Rewarding feedback after correct visual discriminations has both general and specific influences on visual cortex

Abstract

Reward can influence visual performance, but the neural basis of this effect remains poorly understood. Here we used functional magnetic resonance imaging to investigate how rewarding feedback affected activity in distinct areas of human visual cortex, separating rewarding feedback events after correct performance from preceding visual events. Participants discriminated oriented gratings in either hemifield, receiving auditory feedback at trial end that signaled financial reward after correct performance. Greater rewards improved performance for all but the most difficult trials. Rewarding feedback increased blood-oxygen-level-dependent (BOLD) signals in striatum and orbitofrontal cortex. It also increased BOLD signals in visual areas beyond retinotopic cortex, but not in primary visual cortex representing the judged stimuli. These modulations were seen at a time point in which no visual stimuli were presented or expected, demonstrating a novel type of activity change in visual cortex that cannot reflect modulation of response to incoming or anticipated visual stimuli. Rewarded trials led on the next trial to improved performance and enhanced visual activity contralateral to the judged stimulus, for retinotopic representations of the judged visual stimuli in V1. Our findings distinguish general effects in nonretinotopic visual cortex when receiving rewarding feedback after correct performance from consequences of reward for spatially specific responses in V1.

Fig. 1.

Procedure and behavioral findings. A: trials were grouped into short “mini-blocks” of 4 with 2 possible reward levels: 10 or 80 pence per correct discrimination. At the onset of each mini-block, participants heard an auditory cue informing them of the reward level for that mini-block. The onset of each trial began with a small visual precue directing participants to attend covertly to either the left or right grating. Attended side remained constant throughout the mini-block. This was followed by the visual stimuli to discriminate: participants fixated centrally while attending to one side and were shown bilateral gratings for 300 ms, followed by a uniform gray screen, and then a further pair of bilateral gratings with different orientations. The task was to decide, for the attended side only, which display (1st or 2nd) contained the grating with the more vertical orientation. Participants were given 3–5 s to respond using a key press. This was followed by auditory feedback, informing participants of the amount won for a correct response, e.g., “you get 80 pence,” or for an incorrect response: “you get 0 pence.” Jittering the separation of reward feedback from the discrimination task, together with the different levels of reward and the rewarded or no-reward outcome, allowed us to dissociate hemodynamic responses that were specific to the feedback of reward from responses associated with the visual discrimination (see main text). The inter-trial interval was 3–5 s. B: higher reward levels were associated with improved accuracy in the visual discrimination task for the easier but not the hardest trials. C: there were no differences in accuracy for visual discrimination of gratings attended in the left or right hemifields. Error bars = 1 SE of the difference between paired conditions. **, statistical significance (P < 0.05, 2-tailed paired t-test), NS, not significant.

Fig. 2.

Differences in brain activity during visual discrimination. Blood-oxygen-level-dependent (BOLD) signal change (percent relative to the global mean) averaged across 11 retinotopically mapped participants, for the regions of interest (ROIs) responding to the grating stimuli in V1–V3 during the visual-discrimination phase of the trial. Responses are plotted separately for gratings attended in the contra- or ipsilateral hemifields. Error bars are SE of the difference between paired conditions; *, statistical significance (P < 0.05, 2-tailed paired t-test).

Fig. 3.

Changes in brain activity during reward feedback. A: whole brain analysis reveals cortical regions showing increased BOLD signal for rewarded minus nonrewarded trials, during the (auditory) feedback phase of the trial. Activations are projected onto axial, coronal, and axial MRI slices of a T1-weighted canonical brain, thresholded at P < 0.005 uncorrected for display. See results for coordinates, P values, and t scores. B: in visual ROIs, the difference in percent signal change between rewarded minus nonrewarded trials is shown, divided by the sum of activation for the ROIs in V1–V3 and for higher visual cortex (as identified on whole brain analysis). Normalized values are displayed to enable comparison between activity in these different visual areas, but all statistics were performed on actual percentage signal change. Error bars are SE of the difference between paired conditions. C: cortical regions showing increased BOLD signal for rewarded vs. nonrewarded trials during the feedback phase of the trial (threshold: P < 0.005 uncorrected) shown in yellow, along with the combined ROIs for the gratings in V1–V3 for 11 participants (shown in blue), all projected onto coronal, sagittal, and axial MRI slices of a T1-weighted canonical brain at the coordinates shown. Note that the regions responding to rewarded trials are anterior and lateral to the ROIs in V1–3.

Fig. 4.

Trial-to-trial effects of receiving reward feedback following correct discrimination. A: behavioral results. Receiving reward feedback on the previous trial (n − 1) was associated with improved accuracy on the subsequent trial, compared with after a trial that had not been rewarded. However, this effect was not seen for earlier trials: there was no improved accuracy on trials where the previous but 1 trial (n − 2) was rewarded or where the trial prior to that had been rewarded (n − 3). Group means of 12 participants are shown. Error bars indicate the SE of the difference between paired conditions; *, statistical significance. (P = 0.05, 1-tailed paired t-test). B: effect of trials receiving reward feedback on percent signal change in V1. BOLD signal change (percent relative to the global mean) averaged across 11 retinotopically mapped participants, for the V1 stimulus-responsive ROI, during the visual-discrimination phase of the trial, shown for trials subsequent to reward feedback, or to nonreward feedback, separately when attending to ipsilateral or contralateral gratings. Note that for trials preceded by reward feedback, there is a greater difference in percent signal change between attending to a contra- vs. ipsilateral grating, than after unrewarded trials. Error bars indicate the SE of the difference between paired conditions; **, statistical significance (P < 0.05, 2-tailed paired t-test).