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The Journal of Neuroscience, September 9, 2009, 29(36):11182-11191; doi:10.1523/JNEUROSCI.1929-09.2009

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Behavioral/Systems/Cognitive
Reward Modulates Attention Independently of Action Value in Posterior Parietal Cortex

Christopher J. Peck,^1 * David C. Jangraw,^1 * Mototaka Suzuki,¹ Richard Efem,¹ and Jacqueline Gottlieb^1,2

Departments of ¹Neuroscience and ²Psychiatry, Columbia University, New York, New York 10032

Correspondence should be addressed to Dr. Jacqueline Gottlieb, Department of Neuroscience, Columbia University, 1051 Riverside Drive, Unit 87, New York, NY 10032. Email: jg2141{at}columbia.edu

While numerous studies have explored the mechanisms of reward-based decisions (the choice of action based on expected gain), few have asked how reward influences attention (the selection of information relevant for a decision). Here we show that a powerful determinant of attentional priority is the association between a stimulus and an appetitive reward. A peripheral cue heralded the delivery of reward or no reward (these cues are termed herein RC+ and RC–, respectively); to experience the predicted outcome, monkeys made a saccade to a target that appeared unpredictably at the same or opposite location relative to the cue. Although the RC had no operant associations (did not specify the required saccade), they automatically biased attention, such that an RC+ attracted attention and an RC– repelled attention from its location. Neurons in the lateral intraparietal area (LIP) encoded these attentional biases, maintaining sustained excitation at the location of an RC+ and inhibition at the location of an RC–. Contrary to the hypothesis that LIP encodes action value, neurons did not encode the expected reward of the saccade. Moreover, at odds with an adaptive decision process, the cue-evoked biases interfered with the required saccade, and these biases increased rather than abating with training. After prolonged training, valence selectivity appeared at shorter latencies and automatically transferred to a novel task context, suggesting that training produced visual plasticity. The results suggest that reward predictors gain automatic attentional priority regardless of their operant associations, and this valence-specific priority is encoded in LIP independently of the expected reward of an action.

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Received April 22, 2009; revised July 16, 2009; accepted July 29, 2009.

Correspondence should be addressed to Dr. Jacqueline Gottlieb, Department of Neuroscience, Columbia University, 1051 Riverside Drive, Unit 87, New York, NY 10032. Email: jg2141{at}columbia.edu

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