Disambiguating ventral striatum fMRI-related BOLD signal during reward prediction in schizophrenia

Abstract

Reward detection, surprise detection and prediction-error signaling have all been proposed as roles for the ventral striatum (vStr). Previous neuroimaging studies of striatal function in schizophrenia have found attenuated neural responses to reward-related prediction errors; however, as prediction errors represent a discrepancy in mesolimbic neural activity between expected and actual events, it is critical to examine responses to both expected and unexpected rewards (URs) in conjunction with expected and UR omissions in order to clarify the nature of ventral striatal dysfunction in schizophrenia. In the present study, healthy adults and people with schizophrenia were tested with a reward-related prediction-error task during functional magnetic resonance imaging to determine whether schizophrenia is associated with altered neural responses in the vStr to rewards, surprise prediction errors or all three factors. In healthy adults, we found neural responses in the vStr were correlated more specifically with prediction errors than to surprising events or reward stimuli alone. People with schizophrenia did not display the normal differential activation between expected and URs, which was partially due to exaggerated ventral striatal responses to expected rewards (right vStr) but also included blunted responses to unexpected outcomes (left vStr). This finding shows that neural responses, which typically are elicited by surprise, can also occur to well-predicted events in schizophrenia and identifies aberrant activity in the vStr as a key node of dysfunction in the neural circuitry used to differentiate expected and unexpected feedback in schizophrenia.

Figure 1

Three models of possible activation across four conditions of reward (UR: unexpected reward, ER: expected reward, UO: unexpected omission of reward, EO: expected omission of reward). Panel a indicates a main effect of reward; panel b indicates a main effect of surprise; panel c indicates an interaction in which surprise modulates the response to reward in a bidirectional manner.

Figure 2

Examples of card cues and outcomes trial types in prediction task. Four different card stimuli were used (diamonds, triangles, squares and circles) in which one card was trump (diamonds in this example). Money (reward stimulus) was either presented or omitted. Predictions were either correct or incorrect. Top row: expected reward; second row: unexpected reward omission; third row: expected reward omission; fourth row: unexpected reward. Stimulus and feedback duration are provided below.

Figure 3

Regions of significant group differences in prediction-error signals in the ROI among healthy adults and people with schizophrenia. Color bars represent the t-value of the three-way interaction (false-discovery rate P<0.05). Parameter estimates for each condition are shown on the right. (a) In the left vStr, people with schizophrenia displayed a relatively blunted level of BOLD activity during unexpected outcomes (UR and UO conditions). (b) In the right vStr, people with schizophrenia displayed a relatively exaggerated level of BOLD activity during expected outcomes (ER and EO conditions).