Addictive drugs as reinforcers: multiple partial actions on memory systems

WHITE, NORMAN M.

doi:10.1111/j.1360-0443.1996.tb03586.x

Cited by 439Neurotransmitter Receptor Influence on BehaviorMemory and Neural MechanismsNeural and Behavioral Psychology Studies

Addictive drugs as reinforcers: multiple partial actions on memory systems

WHITE, NORMAN M.·1996·Addiction

DOI 10.1111/j.1360-0443.1996.tb03586.x

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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.

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Other frameworks that emphasize multiple parallel memory systems in the brain allow behavioral flexibility.
“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

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Cocaine self-administration is increased by both D1 and D2 dopamine antagonists
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Flavor Aversion Studies
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Self‐Stimulation and Drug Reward Mechanisms
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Voluntary Ethanol Consumption in Rats: An Examination of Blood/Brain Ethanol Levels and Behavior
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Learning about rules but not about reward is impaired following lesions of the cholinergic projection to the hippocampus
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Prefrontal cortex lesions differentially disrupt cocaine-reinforced conditioned place preference but not conditioned taste aversion.
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A functional hypothesis concerning the striatal matrix and patches: Mediation of SR memory and reward
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Lesions of the caudate nucleus selectively impair “reference memory” acquisition in the radial maze
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Understanding brain mechanisms in nicotine reinforcement
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Blockade of hippocampal nicotinic receptors impairs working memory but not reference memory in rats
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Neurobiology of Conditioning to Drugs of Abuse
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Localized intracaudate dopamine D2 receptor activation during the post-training period improves memory for visual or olfactory conditioned emotional responses in rats
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Morphine-induced place preference in the CXBK mouse: characteristics of μ opioid receptor subtypes
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Opiates as Reinforcing Stimuli
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Influence of dopaminergic and serotonergic neurons on intravenous ethanol self-administration in the rat
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Temporal properties of the rewarding and aversive effects of amphetamine in rats
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Reinforcing effects of nicotine in humans and experimental animals responding under intermittent schedules of IV drug injection
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Hypothalamic substrate for the positive reinforcing properties of morphine in the rat
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Effect of acute administration of nicotine on in vivo release of noradrenaline in the hippocampus of freely moving rats: A dose-response and antagonist study
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Cognitive Architectures From The Standpoint Of An Experimental Psychologist
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Intravenous cocaine-induced place preference: attenuation by haloperidol
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Conditioning trial duration affects ethanol-induced conditioned place preference in mice
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Effects of 6-OHDA lesions of the central medial nucleus accumbens on rat intravenous morphine self-administration
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Hormonal Modulation of Memory
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Effects of Frequency and Pattern of Medial Forebrain Bundle Stimulation on Caudate Dialysate Dopamine and Serotonin
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Nicotine self‐administration in rats
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Apparent absence of nicotine-induced conditioned place preference in rats
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Effects of cocaine and amphetamine on acetylcholine release in the hippocampus and caudate nucleus
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Attenuation of amphetamine-induced enhancement of learning by adrenal demedullation
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Conditioned locomotor activity but not conditioned place preference following intra-accumbens infusions of cocaine
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Latent learning in hippocampal-lesioned rats
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Pharmacological evidence of a central effect of naltrexone, morphine, and β-endorphin and a peripheral effect of met- and leu-enkephalin on retention of an inhibitory response in mice
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Lack of an effect of 6-hydroxydopamine lesions of the nucleus accumbens on intravenous morphine self-administration
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Regionally specific effects of acute and chronic nicotine on rates of catecholamine and 5-hydroxytryptamine synthesis in rat brain
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Dissociation of visual and olfactory conditioning in the neostriatum of rats
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Cellular investigations of behavioral reinforcement
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Temporal relationship within the conditioning of a saccharine aversion through radiation exposure.
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Effects of cholinergic drugs on extracellular levels of acetylcholine and choline in rat cortex, hippocampus and striatum studied by brain dialysis
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Kappa receptors mediate the peripheral aversive effects of opiates
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Attenuation of punishing effects of morphine and amphetamine by chronic prior treatment.
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Drug Motivation and Abuse: A Neurobiological Perspective
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Self-administration of small amounts of morphine through glass micropipettes into the ventral tegmental area of the rat
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The effects of selective catecholamine depletions by 6-hydroxydopamine on ethanol preference in rats
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GABA and Nucleus Accumbens Glutamate Neurotransmission Modulate Ethanol Self‐Administration in Ratsa
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Ethanol as a reinforcer for rats: Effects of concurrent access to water and alternate positions of water and ethanol
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The relationship between stereotypy and memory improvement produced by amphetamine
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The influence of cocaine self-administration on in vivo dopamine and acetylcholine neurotransmission in rat caudate-putamen
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The Structure and Organization of Memory
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Kainic acid lesions of the nucleus accumbens selectively attenuate morphine self-administration
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Cocaine-induced taste aversions: Effect of route of administration
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ORAL DRUG SELF‐ADMINISTRATION IN RHESUS MONKEYS: INTERACTIONS BETWEEN DRUG AMOUNT AND FIXED‐RATIO SIZE
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Visceral cortex lesions block conditioned taste aversions induced by morphine
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Opiate antagonists enhance the working memory of rats in the radial maze
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Retrograde amnesia and cholinergic systems in the caudate-putamen complex and dorsal hippocampus of the rat
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The effect of systemically applied cholinergic drugs on the striatal release of dopamine and its metabolites, as determined by automated brain dialysis in conscious rats
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Locus coeruleus potentiation of dentate gyrus responses: Evidence for two systems
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Reinforcing and other behavioral effects of nicotine
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Memory facilitation by post-training injection of ethanol
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Ethanol intake in the absence of concurrent food reinforcement
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The reserpine-sensitive dopamine pool mediates (+)-amphetamine-conditioned reward in the place preference paradigm
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Changes in morphine self-administration and morphine dependence after lesions of the caudate nucleus in rats
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The Neostriatal Mosaic: Multiple Levels Of Compartmental Organization In The Basal Ganglia
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Intraventricular self-administration of morphine in naive laboratory rats
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Neurotransmitter turnover in rat striatum is correlated with morphine self-administration
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Is cholinergic activity of the caudate nucleus involved in memory?
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Self-administration of morphine into the lateral hypothalamus in the mouse
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Oral Ethanol Self‐Administration in Free‐Feeding Rhesus Monkeys
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Neurocircuitry of Addiction
Koob, G. F., & Volkow, N. D. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.110 · Cited by 5,340 · see citing works
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 · see citing works
The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking
Ikemoto, S., & Panksepp, J. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00023-5 · Cited by 1,450 · see citing works
Dopamine in drug abuse and addiction: results from imaging studies and treatment implications
Volkow, N. D., Fowler, J. S., Wang, G.-J., & Swanson, J. M. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001507 · Cited by 1,101 · see citing works
Adult neurogenesis: from precursors to network and physiology
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Brain Reward Circuitry
Wise, R. A. (2002) · Neuron · doi:10.1016/s0896-6273(02)00965-0 · Cited by 881 · see citing works
The addicted human brain: insights from imaging studies
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Images of desire: food-craving activation during fMRI
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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
DOI: 10.1111/j.1360-0443.1996.tb03586.x
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
Licence: doi.wiley.com/10.1002/tdm_license_1 (tdm, 7001 d)
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

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Addictive drugs as reinforcers: multiple partial actions on memory systems

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