Reward-dependent spatial selectivity of anticipatory activity in monkey caudate neurons

Many neurons show anticipatory activity in learned tasks. This phenomenon appears to reflect the brain's ability to predict future events. However, what actually is predicted is unknown. Using a memory-guided saccade task, in which only one out of four directions was rewarded in each block of trials, we found that a group of neurons in the monkey caudate nucleus (CD) showed activity before presentation of an instruction cue stimulus. Among 329 CD neurons that were related to memory-guided saccade tasks, 156 showed the precue activity and 91 of them were examined fully. Remarkably, the magnitude of the precue activity varied across the four blocks of the one-direction-rewarded (1DR) condition, depending on which direction was rewarded. A majority of neurons with precue activity (83/91, 91%) showed significant directional preference. The best and worst directions were usually in the contralateral and ipsilateral directions, respectively. Within a block, the precue activity increased rapidly for the best direction in 1DR and decreased gradually for the worst direction in 1DR and all-directions-rewarded (ADR) condition. The precue activity was weak in ADR. The precue activity did not reflect the likelihood of a particular cue stimulus, because the probability of the cue appearing in each direction was the same regardless of the rewarded direction. These results suggest that each CD neuron indicates a particular position-reward association prospectively, usually with contralateral preference. Assuming that the CD neurons have access to saccadic motor outputs, the precue activity would create a motivational bias toward the contralateral space, even before an instruction is given by the cue stimulus.