Dissociable Neural Effects of Long-term Stimulus–Reward Pairing in Macaque Visual Cortex

It has been proposed that perceptual learning may occur through a reinforcement process, in which consistently pairing stimuli with reward is sufficient for learning. We tested whether stimulus–reward pairing is sufficient to increase the sensorial representation of a stimulus by recording local field potentials (LFPs) in macaque extrastriate area V4 with chronically implanted electrodes. Two oriented gratings were repeatedly presented; one was paired with a fluid reward, whereas no reward was given at any other time. During the course of conditioning the LFP increased for the rewarded compared to the unrewarded orientation. The time course of the effect of stimulus–reward pairing and its reversal differed between an early and late interval of the LFP response: a fast change in the later part of the neural response that was dissociated from a slower change in the early part of the response. The fast change of the late interval LFP suggests that this late LFP change is related to enhanced attention during the presentation of the rewarded stimulus. The slower time course of the early interval response suggests an effect of sensorial learning. Thus, simple stimulus–reward pairing is sufficient to strengthen stimulus representations in visual cortex and does this by means of two dissociable mechanisms.