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The Journal of Neuroscience, December 17, 2008, 28(51):13775-13785; doi:10.1523/JNEUROSCI.3541-08.2008

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Behavioral/Systems/Cognitive
Frontal Cortex Subregions Play Distinct Roles in Choices between Actions and Stimuli

Peter H. Rudebeck,¹ Timothy E. Behrens,¹ Steven W. Kennerley,² Mark G. Baxter,¹ Mark J. Buckley,¹ Mark E. Walton,¹ and Matthew F. S. Rushworth¹

¹Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD, United Kingdom, and ²Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, California 94720

Correspondence should be addressed to Peter H. Rudebeck at his present address: Laboratory of Neuropsychology, National Institute of Mental Health–National Institutes of Health, Building 49, Suite 1B80, 49 Convent Drive, Bethesda, MD 20892-4415. Email: rudebeckp{at}mail.nih.gov

The orbitofrontal cortex (OFC) has been implicated in reinforcement-guided decision making, error monitoring, and the reversal of behavior in response to changing circumstances. The anterior cingulate cortex sulcus (ACC_S), however, has also been implicated in similar aspects of behavior. Dissociating the unique functions of these areas would improve our understanding of the decision-making process. The effect of selective OFC lesions on how monkeys used the history of reinforcement to guide choices of either particular actions or particular stimuli was studied and compared with the effects of ACC_S lesions. Both lesions disrupted decision making, but their effects were differentially modulated by the dependence on action– or stimulus–value contingencies. OFC lesions caused a deficit in stimulus but not action selection, whereas ACC_S lesions had the opposite effect, disrupting action but not stimulus selection. Furthermore, OFC lesions that have previously been found to impair decision making when deterministic stimulus–reward contingencies are switched were found to cause a more general learning impairment in more naturalistic situations in which reward was stochastic. Both OFC and ACC_S are essential for reinforcement-guided decision making rather than just error monitoring or behavioral reversal. The OFC and ACC_S are both, however, more concerned with learning and making decisions, but their roles in selecting between stimulus and action values are distinct.

Key words: reward; prefrontal cortex; learning; macaque; decision; cingulate

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Received July 28, 2008; revised Oct. 14, 2008; accepted Nov. 3, 2008.

Correspondence should be addressed to Peter H. Rudebeck at his present address: Laboratory of Neuropsychology, National Institute of Mental Health–National Institutes of Health, Building 49, Suite 1B80, 49 Convent Drive, Bethesda, MD 20892-4415. Email: rudebeckp{at}mail.nih.gov

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