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Vol. 54, Issue 1, 1-42, March 2002
Behavioral Neuroscience Branch, Intramural Research Program,
National Institute on Drug Abuse, National Institutes of Health,
Baltimore, Maryland
I. Introduction
A. Background and Overview
B. Experimental Approaches
II. Drug Priming-Induced Reinstatement
A. Dopamine
1. Cocaine Priming.
2. Heroin Priming.
B. Opioids
1. Cocaine Priming.
2. Heroin Priming.
C. Glutamate
D. Other Neurotransmitter Systems
1. 5-Hydroxytryptamine.
2. Corticosterone.
3. 
-Aminobutyric Acid.
4. Noradrenaline.
5. Acetylcholine.
6. Endocannabinoids.
E. Summary
III. Cue-Induced Reinstatement
A. Discrete Conditioned Stimuli
B. Extinction Behavior
C. Discriminative and Contextual Drug Cues
1. Discriminative Drug Cues.
2. Contextual Drug Cues.
D. Summary
IV. Stress-Induced Reinstatement
A. Dopamine and Opioids
B. Corticosterone and Corticotropin-Releasing Factor
1. Corticosterone.
2. Corticotropin-Releasing Factor.
C. Noradrenaline
D. Other Neurotransmitter Systems
E. Summary
V. Discussion
A. Neural Mechanisms Underlying Relapse to Heroin and Cocaine: a
Summary
1. Drug Priming-Induced Reinstatement.
2. Cue-Induced Reinstatement.
3. Stress-Induced Reinstatement.
B. Theoretical Issues
1. Drug Priming.
2. Drug Cues.
3. Stress.
4. Summary.
C. Methodological Issues
1. Prior Training for Food Reinforcement.
2. Noncontingent Priming Injections during Training.
3. Response Rates during Training.
4. Amount of Drug Exposure during Training.
5. The Drug Withdrawal Period Prior to Tests for
Reinstatement.
6. Side Effects of the Pharmacological and Brain
Manipulations.
7. Summary.
D. Emerging Issues
1. Does Drug Sensitization Contribute to Relapse to Heroin and
Cocaine?
a. Drug Priming and Drug Cues.
b. Stress.
2. Application of the Reinstatement Model to Mice.
E. Concluding Remarks and Implications for Addiction Theories and
Treatment
1. Implications for Addiction Theories.
2. Implications for Treatment.
Acknowledgments
References
The objective of this article is to review data from studies that used a reinstatement model in rats to elucidate the neural mechanisms underlying relapse to heroin and cocaine seeking induced by exposure to the self-administered drug (drug priming), conditioned drug cues, and stressors. These factors were reported to contribute to relapse to drug use in humans following prolonged abstinence periods. In the reinstatement model, the ability of acute exposure to drug or nondrug stimuli to reinstate drug seeking is determined following training for drug self-administration and subsequent extinction of the drug-reinforced behavior. We will review studies in which pharmacological agents were injected systemically or intracranially to block (or mimic) reinstatement by drug priming, drug cues, and stressors. We also will review studies in which brain lesions, in vivo microdialysis and electrochemistry, and gene expression methods were used to map brain sites involved in relapse to drug seeking. Subsequently, we will discuss theoretical issues related to the processes underlying relapse to drugs and address methodological issues in studies on reinstatement of drug seeking. Finally, the implications of the findings from the studies reviewed for addiction theories and treatment will be discussed. The main conclusion of this review is that the neuronal mechanisms involved in relapse to heroin and cocaine seeking induced by drug priming, drug cues, and stressors are to a large degree dissociable. The data reviewed also suggest that the neuronal events mediating drug-induced reinstatement are to some degree dissociable from those mediating drug reinforcement.
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