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Disruption of model-based behavior and learning by cocaine self-administration in rats

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Abstract

Rationale

Addiction is characterized by maladaptive decision-making, in which individuals seem unable to use adverse outcomes to modify their behavior. Adverse outcomes are often infrequent, delayed, and even rare events, especially when compared to the reliable rewarding drug-associated outcomes. As a result, recognizing and using information about their occurrence put a premium on the operation of so-called model-based systems of behavioral control, which allow one to mentally simulate outcomes of different courses of action based on knowledge of the underlying associative structure of the environment. This suggests that addiction may reflect, in part, drug-induced dysfunction in these systems. Here, we tested this hypothesis.

Objectives

This study aimed to test whether cocaine causes deficits in model-based behavior and learning independent of requirements for response inhibition or perception of costs or punishment.

Methods

We trained rats to self-administer sucrose or cocaine for 2 weeks. Four weeks later, the rats began training on a sensory preconditioning and inferred value blocking task. Like devaluation, normal performance on this task requires representations of the underlying task structure; however, unlike devaluation, it does not require either response inhibition or adapting behavior to reflect aversive outcomes.

Results

Rats trained to self-administer cocaine failed to show conditioned responding or blocking to the preconditioned cue. These deficits were not observed in sucrose-trained rats nor did they reflect any changes in responding to cues paired directly with reward.

Conclusions

These results imply that cocaine disrupts the operation of neural circuits that mediate model-based behavioral control.

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Acknowledgments

This work was supported by the Intramural Research Program (G.S.) and grants from the National Institute on Drug Abuse (H.M.W. F30-DA033100, J.L.J. F32-DA031517). The opinions expressed in this article are the authors' own and do not reflect the view of the NIH/DHHS.

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Authors and Affiliations

  1. Cellular Neurobiology Research Branch, Behavioral Neurophysiology Research Section, National Institute on Drug Abuse Intramural Research Program, 251 Bayview Blvd., Baltimore, MD, 21224, USA

    Heather M. Wied, Joshua L. Jones, Nisha K. Cooch, Benjamin A. Berg & Geoffrey Schoenbaum

  2. Department of Anatomy and Neurobiology, University of Maryland School of Medicine, 20 Penn St., Baltimore, MD, 21201, USA

    Heather M. Wied, Joshua L. Jones, Nisha K. Cooch & Geoffrey Schoenbaum

  3. Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University, Baltimore, MD, USA

    Geoffrey Schoenbaum

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  1. Heather M. Wied
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  2. Joshua L. Jones
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  3. Nisha K. Cooch
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  4. Benjamin A. Berg
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  5. Geoffrey Schoenbaum
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Correspondence to Geoffrey Schoenbaum.

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Wied, H.M., Jones, J.L., Cooch, N.K. et al. Disruption of model-based behavior and learning by cocaine self-administration in rats. Psychopharmacology 229, 493–501 (2013). https://doi.org/10.1007/s00213-013-3222-6

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  • DOI: https://doi.org/10.1007/s00213-013-3222-6

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