Immediate changes in anticipatory activity of caudate neurons associated with reversal of position-reward contingency

The primate caudate nucleus plays a crucial role in transforming cognitive/motivational information into eye movement signals. A subset of caudate projection neurons fire before a visual target's onset. This anticipatory activity is sensitive to position-reward contingencies and correlates with saccade latency, which is shorter toward a rewarded position. We recorded single-unit activity of caudate projection neurons to examine the dynamics of change in anticipatory activity immediately after switches of the position-reward contingency. Two monkeys performed a visually guided saccade task where only one position was associated with reward. The position-reward mapping remained constant within a block, but was reversed frequently between blocks without any indication to the monkey. Therefore the switch could be detected only by unexpected reward delivery or unexpected lack of reward. After the switch, both saccade latency and anticipatory activity showed reliable changes already in the second trial, whether or not the first trial was rewarded. However, anticipatory activity in the second trial was generally higher if the first trial was rewarded, and the measured saccade latencies could be better explained by the difference in anticipatory activity between the two caudate nuclei. We suggest that anticipatory activity of caudate neurons reflects the reversal set of reward-position contingency.