Atypical spatial frequency dependence of visual metacognition among schizophrenia patients

Abstract

Although altered early stages of visual processing have been reported among schizophrenia patients, how such atypical visual processing may affect higher-level cognition remains largely unknown. Here we tested the hypothesis that metacognitive performance may be atypically modulated by spatial frequency (SF) of visual stimuli among individuals with schizophrenia, given their altered magnocellular function. To study the effect of SF on metacognitive performance, we asked patients and controls to perform a visual detection task on gratings with different SFs and report confidence, and analyzed the data using the signal detection theoretic measure meta-d'. Control subjects showed better metacognitive performance after yes- (stimulus presence) than after no- (stimulus absence) responses ('yes-response advantage') for high SF (HSF) stimuli but not for low SF (LSF) stimuli. The patients, to the contrary, showed a 'yes-response advantage' not only for HSF but also for LSF stimuli, indicating atypical SF dependency of metacognition. An fMRI experiment using the same task revealed that the dorsolateral prefrontal cortex (DLPFC), known to be crucial for metacognition, shows activity mirroring the behavioral results: decoding accuracy of perceptual confidence in DLPFC was significantly higher for HSF than for LSF stimuli in controls, whereas this decoding accuracy was independent of SF in patients. Additionally, the functional connectivity of DLPFC with parietal and visual areas was modulated by SF and response type (yes/no) in a different manner between controls and patients. While individuals without schizophrenia may flexibly adapt metacognitive computations across SF ranges, patients may employ a different mechanism that is independent of SF. Because visual stimuli of low SF have been linked to predictive top-down processing, this may reflect atypical functioning in these processes in schizophrenia.

Keywords: Dorsolateral prefrontal cortex; Metacognition; Multivoxel decoding; Schizophrenia; Spatial frequency; fMRI.

Fig. 1

Schematics of the detection task. A. A trial sequence of the task. On half of the trials, a grating target briefly emerged and faded within a background patch containing dynamic white noise refreshed at 60 Hz (similar to TV static). Participants were asked to make a perceptual response indicating whether a grating was present (“yes” response) or absent (“no” response), and then to rate their confidence in their perceptual response with a four-responses scale. B. Two levels of spatial frequency of a grating target. A grating with high and low spatial frequency (2.6 cpd and 0.4 cpd, respectively) levels were used as a target in two separate sessions of Experiments 1 and 2. Grating phase was randomized across trials. ITI: inter-trial-interval. cpd: cycle per degree (in visual angle).

Fig. 2

Differences in Meta-d′ between schizophrenia patients and controls as a function of spatial frequency (HSF/LSF) and that of response type (yes/no) in Experiment 1. A. Controls showed advantageous metacognitive performance with yes- relative to no-responses only during the HSF target detection task but not during the LSF target detection task, whereas patients showed advantageous performance with yes-responses irrespective of the target spatial frequency. There was a significant spatial frequency × response type × group interaction (F(1, 33) = 4.60, p = .039). The results of post-hoc t-tests are shown. B. Same result from the analyses depicted in A. Differences in meta-d′/d′ between yes- and no-responses are shown for demonstrative purposes. Here, larger values indicate more advantageous metacognitive performance with yes- than no-responses. Error bars indicate standard error of the mean. ** p < .01, * < p < .05.

Fig. 3

There was a significant interaction between group and spatial frequency in the decoding accuracy of the trial-wise confidence level (high/low) from the multivariate activation patterns in the DLPFC ROI (shown in Fig. 4). Only among controls, decoding accuracy was significantly higher with HSF than LSF stimulus judgement, whereas it was statistically similar between the spatial frequency levels among patients. * p < .05.

Fig. 4

The results of a whole-brain analysis examining where in the brain showed altered functional connectivity with the DLPFC during confidence rating as a function of spatial frequency, response type, and group. Here, the degree of functional connectivity was estimated with a general form of context-dependent psychophysiological interaction (gPPI) (McLaren et al., 2012). The functional connectivity between the DLPFC and bilateral clusters in parietal and visual cortices were significantly modulated as a function of the interaction between spatial frequency, response type, and group (p < .01, corrected with cluster-size thresholding (Forman et al., 1995, Goebel et al., 2006)). Here, DLPFC ROIs were functionally defined from a group GLM. ROIs include the voxels that showed significantly larger activity during the confidence rating period relative to fixation in a group GLM (p < .01, Bonferroni corrected). a: anterior, r: right.