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The Journal of Neuroscience, August 9, 2006, 26(32):8368-8376; doi:10.1523/JNEUROSCI.0271-06.2006

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Behavioral/Systems/Cognitive
Reward-Related Cortical Inputs Define a Large Striatal Region in Primates That Interface with Associative Cortical Connections, Providing a Substrate for Incentive-Based Learning

Suzanne N. Haber,¹ Ki-Sok Kim,² Philippe Mailly,³ and Roberta Calzavara¹

¹Department of Pharmacology and Physiology, University of Rochester School of Medicine, Rochester, New York 14642, ²Department of Public Health, Keimyung University, Taegue 704-701, Korea, and ³Neurobiologie des Signaux Intercellulaires, Centre National de la Recherche Scientifique, Universite Pierre et Marie Curie, 75252 Paris, France

Correspondence should be addressed to Dr. Suzanne N. Haber, Department of Pharmacology and Physiology, University of Rochester School of Medicine, 601 Elmwood Avenue, Rochester, NY 14642. Email: suzanne_haber{at}urmc.rochester.edu

The anterior cingulate and orbital cortices and the ventral striatum process different aspects of reward evaluation, whereas the dorsolateral prefrontal cortex and the dorsal striatum are involved in cognitive function. Collectively, these areas are critical to decision making. We mapped the striatal area that receives information about reward evaluation. We also explored the extent to which terminals from reward-related cortical areas converge in the striatum with those from cognitive regions. Using three-dimensional-rendered reconstructions of corticostriatal projection fields along with two-dimensional chartings, we demonstrate the reward and cognitive territories in the primate striatum and show the convergence between these cortical inputs. The results show two labeling patterns: a focal projection field that consists of densely distributed terminal patches, and a diffuse projection consisting of clusters of fibers, extending throughout a wide area of the striatum. Together, these projection fields demonstrate a remarkably large, rostral, reward-related striatal territory that reaches into the dorsal striatum. Fibers from different reward-processing and cognitive cortical areas occupy both separate and converging territories. Furthermore, the diffuse projection may serve a separate integrative function by broadly disseminating general cortical activity. These findings show that the rostral striatum is in a unique position to mediate different aspects of incentive learning. Furthermore, areas of convergence may be particularly sensitive to dopamine modulation during decision making and habit formation.

Key words: decision making; incentive learning; dorsolateral prefrontal cortex; orbital cortex; cingulate cortex; ventral striatum; dopamine

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Received Jan. 20, 2006; revised July 10, 2006; accepted July 11, 2006.

Correspondence should be addressed to Dr. Suzanne N. Haber, Department of Pharmacology and Physiology, University of Rochester School of Medicine, 601 Elmwood Avenue, Rochester, NY 14642. Email: suzanne_haber{at}urmc.rochester.edu

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