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

Abstract

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.

Decoding Stimulus-Reward Pairing From Local Field Potentials Recorded From Monkey Visual Cortex

“…4(a) reveals that the time interval during which a wave with a constant direction is present (around 50-100 ms after stimuli onset) corresponds to the early time interval of a prominent difference in average synchrony between the responses to the rewarded and unrewarded stimuli. This interval also corresponds to the one described in [14] and was attributed to sensorial learning in V4.…”

“…When the signal of interest is large, fewer trials for averaging will be needed. As was shown in [14], which details the conditioning training of the experiment considered in this paper, an early neural response was observed that was suggested to be related to sensorial learning, and a later one to attentional learning. Based on this, temporal features are developed in this paper, and supplemented with a number of spatial features that serve as the input to the classifier whose aim is to distinguish the rewarded from the unrewarded stimulus responses.…”

“…For our analysis, we looked only in the 300-ms time interval after stimulus onset (i.e., 100 ms before the reward) to avoid any influence from receiving the reward, as was done in [14], and concentrate on the differences in the responses to the rewarded and unrewarded stimuli. Also, we considered only those recordings that were preceded by three background noise images and were observed by the monkey without failing to fixate a small dot on the screen.…”

“…5(a)]. These two intervals could correspond to two stages in learning, a sensorial one and an attentive one [14]. Between the monkeys, the difference in timing of these intervals can be due to differences in stimulus size or eccentricity, to the recorded cortical layers, or to slightly different electrical properties of the Utah array.…”

Reward Changes Salience in Human Vision via the Anterior Cingulate

“…Nonetheless, previous work found an enhanced and earlier N2pc-the ERP component used as an index of selective attention in the present study-when elicited by targets associated to the expectation of high rewards (Kiss et al, 2009). Animal electrophysiology is just beginning to explore modulations of visual processing that result from controlled stimulus-reward associations (Schuler and Bear, 2006;Peck et al, 2009;Frankó et al, 2010), but the exact link to the present findings is still unclear. Despite the recent surge of interest, and as noted in Introduction, the impact of reward on attention is not a prominent factor in models of visual search and attention (with the notable exception of Navalpakkam et al, 2009).…”