Comparing the neural basis of monetary reward and cognitive feedback during information-integration category learning

Abstract

The dopaminergic system is known to play a central role in reward-based learning (Schultz, 2006), yet it was also observed to be involved when only cognitive feedback is given (Aron et al., 2004). Within the domain of information-integration category learning, in which information from several stimulus dimensions has to be integrated predecisionally (Ashby and Maddox, 2005), the importance of contingent feedback is well established (Maddox et al., 2003). We examined the common neural correlates of reward anticipation and prediction error in this task. Sixteen subjects performed two parallel information-integration tasks within a single event-related functional magnetic resonance imaging session but received a monetary reward only for one of them. Similar functional areas including basal ganglia structures were activated in both task versions. In contrast, a single structure, the nucleus accumbens, showed higher activation during monetary reward anticipation compared with the anticipation of cognitive feedback in information-integration learning. Additionally, this activation was predicted by measures of intrinsic motivation in the cognitive feedback task and by measures of extrinsic motivation in the rewarded task. Our results indicate that, although all other structures implicated in category learning are not significantly affected by altering the type of reward, the nucleus accumbens responds to the positive incentive properties of an expected reward depending on the specific type of the reward.

Figure 1.

Category structures and sample stimuli. Each square denotes the orientation and line width of a stimulus from category A, and each triangle denotes those of a stimulus from category B. The lines represent the optimal decision bound. Two types of category structures were presented, one with a positive slope of the optimal decision bound and one with a negative slope. For both types of stimuli used in the experiment (circles and lines), examples of three stimuli from each category are shown. Both types of stimuli were used with both types of decision bounds. Note that 0° does not correspond to a horizontal alignment of the stimuli to make the verbalization of a categorization rule more difficult.

Figure 2.

Trial structure. Each trial started with the presentation of a stimulus for 2 s. Subjects were instructed to respond during this period by the pressing of one of two buttons. The stimulus was followed by a delay that was randomly sampled from an exponential distribution with a mean of 2 s (range of 0.5–6 s), after which feedback was presented for 1.5 s. Positive feedback was given by showing a green circle, or, in the rewarded condition by a 20¢ coin, and a high tone. Negative feedback consisted of a red circle and a low tone. If the subject failed to respond, a yellow circle was presented together with the low tone. Trials were separated by an interval that was randomly sampled from an exponential distribution with a mean of 6 s (range of 1–12 s).

Figure 3.

Session structure. Each subject was trained on both tasks on the day before the fMRI session. Whether the first task was rewarded or not, whether it contained circle or line stimuli, and whether the optimal decision bound had a positive or negative slope was randomized across subjects. Training ended independently for both tasks after the subject reached an accuracy rate of 80% within a single block. During the fMRI session, the two trained tasks were presented alternatingly in four blocks of 50 trials each.

Figure 4.

fMRI results. A, Activation in the contrast of monetary reward minus cognitive feedback during stimulus presentation. The time course represents the finite impulse response (FIR) to both monetary reward and cognitive feedback during stimulus presentation, extracted using MarsBar and an anatomical ROI of the nucleus accumbens from the Harvard–Oxford subcortical structural atlas. For each subject, individual functional ROIs within this anatomical ROI were defined based on the areas in which the main effect of stimulus presentation exceeded an uncorrected threshold of p ≤ 0.1. Error bars represent the SEM. Results of this analysis are also plotted separately for subjects with use of the optimal decision bound in at least one condition and those with no information-integration use (no II use). A significant peak activation difference between the task conditions is only observed in the group of subjects with information-integration use (II use). B, C, E, F, Activations (yellow to red) and deactivations (white to blue) for contrasts against fixation. B, Successful categorization minus fixation. Activations are observed in occipital and parietal cortices, as well as in subcortical areas. C, Unsuccessful categorization minus fixation. Activations are mainly observed in occipital and parietal cortices. D, Activations in the contrast of successful minus unsuccessful categorization. No voxel showed higher activations for unsuccessful categorization, whereas bilateral clusters of higher activation during successful categorization were observed in the putamen. E, Positive feedback minus fixation. Both the caudate nuclei and the hippocampi are activated. F, Negative feedback minus fixation. Activations include the rostral cingulate zone and right prefrontal areas. G, Activations in the contrast of positive minus negative feedback. Voxels that were more activated during the processing of negative feedback include the RCZ and anterior insula, whereas voxels more activated during the processing of positive feedback are observed in the nucleus accumbens and right caudate body. All maps are thresholded at a level of p_FWE < 0.05. Left hemisphere is presented at the left.