Atypical spatial frequency dependence of visual metacognition among schizophrenia patients

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 frequ...

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Main Authors: Ai Koizumi, Tomoki Hori, Brian Maniscalco, Makoto Hayase, Ryou Mishima, Takahiko Kawashima, Jun Miyata, Toshihiko Aso, Hakwan Lau, Hidehiko Takahashi, Kaoru Amano
Format: Article
Language:English
Published: Elsevier 2020-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158220301339
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spelling doaj-fd786f3118c24b97afa5edfe9e2224b62020-11-25T04:01:39ZengElsevierNeuroImage: Clinical2213-15822020-01-0127102296Atypical spatial frequency dependence of visual metacognition among schizophrenia patientsAi Koizumi0Tomoki Hori1Brian Maniscalco2Makoto Hayase3Ryou Mishima4Takahiko Kawashima5Jun Miyata6Toshihiko Aso7Hakwan Lau8Hidehiko Takahashi9Kaoru Amano10Center for Information and Neural Networks (CiNet), NICT, Japan; Sony Computer Science Laboratories, Inc., Japan; Graduate School of Media and Governance, Keio University, Japan; Japan Science and Technology Agency (JST), PRESTO, Japan; Corresponding authors.Department of Psychiatry, Kyoto University Graduate School of Medicine, JapanDepartment of Psychology, Columbia University, United States; Department of Cognitive Sciences, UC Irvine, United StatesDepartment of Psychiatry, Kyoto University Graduate School of Medicine, JapanDepartment of Psychiatry, Kyoto University Graduate School of Medicine, JapanDepartment of Psychiatry, Kyoto University Graduate School of Medicine, JapanDepartment of Psychiatry, Kyoto University Graduate School of Medicine, JapanHuman Brain Research Center, Kyoto University Graduate School of Medicine, JapanDepartment of Psychology, UCLA, United States; Brain Research Institute, UCLA, United States; Department of Psychology & State Key Laboratory for Brain and Cognitive Sciences, University of Hong Kong, Hong KongDepartment of Psychiatry, Kyoto University Graduate School of Medicine, Japan; Department of Psychiatry and Behavioral Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Japan; Corresponding authors.Center for Information and Neural Networks (CiNet), NICT, Japan; Japan Science and Technology Agency (JST), PRESTO, JapanAlthough 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.http://www.sciencedirect.com/science/article/pii/S2213158220301339SchizophreniaMetacognitionSpatial frequencyfMRIMultivoxel decodingDorsolateral prefrontal cortex
collection DOAJ
language English
format Article
sources DOAJ
author Ai Koizumi
Tomoki Hori
Brian Maniscalco
Makoto Hayase
Ryou Mishima
Takahiko Kawashima
Jun Miyata
Toshihiko Aso
Hakwan Lau
Hidehiko Takahashi
Kaoru Amano
spellingShingle Ai Koizumi
Tomoki Hori
Brian Maniscalco
Makoto Hayase
Ryou Mishima
Takahiko Kawashima
Jun Miyata
Toshihiko Aso
Hakwan Lau
Hidehiko Takahashi
Kaoru Amano
Atypical spatial frequency dependence of visual metacognition among schizophrenia patients
NeuroImage: Clinical
Schizophrenia
Metacognition
Spatial frequency
fMRI
Multivoxel decoding
Dorsolateral prefrontal cortex
author_facet Ai Koizumi
Tomoki Hori
Brian Maniscalco
Makoto Hayase
Ryou Mishima
Takahiko Kawashima
Jun Miyata
Toshihiko Aso
Hakwan Lau
Hidehiko Takahashi
Kaoru Amano
author_sort Ai Koizumi
title Atypical spatial frequency dependence of visual metacognition among schizophrenia patients
title_short Atypical spatial frequency dependence of visual metacognition among schizophrenia patients
title_full Atypical spatial frequency dependence of visual metacognition among schizophrenia patients
title_fullStr Atypical spatial frequency dependence of visual metacognition among schizophrenia patients
title_full_unstemmed Atypical spatial frequency dependence of visual metacognition among schizophrenia patients
title_sort atypical spatial frequency dependence of visual metacognition among schizophrenia patients
publisher Elsevier
series NeuroImage: Clinical
issn 2213-1582
publishDate 2020-01-01
description 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.
topic Schizophrenia
Metacognition
Spatial frequency
fMRI
Multivoxel decoding
Dorsolateral prefrontal cortex
url http://www.sciencedirect.com/science/article/pii/S2213158220301339
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