Abstract
Recent evidence suggests that the aberrant signaling of salience is associated with psychotic illness. Salience, however, can take many forms in task environments. For example, salience may refer to any of the following: (1) the valence of an outcome, (2) outcomes that are unexpected, called reward prediction errors (PEs), or (3) cues associated with uncertain outcomes. Here, we measure brain responses to different forms of salience in the context of a passive PE-signaling task, testing whether patients with schizophrenia (SZ) showed aberrant signaling of particular types of salience. We acquired event-related MRI data from 29 SZ patients and 23 controls during the performance of a passive outcome prediction task. Across groups, we found that the anterior insula and posterior parietal cortices were activated to multiple different types of salience, including PE magnitude and heightened levels of uncertainty. However, BOLD activation to salient events was not significantly different between patients and controls in many regions, including the insula, posterior parietal cortices, and default mode network nodes. Such results suggest that deficiencies in salience processing in SZ may not result from an impaired ability to signal salience per se, but instead the ability to use such signals to guide future actions. Notably, no between-group differences were observed in BOLD signal changes associated with PE-signaling in the striatum. However, positive symptom severity was found to significantly correlate with the magnitudes of salience contrasts in default mode network nodes. Our results suggest that, in an observational environment, SZ patients may show an intact ability to activate striatal and cortical regions to rewarding and non-rewarding salient events. Furthermore, reduced deactivation of a hypothesized default mode network node for SZ participants with high levels of positive symptoms, following salient events, point to abnormalities in interactions of the salience network with other brain networks, and their potential importance to positive symptoms.
Highlights
Among the 28 patients and 23 controls remaining, we examined 2 aspects of behavior, in order to ascertain if participants had acquired the probabilistic contingencies: their within-trial predictions of outcomes, and their between-run estimations of the reinforcement probability associated with each card
B, both groups showed learning of reward probabilities and sensitivity to contingencies associated with particular cues. Participants modulated their trial-wise predictions of winning, given the reward probabilities associated with particular cues, and gave appropriate estimates of the reward probabilities for particular cues when asked between runs
[F(3,35) = 2.130, p = 0.100], and no main effect of GROUP [F(1,37) = 0.423, p = 0.519]. Both the reduced and full samples showed robust effects of CUE; the small effects of GROUP and GROUP × CUE interactions described above were not found in the reduced sample (See Supplementary Materials Figure S1 for description of behavioral performance in the reduced sample)
Summary
Motivated by the dopamine (DA) hypothesis of schizophrenia (SZ) and more recent formulations arguing that psychosis may emerge from faulty causal learning [1], brought on by frequent instances of aberrant salience signaling [2,3], there has been a tremendous increase in studies of DA and reward system signaling, associated with learning in SZ. Dopamine cells have been shown to play a critical role in feedback-driven learning, by signaling both the expectation of rewards and mismatches between expectations and outcomes, called prediction errors (PEs; [4]). Functional imaging studies in human subjects have identified responses in the striatum that signals the valence of reward PEs [6,7,8]
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