Temporal difference error prediction signal dysregulation in cocaine dependence

Emma Jane Rose, Betty Jo Salmeron, Thomas J. Ross, James Waltz, Julie B. Schweitzer, Samuel M. McClure, Elliot A. Stein

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

Cocaine dependence impacts drug-related, dopamine-dependent reward processing, yet its influence on non-drug reward processing is unclear. Here, we investigated cocaine-mediated effects on reward learning using a natural food reinforcer. Cocaine-dependent subjects (N=14) and healthy controls (N=14) learned to associate a visual cue with a juice reward. In subsequent functional imaging sessions they were exposed to trials where juice was received as learned, withheld (negative temporal difference error (NTDE)), or received unexpectedly (positive temporal difference error (PTDE)). Subjects were scanned twice in sessions that were identical, except that cocaine-dependent participants received cocaine or saline 10 min before task onset. In the insula, precentral and postcentral gyri NTDE signals were greater, and PTDE-related function was reduced in cocaine-dependent subjects. Compared with healthy controls, in the cocaine-dependent group PTDE signals were also reduced in medial frontal gyrus and reward-related function, irrespective of predictability, was reduced in the putamen. Group differences in error-related activity were predicted by the time as last self-administered cocaine use, but TDE function was not influenced by acute cocaine. Thus, cocaine dependence seems to engender increased responsiveness to unexpected negative outcomes and reduced sensitivity to positive events in dopaminergic reward regions. Although it remains to be established if these effects are a consequence of or antecedent to cocaine dependence, they likely have implications for the high-cocaine use recidivism rates by contributing to the drive to consume cocaine, perhaps via influence on dopamine-related reward computations. The fact that these effects do not acquiesce to acute cocaine administration might factor in binge-related escalated consumption.

Original languageEnglish (US)
Pages (from-to)1732-1742
Number of pages11
JournalNeuropsychopharmacology
Volume39
Issue number7
DOIs
StatePublished - Jan 1 2014

Fingerprint

Cocaine-Related Disorders
Cocaine
Reward
Dichlorodiphenyldichloroethane
Dopamine Agents
Somatosensory Cortex
Putamen
Frontal Lobe
Prefrontal Cortex
Cues
Dopamine
Learning

All Science Journal Classification (ASJC) codes

  • Pharmacology
  • Psychiatry and Mental health

Cite this

Rose, E. J., Salmeron, B. J., Ross, T. J., Waltz, J., Schweitzer, J. B., McClure, S. M., & Stein, E. A. (2014). Temporal difference error prediction signal dysregulation in cocaine dependence. Neuropsychopharmacology, 39(7), 1732-1742. https://doi.org/10.1038/npp.2014.21
Rose, Emma Jane ; Salmeron, Betty Jo ; Ross, Thomas J. ; Waltz, James ; Schweitzer, Julie B. ; McClure, Samuel M. ; Stein, Elliot A. / Temporal difference error prediction signal dysregulation in cocaine dependence. In: Neuropsychopharmacology. 2014 ; Vol. 39, No. 7. pp. 1732-1742.
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Rose, EJ, Salmeron, BJ, Ross, TJ, Waltz, J, Schweitzer, JB, McClure, SM & Stein, EA 2014, 'Temporal difference error prediction signal dysregulation in cocaine dependence', Neuropsychopharmacology, vol. 39, no. 7, pp. 1732-1742. https://doi.org/10.1038/npp.2014.21

Temporal difference error prediction signal dysregulation in cocaine dependence. / Rose, Emma Jane; Salmeron, Betty Jo; Ross, Thomas J.; Waltz, James; Schweitzer, Julie B.; McClure, Samuel M.; Stein, Elliot A.

In: Neuropsychopharmacology, Vol. 39, No. 7, 01.01.2014, p. 1732-1742.

Research output: Contribution to journalArticle

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Rose EJ, Salmeron BJ, Ross TJ, Waltz J, Schweitzer JB, McClure SM et al. Temporal difference error prediction signal dysregulation in cocaine dependence. Neuropsychopharmacology. 2014 Jan 1;39(7):1732-1742. https://doi.org/10.1038/npp.2014.21