Information content and reward processing in the human striatum during performance of a declarative memory task

Abstract

Negative feedback can signal poor performance, but it also provides information that can help learners reach the goal of task mastery. The primary aim of this study was to test the hypothesis that the amount of information provided by negative feedback during a paired-associate learning task influences feedback-related processing in the caudate nucleus. To do this, we manipulated the number of response options: With two options, positive and negative feedback provide equal amounts of information, whereas with four options, positive feedback provides more information than does negative feedback. We found that positive and negative feedback activated the caudate similarly when there were two response options. With four options, the caudate's response to negative feedback was reduced. A secondary goal was to investigate the link between brain-based measures of feedback-related processing and behavioral indices of learning. Analysis of the posttest measures showed that trials with positive feedback were associated with higher posttest confidence ratings. Additionally, when positive feedback was delivered, caudate activity was greater for trials with high than with low posttest confidence. This experiment demonstrated the context sensitivity of feedback processing and provided evidence that feedback processing in the striatum can contribute to the strengthening of the representations available within declarative memory.

Fig. 1

Experimental Design. Each trial, a target word was presented, along with options for possible word matches, labeled as in a multiple choice test. After a 6-s response period, the display was replaced with a 1-s feedback display of 3 green √s, indicating a correct response, 3 red Xs, indicating an incorrect response, or 3 white hypens, indicating that no response was made. After a 13-s delay, with a screen showing a fixation cross, the next trial began

Fig. 2

Behavioral Results from the Immediate Post-test. Mean confidence scores (normalized to the subject mean) were higher for accurate trials than inaccurate trials and higher for trials for which participants received positive feedback rather than negative feedback during the scan. For accurate trials, the latter effect was more pronounced for the 4-choice condition than the 2-choice condition

Fig. 3

Caudate Activation Across Conditions. a) The left caudate shows a feedback type by time interaction in the 4-choice condition (p < 0.001; contiguity threshold of 41 voxels). The image is left-right reversed. The green crosshair marked the center of the a prioi ROI used for the analyses and the graph in Part b. b) Mean intensity of the BOLD response during the trial outcome phase in the left caudate, using a sphere centered on a priori Talairach coordinates of (-12, 8, 12; cf. Zink et al., 2003). The signal is significantly greater following positive feedback than negative feedback in the 4-choice condition but not the 2-choice condition, and the signal is significantly greater for negative feedback in the 2-choice condition than in the 4-choice condition

Fig. 4

Left Prefrontal Cortex Activation Across Conditions. a) The left PFC (circled) shows a Feedback Type by Trial Type by Time interaction (p < 0.001; contiguity threshold of 41 voxels). The image is left-right reversed. b) Mean intensity of the BOLD response during the trial outcome phase in the left prefrontal cortex. There is a significant interaction of Trial Type and Feedback Type, with a greater signal following positive feedback than negative feedback in the 4-choice condition but not the 2-choice condition. The signal is also significantly greater for negative feedback in the 2-choice condition than in the 4-choice condition. The plot was constructed using data from the entire left PFC cluster identified in our whole-brain analysis