psychopharmacology · doi:10.1007/bf02245422 · Cited by 25
Facilitation of hot-plate response learning by pre- and posttraining naltrexone administration
Messing, R. B., Rijk, H., & Rigter, H. (1983) · Psychopharmacology · doi:10.1007/bf00439270 · Cited by 25
Intravenous self-administration of pentobarbital and ethanol in rats
DeNoble, V. J., Mele, P. C., & Porter, J. H. (1985) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(85)90068-1 · Cited by 24
Effect of intrahippocampal injection of atropine on different phases of a learning experiment
Singh, H. K., Ott, T., & Matthies, H. J. G. (1974) · Psychopharmacology · doi:10.1007/bf00421377 · Cited by 24
Freund, R. K., Jungschaffer, D. A., & Collins, A. C. (1990) · Brain Research · doi:10.1016/0006-8993(90)90160-d · Cited by 24
Maeda, H., Morimoto, H., & Yanagimoto, K. (1993) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y93-057 · Cited by 24
Rewarding and aversive effects of stimulant drugs in infant rats
Smith, C. A., & Holman, E. W. (1987) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(87)90107-9 · Cited by 23
Theories of Reinforcement, Drive, and Motivation
Milner, P. M. (1977) · Springer eBooks · doi:10.1007/978-1-4613-4214-4_6 · Cited by 22
Hippocampal mossy fibers, motivational states, and contextual retrieval
Hirsh, R., Holt, L., & Mosseri, A. (1978) · Experimental Neurology · doi:10.1016/0014-4886(78)90041-9 · Cited by 22
The Effects of Ethanol on Cerebral Regional Acetylcholine Concentration and Utilization
Parker, T. H., Roberts, R. K., Henderson, G. I., et al. (1978) · Experimental Biology and Medicine · doi:10.3181/00379727-159-40330 · Cited by 21
EtOH self-administration in anticipation of noise stress in C57BL/6J mice
Mollenauer, S. O., Bryson, R., Robison, M., Sardo, J., & Coleman, C. (1993) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(93)90313-i · Cited by 20
Amit, Z., & Smith, B. R. (1992) · Psychopharmacology · doi:10.1007/bf02245298 · Cited by 19
Effect of morphine on dopaminergic neurons in the rat basal forebrain and striatum
Moleman, P., & Bruitivels, J. (1979) · Journal of Neural Transmission · doi:10.1007/bf01250788 · Cited by 17
Changes in hippocampal cholinergic activity following learning in mice
Jaffard, R., Destrade, C., Soumireu-Mourat, B., et al. (1980) · Neuroscience Letters · doi:10.1016/0304-3940(80)90286-4 · Cited by 17
Stefurak, T. L., Martin, G. M., & van der Kooy, D. (1990) · Psychobiology · doi:10.3758/bf03333091 · Cited by 16
Attenuation of x-ray-induced taste aversions by olfactory-bulb or amygdaloid lesions
Elkins, R. L. (1980) · Physiology & Behavior · doi:10.1016/0031-9384(80)90245-0 · Cited by 15
Effect of posttraining exposure to an aversive stimulus on retention
White, N. M., & Legree, P. J. (1984) · Physiological Psychology · doi:10.3758/bf03332196 · Cited by 15
Self-citationFornix—Thalamus fibers, motivational states, and contextual retrieval
Hirsh, R., Davis, R. E., & Holt, L. (1979) · Experimental Neurology · doi:10.1016/0014-4886(79)90105-5 · Cited by 15
Castellano, C., Libri, V., & Ammassari‐Teule, M. (1988) · Behavioural Brain Research · doi:10.1016/0166-4328(88)90168-4 · Cited by 15
Pleasure and preference in a two-dimensional sensory space
Cabanac, M., & Ferber, C. (1987) · Appetite · doi:10.1016/s0195-6663(87)80023-5 · Cited by 14
Ableitner, A., & Herz, A. (1989) · Brain Research · doi:10.1016/0006-8993(89)91513-8 · Cited by 14
Tolman and Tryon: Early research on the inheritance of the ability to learn.
Innis, N. K. (1992) · American Psychologist · doi:10.1037//0003-066x.47.2.190 · Cited by 13
Effects of lesions of the caudate nucleus on morphine dependence in the rat
Linseman, M. A. (1976) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(76)90111-8 · Cited by 12
Clinical validators: Comparisons of demented and amnesic patients.
Butters, N., Martone, M. E., White, B. E., et al. (1986) · American Psychological Association eBooks · doi:10.1037/10057-029 · Cited by 12
Packard, M. G., Williams, C. L., & McGaugh, J. L. (1992) · Psychobiology · doi:10.3758/bf03332060 · Cited by 11
Rector, D. M., Poe, G. R., & Harper, R. M. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90234-7 · Cited by 11
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
Cocaine enhances one-way avoidance responding in mice
Weinberger, S. B., Riedel, C. A., Janak, P. H., et al. (1992) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(92)90238-b · Cited by 9
The Role of Norepinephrine in Long-Term Potentiation at Mossy-Fiber Synapses in the Hippocampus
Johnston, D., Hopkins, W. F., & Gray, R. (1989) · Elsevier eBooks · doi:10.1016/b978-0-12-148955-7.50019-9 · Cited by 7
R., S. S. Z.-M. A. L. (1993) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.16.1.547 · Cited by 5
Research works printed but not linked: 43
- 10.1146/annurev.neuro.9.1.357 · DOI · Paper page
- Amit Z., 1977, Archives Internationales de Pharmacodynamie et de Therapie, 230, 65
- 10.1037//0097-7403.18.3.236 · DOI
- Brown Z. W., 1977, Archives Internationales de Pharmacodynamie et de Therapie, 230, 76
- Cabanac M., 1968, Communications in Behavioral Biology, 1, 77
- Candland D. K., 1977, Emotion
- 10.1146/annurev.neuro.15.1.353 · DOI · Paper page
- Divac I., 1968, Acta Biologiae Experimentalis (Warsaw, 28, 107
- Drummond D. C., 1991, Addiction Behaviour, 240
- Evangelista A. M., 1970, Psychopharmacology, 3, 91
- Falkowski W., 1991, Addiction Behaviour, 244
- Garcia J., 1966, Psychonomic Science, 7, 439
- Gold P. E., 1975, Short Term Memory
- Hull C. L., 1943, Principles of Behavior
- 10.1037//0735-7044.103.2.345 · DOI
- Izard C. E., 1972, Patterns of Emotions
- Jaffard R., 1982, Genetics of the Brain, 299
- Jon R. J., 1981, Substances Alcohol Actions/Misuses, 2, 15
- Lamb R. J., 1991, Journal of Pharmacology and Experimental Therapeutics, 259, 1165
- Littleton J., 1991, Addiction Behaviours, 11
- 10.1037//0735-7044.107.1.3 · DOI · Paper page
- McGaugh J. L., 1972, Memory Consolidation
- Mishkin M., 1984, Neuropsychology of Memory, 287
- Mishkin M., 1984, Neurobiology of Human Memory and Learning, 65
- O'Brien C. P., 1991, Addiction Behaviour, 230
- Olton D. S., 1982, Spatial Abilities: Develop Physiological Foundations, 335
- 10.1037//0097-7403.2.2.97 · DOI
- Packard M. G., 1993, Society for Neuroscience Abstracts, 19, 1226
- Pavlov I. P., 1927, Conditioned Reflexes
- Petri H. L., 1993, American Scientist, 82, 30
- Phillips A. G., 1982, The Neural Basis of Feeding and Reward, 455
- Pickens R., 1968, Journal of Pharmacology and Experimental Therapeutics, 161, 122
- Silverstone P. H., 1993, Neuro Report, 4, 1043
- Skinner B. F., 1938, The Behavior of Organisms
- 10.1037//0033-295X.91.2.251 · DOI
- Thorndike E. L., 1911, Animal Intelligence
- Toates F. M., 1986, Motivational Systems
- Tolman E. C., 1949, Psychological Review, 56, 144, 10.1037/h0055304 · DOI
- Viaud M. D., 1989, Society for Neuroscience Abstracts, 15, 734
- Wang J., 1990, Society for Neuroscience Abstracts, 16, 617
- Weeks J. R., 1968, The Addictive States, 288
- West R., 1991, Addiction Behaviour, 20
- 10.1037//0021-843X.97.2.118 · DOI
Cited by
Sorted by citations
Koob, G. F., & Volkow, N. D. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.110 · Cited by 5,340
What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?
Berridge, K. C., & Robinson, T. E. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00019-8 · Cited by 4,127
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
Robinson, T. E., & Berridge, K. C. (2003) · Annual Review of Psychology · doi:10.1146/annurev.psych.54.101601.145237 · Cited by 1,509
Ikemoto, S., & Panksepp, J. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00023-5 · Cited by 1,450
Metadata
- Authors
- WHITE, N. M.
- Affiliations
- McGill University (CA)
- Corresponding author
- WHITE, NORMAN M.
- ORCID
- WHITE, NORMAN M.
- Venue
- Addiction
- Publisher
- Wiley
- Published
- 1996-07
- Volume
- 91
- Issue
- 7
- Pages
- 921-950
- ISSN
- 0965-2140 (ISSN-L)
- 1360-0443
- OpenAlex
- W2135546946
- Cited by
- 439
- References
- 269
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 7 · 2023: 9 · 2022: 8 · 2021: 17 · 2020: 18 · 2019: 6 · 2018: 9 · 2017: 21 · 2016: 16 · 2015: 19 · 2014: 19 · 2013: 19 · 2012: 18
- FWCI
- 2.83
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Addiction (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- drugs of abuse, reinforcement, memory systems, self-administration, reward, learning and memory, amphetamine, cocaine, nicotine, alcohol, morphine, aversive stimuli
- MeSH terms
- Ethanol, Amphetamines, Animals, Behavior, Animal, Brain, Cocaine, Hippocampus, Learning, Memory, Morphine, Nicotine, Reinforcement, Psychology, Self Administration
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review