Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging

Abstract

Event-related functional magnetic resonance imaging was used to measure blood oxygenation level-dependent responses in 13 young healthy human volunteers during performance of a probabilistic reversal-learning task. The task allowed the separate investigation of the relearning of stimulus-reward associations and the reception of negative feedback. Significant signal change in the right ventrolateral prefrontal cortex was demonstrated on trials when subjects stopped responding to the previously relevant stimulus and shifted responding to the newly relevant stimulus. Significant signal change in the region of the ventral striatum was also observed on such reversal errors, from a region of interest analysis. The ventrolateral prefrontal cortex and ventral striatum were not significantly activated by the other, preceding reversal errors, or when subjects received negative feedback for correct responses. Moreover, the response on the final reversal error, before shifting, was not modulated by the number of preceding reversal errors, indicating that error-related activity does not simply accumulate in this network. The signal change in this ventral frontostriatal circuit is therefore associated with reversal learning and is uncontaminated by negative feedback. Overall, these data concur with findings in rodents and nonhuman primates of reversal-learning deficits after damage to ventral frontostriatal circuitry, and also support recent clinical findings using this task.

Fig. 1.

The probabilistic reversal-learning task. An example of several consecutive trials in the probabilistic reversal-learning task is shown (running from bottom totop). On each trial, subjects are presented with two abstract visual patterns. Using trial-and-error feedback, subjects must discover which of the two patterns is correct (here indicated by asmall arrowhead on top of the pattern to improve legibility). Feedback (a green smiley face or red sad face) is presented as soon as the subject has chosen one of the patterns by a left or right button press.

Fig. 2.

Signal changes in ventral frontostriatal circuitry during the critical final reversal errors. Signal changes in the bilateral ventrolateral PFC and ventral striatum, identified by the contrast, final reversal errors minus correct responses, are superimposed on the MNI template brain (individual brain considered most typical of the 305 brains used to define the MNI standard). See Results and Table 1 for statistical values. In all three axial slices, the z-coordinate represents the position of the slice relative to the anterior commissure–posterior commissure axis (dorsal, positive).