Reward- and Attention-related Biasing of Sensory Selection in Visual Cortex

Abstract

Attention to task-relevant features leads to a biasing of sensory selection in extrastriate cortex. Features signaling reward seem to produce a similar bias, but how modulatory effects due to reward and attention relate to each other is largely unexplored. To address this issue, it is critical to separate top-down settings defining reward relevance from those defining attention. To this end, we used a visual search paradigm in which the target's definition (attention to color) was dissociated from reward relevance by delivering monetary reward on search frames where a certain task-irrelevant color was combined with the target-defining color to form the target object. We assessed the state of neural biasing for the attended and reward-relevant color by analyzing the neuromagnetic brain response to asynchronously presented irrelevant distractor probes drawn in the target-defining color, the reward-relevant color, and a completely irrelevant color as a reference. We observed that for the prospect of moderate rewards, the target-defining color but not the reward-relevant color produced a selective enhancement of the neuromagnetic response between 180 and 280 msec in ventral extrastriate visual cortex. Increasing reward prospect caused a delayed attenuation (220-250 msec) of the response to reward probes, which followed a prior (160-180 msec) response enhancement in dorsal ACC. Notably, shorter latency responses in dorsal ACC were associated with stronger attenuation in extrastriate visual cortex. Finally, an analysis of the brain response to the search frames revealed that the presence of the reward-relevant color in search distractors elicited an enhanced response that was abolished after increasing reward size. The present data together indicate that when top-down definitions of reward relevance and attention are separated, the behavioral significance of reward-associated features is still rapidly coded in higher-level cortex areas, thereby commanding effective top-down inhibitory control to counter a selection bias for those features in extrastriate visual cortex.