Influence of Reward Expectation on Visuospatial Processing in Macaque Lateral Prefrontal Cortex

Abstract

The lateral prefrontal cortex (LPFC) has been implicated in visuospatial processing, especially when it is required to hold spatial information during a delay period. It has also been reported that the LPFC receives information about expected reward outcome. However, the interaction between visuospatial processing and reward processing is still unclear because the two types of processing could not be dissociated in conventional delayed response tasks. To examine this, we used a memory-guided saccade task with an asymmetric reward schedule and recorded 228 LPFC neurons. The position of the target cue indicated the spatial location for the following saccade and the color of the target cue indicated the reward outcome for a correct saccade. Activity of LPFC was classified into three main types: S-type activity carried only spatial signals, R-type activity carried only reward signals, and SR-type activity carried both. Therefore only SR-type cells were potentially involved in both visuospatial processing and reward processing. SR-type activity was enhanced (SR+) or depressed (SR-) by the reward expectation. The spatial discriminability as expressed by the transmitted information was improved by reward expectation in SR+ type. In contrast, when reward information was coded by an increase of activity in the reward-absent condition (SR- type), it did not improve the spatial representation. This activity appeared to be involved in gaze fixation. These results extend previous findings suggesting that the LPFC exerts dual influences based on predicted reward outcome: improvement of memory-guided saccades (when reward is expected) and suppression of inappropriate behavior (when reward is not expected).

Modulation of Dorsolateral Prefrontal Delay Activity during Self-Organized Behavior

“…In fact, the level of expectations is similar in the DR task and in repetition, and differs in the search period. Variation in the size of the reward expected by the monkey does not induce delay activity variations comparable with those observed depending on types of trials, a result that have been observed for planning related activity (Kobayashi et al, 2002;Amemori and Sawaguchi, 2006). Finally, pure expectation (directly related to reward probability) does not account for activity changes be- tween the last trials in the search period (indices 3) and the other correct trials: if the amplitude of activity were related to reward probability, then activity should remain elevated for the following repetition trials during which reward expectation is maximal (i.e., during which the probability to get a reward is p ϭ 1).…”

“…Thus, modulation of prefrontal activity during the PS task does not simply reflect an anticipatory reward-related bias as reported in the caudate nucleus . However, it is possible that DLPFC integrates some dimensions of reward expectation (Kobayashi et al, 2002;Amemori and Sawaguchi, 2006) with other factors involved in learning and control of behavior. One candidate is uncertainty.…”

Different Pedunculopontine Tegmental Neurons Signal Predicted and Actual Task Rewards

“…The FT neurons may receive the signals of reward prediction from the orbitofrontal cortex (OFC) (Tremblay and Schultz, 1999;Hikosaka and Watanabe, 2000;Roesch and Olson, 2004;Simmons and Richmond, 2008), prefrontal cortex (Leon and Shadlen, 1999;Kobayashi et al, 2002a;Roesch and Olson, 2003), or the striatum (Mena-Segovia et al, 2004;Hikosaka et al, 2006;Winn, 2006). These structures may learn the cue-reward magnitude contingency during the training and task periods as a synaptic memory and recall that memory as the signals of the predicted reward magnitude at the time of cue presentation.…”

Risk-dependent reward value signal in human prefrontal cortex

“…In turn, it projects to dorsolateral prefrontal and premotor regions, and could, thus, influence behavioral output (51,54). Neurophysiological studies have shown that single lateral prefrontal neurons use reward information to increase spatial discrimination, encode reward-based stimulus category, and integrate reward and response history (64)(65)(66). Together, these findings on expected reward value and risk processing in the lateral prefrontal cortex underline the role of this structure as a key component of the decision system of the brain.…”