Abstract

In order for organisms to survive, they need to detect rewarding stimuli, for example, food or a mate, in a complex environment with many competing stimuli. These rewarding stimuli should be detected even if they are nonsalient or irrelevant to the current goal. The value-driven theory of attentional selection proposes that this detection takes place through reward-associated stimuli automatically engaging attentional mechanisms. But how this is achieved in the brain is not very well understood. Here, we investigate the effect of differential reward on the multiunit activity in visual area V4 of monkeys performing a perceptual judgment task. Surprisingly, instead of finding reward-related increases in neural responses to the perceptual target, we observed a large suppression at the onset of the reward indicating cues. Therefore, while previous research showed that reward increases neural activity, here we report a decrease. More suppression was caused by cues associated with higher reward than with lower reward, although neither cue was informative about the perceptually correct choice. This finding of reward-associated neural suppression further highlights normalization as a general cortical mechanism and is consistent with predictions of the value-driven attention theory.

Highlights

  • The reward system of the brain is essential for the survival of complex organisms because it generates the teaching signal that encourages behaviors contributing to selective fitness (Dayan and Balleine 2002; Wise 2004)

  • The two saccade targets changed color. They assumed the additional function of cues which indicated the reward value of correct saccades to each location. This resulted in four possible conditions, high reward (HH) and LL, in which both saccade directions led to high or low reward, respectively, and HL and LH, in which the two saccade targets were associated with different reward magnitudes

  • When reward-predicting visual cues appeared in the receptive fields (RF) surrounds of the assessed neurons, the neural responses to the target stimulus positioned in the RF were strongly suppressed

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Summary

Introduction

The reward system of the brain is essential for the survival of complex organisms because it generates the teaching signal that encourages behaviors contributing to selective fitness (Dayan and Balleine 2002; Wise 2004). It is crucial to gain a better understanding of how reward signals impact the brain’s responses to stimuli and influence behavior. To understand better how reward influences behavior, we investigated how nonsensory aspects of a task, expected reward and behavioral choice, interact with the sensory representation of stimuli in the early visual cortex. We reasoned that this counterintuitive outcome can be accounted for if the cues predicting reward value had themselves attracted attention, the amount of allocated attention depending on the amount of predicted reward

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