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The Journal of Neuroscience, December 26, 2007, 27(52):14502-14514; doi:10.1523/JNEUROSCI.3060-07.2007

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Behavioral/Systems/Cognitive
Action and Outcome Encoding in the Primate Caudate Nucleus

Brian Lau and Paul W. Glimcher

Center for Neural Science, New York University, New York, New York 10003

Correspondence should be addressed to Paul W. Glimcher, Center for Neural Science, New York University, 4 Washington Place, Room 809, New York, NY 10003. Email: pglimcher{at}cns.nyu.edu

The basal ganglia appear to have a central role in reinforcement learning. Previous experiments, focusing on activity preceding movement execution, support the idea that dorsal striatal neurons bias action selection according to the expected values of actions. However, many phasically active striatal neurons respond at a time too late to initiate or select movements. Given the data suggesting a role for the basal ganglia in reinforcement learning, postmovement activity may therefore reflect evaluative processing important for learning the values of actions. To better understand these postmovement neurons, we determined whether individual striatal neurons encode information about saccade direction, whether a reward had been received, or both. We recorded from phasically active neurons in the caudate nucleus while monkeys performed a probabilistically rewarded delayed saccade task. Many neurons exhibited peak responses after saccade execution (77 of 149) that were often tuned for the direction of the preceding saccade (61 of 77). Of those neurons responding during the reward epoch, one subset showed direction tuning for the immediately preceding saccade (43 of 60), whereas another subset responded differentially on rewarded versus unrewarded trials (35 of 60). We found that there was relatively little overlap of these properties in individual neurons. The encoding of action and outcome was performed by largely separate populations of caudate neurons that were active after movement execution. Thus, striatal neurons active primarily after a movement appear to be segregated into two distinct groups that provide complimentary information about the outcomes of actions.

Key words: basal ganglia; oculomotor; reward; reinforcement learning; monkey; caudate

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Received May 7, 2007; revised Nov. 22, 2007; accepted Nov. 26, 2007.

Correspondence should be addressed to Paul W. Glimcher, Center for Neural Science, New York University, 4 Washington Place, Room 809, New York, NY 10003. Email: pglimcher{at}cns.nyu.edu

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