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Articles, Behavioral/Cognitive

Direct-Pathway Striatal Neurons Regulate the Retention of Decision-Making Strategies

Susan M. Ferguson, Paul E. M. Phillips, Bryan L. Roth, Jürgen Wess and John F. Neumaier
Journal of Neuroscience 10 July 2013, 33 (28) 11668-11676; DOI: https://doi.org/10.1523/JNEUROSCI.4783-12.2013
Susan M. Ferguson
1Center for Integrative Brain Research, Seattle Children's Research Institute, Seattle, Washington 98101,
Departments of 2Psychiatry and Behavioral Sciences and
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Paul E. M. Phillips
Departments of 2Psychiatry and Behavioral Sciences and
3Pharmacology, University of Washington, Seattle, Washington 98195,
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Bryan L. Roth
4Department of Pharmacology, Division of Chemical Biology and National Institute of Mental Health Psychoactive Drug Screening Program, University of North Carolina Medical School, Chapel Hill, North Carolina 27599, and
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Jürgen Wess
5Laboratory of Bioorganic Chemistry, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland 20892
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John F. Neumaier
Departments of 2Psychiatry and Behavioral Sciences and
3Pharmacology, University of Washington, Seattle, Washington 98195,
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Abstract

The dorsal striatum has been implicated in reward-based decision making, but the role played by specific striatal circuits in these processes is essentially unknown. Using cell phenotype-specific viral vectors to express engineered G-protein-coupled DREADD (designer receptors exclusively activated by designer drugs) receptors, we enhanced Gi/o- or Gs-protein-mediated signaling selectively in direct-pathway (striatonigral) neurons of the dorsomedial striatum in Long–Evans rats during discrete periods of training of a high versus low reward-discrimination task. Surprisingly, these perturbations had no impact on reward preference, task performance, or improvement of performance during training. However, we found that transiently increasing Gi/o signaling during training significantly impaired the retention of task strategies used to maximize reward obtainment during subsequent preference testing, whereas increasing Gs signaling produced the opposite effect and significantly enhanced the encoding of a high-reward preference in this decision-making task. Thus, the fact that the endurance of this improved performance was significantly altered over time—long after these neurons were manipulated—indicates that it is under bidirectional control of canonical G-protein-mediated signaling in striatonigral neurons during training. These data demonstrate that cAMP-dependent signaling in direct-pathway neurons play a well-defined role in reward-related behavior; that is, they modulate the plasticity required for the retention of task-specific information that is used to improve performance on future renditions of the task.

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The Journal of Neuroscience: 33 (28)
Journal of Neuroscience
Vol. 33, Issue 28
10 Jul 2013
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Direct-Pathway Striatal Neurons Regulate the Retention of Decision-Making Strategies
Susan M. Ferguson, Paul E. M. Phillips, Bryan L. Roth, Jürgen Wess, John F. Neumaier
Journal of Neuroscience 10 July 2013, 33 (28) 11668-11676; DOI: 10.1523/JNEUROSCI.4783-12.2013

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Direct-Pathway Striatal Neurons Regulate the Retention of Decision-Making Strategies
Susan M. Ferguson, Paul E. M. Phillips, Bryan L. Roth, Jürgen Wess, John F. Neumaier
Journal of Neuroscience 10 July 2013, 33 (28) 11668-11676; DOI: 10.1523/JNEUROSCI.4783-12.2013
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