Dysconnectivity of the Agency Network in Schizophrenia: A Functional Magnetic Resonance Imaging Study

Background: Self-disturbances in schizophrenia have recently been explained by an abnormality in the sense of agency (SoA). The cerebral structures of SoA in healthy people are considered to mainly include the insula and inferior parietal lobule. In contrast, the functional lesion of aberrant SoA in...

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Main Authors: Akihiro Koreki, Takaki Maeda, Tsukasa Okimura, Yuri Terasawa, Toshiaki Kikuchi, Satoshi Umeda, Shiro Nishikata, Tatsuhiko Yagihashi, Mari Kasahara, Chiyoko Nagai, Yasushi Moriyama, Ryosuke Den, Tamotsu Watanabe, Hirotsugu Kikumoto, Motoichiro Kato, Masaru Mimura
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-04-01
Series:Frontiers in Psychiatry
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpsyt.2019.00171/full
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author Akihiro Koreki
Akihiro Koreki
Akihiro Koreki
Takaki Maeda
Takaki Maeda
Tsukasa Okimura
Tsukasa Okimura
Yuri Terasawa
Yuri Terasawa
Toshiaki Kikuchi
Satoshi Umeda
Satoshi Umeda
Shiro Nishikata
Shiro Nishikata
Tatsuhiko Yagihashi
Tatsuhiko Yagihashi
Mari Kasahara
Mari Kasahara
Chiyoko Nagai
Chiyoko Nagai
Yasushi Moriyama
Yasushi Moriyama
Ryosuke Den
Ryosuke Den
Tamotsu Watanabe
Tamotsu Watanabe
Hirotsugu Kikumoto
Motoichiro Kato
Motoichiro Kato
Masaru Mimura
spellingShingle Akihiro Koreki
Akihiro Koreki
Akihiro Koreki
Takaki Maeda
Takaki Maeda
Tsukasa Okimura
Tsukasa Okimura
Yuri Terasawa
Yuri Terasawa
Toshiaki Kikuchi
Satoshi Umeda
Satoshi Umeda
Shiro Nishikata
Shiro Nishikata
Tatsuhiko Yagihashi
Tatsuhiko Yagihashi
Mari Kasahara
Mari Kasahara
Chiyoko Nagai
Chiyoko Nagai
Yasushi Moriyama
Yasushi Moriyama
Ryosuke Den
Ryosuke Den
Tamotsu Watanabe
Tamotsu Watanabe
Hirotsugu Kikumoto
Motoichiro Kato
Motoichiro Kato
Masaru Mimura
Dysconnectivity of the Agency Network in Schizophrenia: A Functional Magnetic Resonance Imaging Study
Frontiers in Psychiatry
schizophrenia
sense of agency
self-disturbance
functional connectivity
imaging
caudate
author_facet Akihiro Koreki
Akihiro Koreki
Akihiro Koreki
Takaki Maeda
Takaki Maeda
Tsukasa Okimura
Tsukasa Okimura
Yuri Terasawa
Yuri Terasawa
Toshiaki Kikuchi
Satoshi Umeda
Satoshi Umeda
Shiro Nishikata
Shiro Nishikata
Tatsuhiko Yagihashi
Tatsuhiko Yagihashi
Mari Kasahara
Mari Kasahara
Chiyoko Nagai
Chiyoko Nagai
Yasushi Moriyama
Yasushi Moriyama
Ryosuke Den
Ryosuke Den
Tamotsu Watanabe
Tamotsu Watanabe
Hirotsugu Kikumoto
Motoichiro Kato
Motoichiro Kato
Masaru Mimura
author_sort Akihiro Koreki
title Dysconnectivity of the Agency Network in Schizophrenia: A Functional Magnetic Resonance Imaging Study
title_short Dysconnectivity of the Agency Network in Schizophrenia: A Functional Magnetic Resonance Imaging Study
title_full Dysconnectivity of the Agency Network in Schizophrenia: A Functional Magnetic Resonance Imaging Study
title_fullStr Dysconnectivity of the Agency Network in Schizophrenia: A Functional Magnetic Resonance Imaging Study
title_full_unstemmed Dysconnectivity of the Agency Network in Schizophrenia: A Functional Magnetic Resonance Imaging Study
title_sort dysconnectivity of the agency network in schizophrenia: a functional magnetic resonance imaging study
publisher Frontiers Media S.A.
series Frontiers in Psychiatry
issn 1664-0640
publishDate 2019-04-01
description Background: Self-disturbances in schizophrenia have recently been explained by an abnormality in the sense of agency (SoA). The cerebral structures of SoA in healthy people are considered to mainly include the insula and inferior parietal lobule. In contrast, the functional lesion of aberrant SoA in schizophrenia is not yet fully understood. Considering the recent explanation of establishing SoA from the standpoint of associative learning, the “agency network” may include not only the insula and inferior parietal lobule but also the striatum. We hypothesized that aberrant SoA in schizophrenia is based on a deficit in the “agency network.”Methods: Functional magnetic resonance imaging data were acquired while patients with schizophrenia (n = 15) and matched controls (n = 15) performed our adaptation method of agency attribution task on a trial-by-trial basis to assess participants' explicit experience of the temporal causal relationship between an action and an external event with temporal biases. Analysis of functional connectivity was done using the right supramarginal gyrus and the right middle frontal gyrus as seed regions.Results: In healthy controls, analyses revealed increased activation of the right inferior parietal lobule (mainly the supramarginal gyrus), right insula, and right middle frontal gyrus as an activation of the agency condition. We defined activated Brodmann areas shown in the agency condition of healthy controls as the seed region for connectivity analysis. The connectivity analysis revealed lower connectivity between the head of the left caudate nucleus and right supramarginal gyrus in the patients compared to healthy controls.Conclusions: This dysconnectivity of the agency network in schizophrenia may lead to self-disturbance through deficits in associative learning of SoA. These findings may explain why pathological function of the striatum in schizophrenia leads to self-disturbance.
topic schizophrenia
sense of agency
self-disturbance
functional connectivity
imaging
caudate
url https://www.frontiersin.org/article/10.3389/fpsyt.2019.00171/full
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spelling doaj-3f1fa57a2d624e7ab15d4c66d2bf2ef32020-11-24T21:59:13ZengFrontiers Media S.A.Frontiers in Psychiatry1664-06402019-04-011010.3389/fpsyt.2019.00171434416Dysconnectivity of the Agency Network in Schizophrenia: A Functional Magnetic Resonance Imaging StudyAkihiro Koreki0Akihiro Koreki1Akihiro Koreki2Takaki Maeda3Takaki Maeda4Tsukasa Okimura5Tsukasa Okimura6Yuri Terasawa7Yuri Terasawa8Toshiaki Kikuchi9Satoshi Umeda10Satoshi Umeda11Shiro Nishikata12Shiro Nishikata13Tatsuhiko Yagihashi14Tatsuhiko Yagihashi15Mari Kasahara16Mari Kasahara17Chiyoko Nagai18Chiyoko Nagai19Yasushi Moriyama20Yasushi Moriyama21Ryosuke Den22Ryosuke Den23Tamotsu Watanabe24Tamotsu Watanabe25Hirotsugu Kikumoto26Motoichiro Kato27Motoichiro Kato28Masaru Mimura29Department of Neuropsychiatry, School of Medicine, Keio University, Tokyo, JapanCenter for Psychiatry and Behavioral Science, Komagino Hospital, Tokyo, JapanDepartment of Neuropsychiatry, National Hospital Organization Shimofusa Psychiatric Medical Center, Chiba, JapanDepartment of Neuropsychiatry, School of Medicine, Keio University, Tokyo, JapanCenter for Psychiatry and Behavioral Science, Komagino Hospital, Tokyo, JapanDepartment of Neuropsychiatry, School of Medicine, Keio University, Tokyo, JapanCenter for Psychiatry and Behavioral Science, Komagino Hospital, Tokyo, JapanCenter for Psychiatry and Behavioral Science, Komagino Hospital, Tokyo, JapanDepartment of Psychology, Keio University, Tokyo, JapanCenter for Psychiatry and Behavioral Science, Komagino Hospital, Tokyo, JapanCenter for Psychiatry and Behavioral Science, Komagino Hospital, Tokyo, JapanDepartment of Psychology, Keio University, Tokyo, JapanCenter for Psychiatry and Behavioral Science, Komagino Hospital, Tokyo, JapanDepartment of Psychiatry, Komagino Hospital, Tokyo, JapanCenter for Psychiatry and Behavioral Science, Komagino Hospital, Tokyo, JapanDepartment of Psychiatry, Komagino Hospital, Tokyo, JapanCenter for Psychiatry and Behavioral Science, Komagino Hospital, Tokyo, JapanDepartment of Psychiatry, Komagino Hospital, Tokyo, JapanCenter for Psychiatry and Behavioral Science, Komagino Hospital, Tokyo, JapanDepartment of Speech-Language Pathology and Audiology, Teikyo Heisei University, Tokyo, JapanCenter for Psychiatry and Behavioral Science, Komagino Hospital, Tokyo, JapanDepartment of Psychiatry, Komagino Hospital, Tokyo, JapanCenter for Psychiatry and Behavioral Science, Komagino Hospital, Tokyo, JapanDepartment of Psychiatry, Komagino Hospital, Tokyo, JapanCenter for Psychiatry and Behavioral Science, Komagino Hospital, Tokyo, JapanDepartment of Psychiatry, Komagino Hospital, Tokyo, JapanDepartment of Psychiatry, Komagino Hospital, Tokyo, JapanDepartment of Neuropsychiatry, School of Medicine, Keio University, Tokyo, JapanCenter for Psychiatry and Behavioral Science, Komagino Hospital, Tokyo, JapanDepartment of Neuropsychiatry, School of Medicine, Keio University, Tokyo, JapanBackground: Self-disturbances in schizophrenia have recently been explained by an abnormality in the sense of agency (SoA). The cerebral structures of SoA in healthy people are considered to mainly include the insula and inferior parietal lobule. In contrast, the functional lesion of aberrant SoA in schizophrenia is not yet fully understood. Considering the recent explanation of establishing SoA from the standpoint of associative learning, the “agency network” may include not only the insula and inferior parietal lobule but also the striatum. We hypothesized that aberrant SoA in schizophrenia is based on a deficit in the “agency network.”Methods: Functional magnetic resonance imaging data were acquired while patients with schizophrenia (n = 15) and matched controls (n = 15) performed our adaptation method of agency attribution task on a trial-by-trial basis to assess participants' explicit experience of the temporal causal relationship between an action and an external event with temporal biases. Analysis of functional connectivity was done using the right supramarginal gyrus and the right middle frontal gyrus as seed regions.Results: In healthy controls, analyses revealed increased activation of the right inferior parietal lobule (mainly the supramarginal gyrus), right insula, and right middle frontal gyrus as an activation of the agency condition. We defined activated Brodmann areas shown in the agency condition of healthy controls as the seed region for connectivity analysis. The connectivity analysis revealed lower connectivity between the head of the left caudate nucleus and right supramarginal gyrus in the patients compared to healthy controls.Conclusions: This dysconnectivity of the agency network in schizophrenia may lead to self-disturbance through deficits in associative learning of SoA. These findings may explain why pathological function of the striatum in schizophrenia leads to self-disturbance.https://www.frontiersin.org/article/10.3389/fpsyt.2019.00171/fullschizophreniasense of agencyself-disturbancefunctional connectivityimagingcaudate