Dysconnectivity of the agency network in schizophrenia: A functional magnetic resonance imaging study

Akihiro Koreki, Takaki Maeda, Tsukasa Okimura, Yuuri 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

Research output: Contribution to journalArticle

Abstract

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.

Original languageEnglish
Article number171
JournalFrontiers in Psychiatry
Volume10
Issue numberAPR
DOIs
Publication statusPublished - 2019 Jan 1

Fingerprint

Parietal Lobe
Schizophrenia
Magnetic Resonance Imaging
Seeds
Learning
Caudate Nucleus

Keywords

  • Caudate
  • Functional connectivity
  • Imaging
  • Inferior parietal lobule
  • Insula
  • Schizophrenia
  • Self-disturbance
  • Sense of agency

ASJC Scopus subject areas

  • Psychiatry and Mental health

Cite this

Dysconnectivity of the agency network in schizophrenia : A functional magnetic resonance imaging study. / Koreki, Akihiro; Maeda, Takaki; Okimura, Tsukasa; Terasawa, Yuuri; Kikuchi, Toshiaki; Umeda, Satoshi; Nishikata, Shiro; Yagihashi, Tatsuhiko; Kasahara, Mari; Nagai, Chiyoko; Moriyama, Yasushi; Den, Ryosuke; Watanabe, Tamotsu; Kikumoto, Hirotsugu; Kato, Motoichiro; Mimura, Masaru.

In: Frontiers in Psychiatry, Vol. 10, No. APR, 171, 01.01.2019.

Research output: Contribution to journalArticle

Koreki, A, Maeda, T, Okimura, T, Terasawa, Y, Kikuchi, T, Umeda, S, Nishikata, S, Yagihashi, T, Kasahara, M, Nagai, C, Moriyama, Y, Den, R, Watanabe, T, Kikumoto, H, Kato, M & Mimura, M 2019, 'Dysconnectivity of the agency network in schizophrenia: A functional magnetic resonance imaging study', Frontiers in Psychiatry, vol. 10, no. APR, 171. https://doi.org/10.3389/fpsyt.2019.00171
Koreki, Akihiro ; Maeda, Takaki ; Okimura, Tsukasa ; Terasawa, Yuuri ; Kikuchi, Toshiaki ; Umeda, Satoshi ; Nishikata, Shiro ; Yagihashi, Tatsuhiko ; Kasahara, Mari ; Nagai, Chiyoko ; Moriyama, Yasushi ; Den, Ryosuke ; Watanabe, Tamotsu ; Kikumoto, Hirotsugu ; Kato, Motoichiro ; Mimura, Masaru. / Dysconnectivity of the agency network in schizophrenia : A functional magnetic resonance imaging study. In: Frontiers in Psychiatry. 2019 ; Vol. 10, No. APR.
@article{bfcb18f05c9a46da979c85316f0cbd7b,
title = "Dysconnectivity of the agency network in schizophrenia: A functional magnetic resonance imaging study",
abstract = "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.",
keywords = "Caudate, Functional connectivity, Imaging, Inferior parietal lobule, Insula, Schizophrenia, Self-disturbance, Sense of agency",
author = "Akihiro Koreki and Takaki Maeda and Tsukasa Okimura and Yuuri Terasawa and Toshiaki Kikuchi and Satoshi Umeda and Shiro Nishikata and Tatsuhiko Yagihashi and Mari Kasahara and Chiyoko Nagai and Yasushi Moriyama and Ryosuke Den and Tamotsu Watanabe and Hirotsugu Kikumoto and Motoichiro Kato and Masaru Mimura",
year = "2019",
month = "1",
day = "1",
doi = "10.3389/fpsyt.2019.00171",
language = "English",
volume = "10",
journal = "Frontiers in Psychiatry",
issn = "1664-0640",
publisher = "Frontiers Research Foundation",
number = "APR",

}

TY - JOUR

T1 - Dysconnectivity of the agency network in schizophrenia

T2 - A functional magnetic resonance imaging study

AU - Koreki, Akihiro

AU - Maeda, Takaki

AU - Okimura, Tsukasa

AU - Terasawa, Yuuri

AU - Kikuchi, Toshiaki

AU - Umeda, Satoshi

AU - Nishikata, Shiro

AU - Yagihashi, Tatsuhiko

AU - Kasahara, Mari

AU - Nagai, Chiyoko

AU - Moriyama, Yasushi

AU - Den, Ryosuke

AU - Watanabe, Tamotsu

AU - Kikumoto, Hirotsugu

AU - Kato, Motoichiro

AU - Mimura, Masaru

PY - 2019/1/1

Y1 - 2019/1/1

N2 - 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.

AB - 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.

KW - Caudate

KW - Functional connectivity

KW - Imaging

KW - Inferior parietal lobule

KW - Insula

KW - Schizophrenia

KW - Self-disturbance

KW - Sense of agency

UR - http://www.scopus.com/inward/record.url?scp=85067988957&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85067988957&partnerID=8YFLogxK

U2 - 10.3389/fpsyt.2019.00171

DO - 10.3389/fpsyt.2019.00171

M3 - Article

AN - SCOPUS:85067988957

VL - 10

JO - Frontiers in Psychiatry

JF - Frontiers in Psychiatry

SN - 1664-0640

IS - APR

M1 - 171

ER -