Cortical white matter microstructural alterations underlying the impaired gamma-band auditory steady-state response in schizophrenia

Abstract The gamma-band auditory steady-state response (ASSR), primarily generated from the auditory cortex, has received substantial attention as a potential brain marker indicating the pathophysiology of schizophrenia. Previous studies have shown reduced gamma-band ASSR in patients with schizophre...

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Main Authors: Daisuke Koshiyama, Ryoichi Nishimura, Kaori Usui, Mao Fujioka, Mariko Tada, Kenji Kirihara, Tsuyoshi Araki, Shintaro Kawakami, Naohiro Okada, Shinsuke Koike, Hidenori Yamasue, Osamu Abe, Kiyoto Kasai
Format: Article
Language:English
Published: Nature Portfolio 2024-03-01
Series:Schizophrenia
Online Access:https://doi.org/10.1038/s41537-024-00454-4
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author Daisuke Koshiyama
Ryoichi Nishimura
Kaori Usui
Mao Fujioka
Mariko Tada
Kenji Kirihara
Tsuyoshi Araki
Shintaro Kawakami
Naohiro Okada
Shinsuke Koike
Hidenori Yamasue
Osamu Abe
Kiyoto Kasai
author_facet Daisuke Koshiyama
Ryoichi Nishimura
Kaori Usui
Mao Fujioka
Mariko Tada
Kenji Kirihara
Tsuyoshi Araki
Shintaro Kawakami
Naohiro Okada
Shinsuke Koike
Hidenori Yamasue
Osamu Abe
Kiyoto Kasai
author_sort Daisuke Koshiyama
collection DOAJ
description Abstract The gamma-band auditory steady-state response (ASSR), primarily generated from the auditory cortex, has received substantial attention as a potential brain marker indicating the pathophysiology of schizophrenia. Previous studies have shown reduced gamma-band ASSR in patients with schizophrenia and demonstrated correlations with impaired neurocognition and psychosocial functioning. Recent studies in clinical and healthy populations have suggested that the neural substrates of reduced gamma-band ASSR may be distributed throughout the cortices surrounding the auditory cortex, especially in the right hemisphere. This study aimed to investigate associations between the gamma-band ASSR and white matter alterations in the bundles broadly connecting the right frontal, parietal and occipital cortices to clarify the networks underlying reduced gamma-band ASSR in patients with schizophrenia. We measured the 40 Hz ASSR using electroencephalography and diffusion tensor imaging in 42 patients with schizophrenia and 22 healthy comparison subjects. The results showed that the gamma-band ASSR was positively correlated with fractional anisotropy (an index of white matter integrity) in the regions connecting the right frontal, parietal and occipital cortices in healthy subjects (β = 0.41, corrected p = 0.075, uncorrected p = 0.038) but not in patients with schizophrenia (β = 0.17, corrected p = 0.46, uncorrected p = 0.23). These findings support our hypothesis that the generation of gamma-band ASSR is supported by white matter bundles that broadly connect the cortices and that these relationships may be disrupted in schizophrenia. Our study may help characterize and interpret reduced gamma-band ASSR as a useful brain marker of schizophrenia.
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spelling doaj.art-e037573a0f6646489ea891f6e38111362024-03-17T12:29:13ZengNature PortfolioSchizophrenia2754-69932024-03-011011810.1038/s41537-024-00454-4Cortical white matter microstructural alterations underlying the impaired gamma-band auditory steady-state response in schizophreniaDaisuke Koshiyama0Ryoichi Nishimura1Kaori Usui2Mao Fujioka3Mariko Tada4Kenji Kirihara5Tsuyoshi Araki6Shintaro Kawakami7Naohiro Okada8Shinsuke Koike9Hidenori Yamasue10Osamu Abe11Kiyoto Kasai12Department of Neuropsychiatry, Graduate School of Medicine, The University of TokyoDepartment of Neuropsychiatry, Graduate School of Medicine, The University of TokyoDepartment of Neuropsychiatry, Graduate School of Medicine, The University of TokyoDepartment of Neuropsychiatry, Graduate School of Medicine, The University of TokyoDepartment of Neuropsychiatry, Graduate School of Medicine, The University of TokyoDepartment of Neuropsychiatry, Graduate School of Medicine, The University of TokyoDepartment of Neuropsychiatry, Graduate School of Medicine, The University of TokyoDepartment of Neuropsychiatry, Graduate School of Medicine, The University of TokyoDepartment of Neuropsychiatry, Graduate School of Medicine, The University of TokyoDepartment of Neuropsychiatry, Graduate School of Medicine, The University of TokyoDepartment of Psychiatry, Hamamatsu University School of MedicineDepartment of Radiology, Graduate School of Medicine, The University of TokyoDepartment of Neuropsychiatry, Graduate School of Medicine, The University of TokyoAbstract The gamma-band auditory steady-state response (ASSR), primarily generated from the auditory cortex, has received substantial attention as a potential brain marker indicating the pathophysiology of schizophrenia. Previous studies have shown reduced gamma-band ASSR in patients with schizophrenia and demonstrated correlations with impaired neurocognition and psychosocial functioning. Recent studies in clinical and healthy populations have suggested that the neural substrates of reduced gamma-band ASSR may be distributed throughout the cortices surrounding the auditory cortex, especially in the right hemisphere. This study aimed to investigate associations between the gamma-band ASSR and white matter alterations in the bundles broadly connecting the right frontal, parietal and occipital cortices to clarify the networks underlying reduced gamma-band ASSR in patients with schizophrenia. We measured the 40 Hz ASSR using electroencephalography and diffusion tensor imaging in 42 patients with schizophrenia and 22 healthy comparison subjects. The results showed that the gamma-band ASSR was positively correlated with fractional anisotropy (an index of white matter integrity) in the regions connecting the right frontal, parietal and occipital cortices in healthy subjects (β = 0.41, corrected p = 0.075, uncorrected p = 0.038) but not in patients with schizophrenia (β = 0.17, corrected p = 0.46, uncorrected p = 0.23). These findings support our hypothesis that the generation of gamma-band ASSR is supported by white matter bundles that broadly connect the cortices and that these relationships may be disrupted in schizophrenia. Our study may help characterize and interpret reduced gamma-band ASSR as a useful brain marker of schizophrenia.https://doi.org/10.1038/s41537-024-00454-4
spellingShingle Daisuke Koshiyama
Ryoichi Nishimura
Kaori Usui
Mao Fujioka
Mariko Tada
Kenji Kirihara
Tsuyoshi Araki
Shintaro Kawakami
Naohiro Okada
Shinsuke Koike
Hidenori Yamasue
Osamu Abe
Kiyoto Kasai
Cortical white matter microstructural alterations underlying the impaired gamma-band auditory steady-state response in schizophrenia
Schizophrenia
title Cortical white matter microstructural alterations underlying the impaired gamma-band auditory steady-state response in schizophrenia
title_full Cortical white matter microstructural alterations underlying the impaired gamma-band auditory steady-state response in schizophrenia
title_fullStr Cortical white matter microstructural alterations underlying the impaired gamma-band auditory steady-state response in schizophrenia
title_full_unstemmed Cortical white matter microstructural alterations underlying the impaired gamma-band auditory steady-state response in schizophrenia
title_short Cortical white matter microstructural alterations underlying the impaired gamma-band auditory steady-state response in schizophrenia
title_sort cortical white matter microstructural alterations underlying the impaired gamma band auditory steady state response in schizophrenia
url https://doi.org/10.1038/s41537-024-00454-4
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