Altered sense of agency in schizophrenia: the aberrant effect of cardiac interoceptive signals
BackgroundSchizophrenia (SZ) is characterized by abnormalities in self-representation, including a disturbed sense of agency (SoA). The continuous processing of sensory information concerning the internal state of the body (interoception) is argued to be fundamental to neural representations of the...
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Frontiers Media S.A.
2024-09-01
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| Series: | Frontiers in Psychiatry |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpsyt.2024.1441585/full |
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| author | Akihiro Koreki Akihiro Koreki Akihiro Koreki Yuri Terasawa Atsuo Nuruki Hiroki Oi Hugo Critchley Mahinda Yogarajah Mitsumoto Onaya |
| author_facet | Akihiro Koreki Akihiro Koreki Akihiro Koreki Yuri Terasawa Atsuo Nuruki Hiroki Oi Hugo Critchley Mahinda Yogarajah Mitsumoto Onaya |
| author_sort | Akihiro Koreki |
| collection | DOAJ |
| description | BackgroundSchizophrenia (SZ) is characterized by abnormalities in self-representation, including a disturbed sense of agency (SoA). The continuous processing of sensory information concerning the internal state of the body (interoception) is argued to be fundamental to neural representations of the self. We, therefore, tested if aberrant interoception underpins disturbances in SoA in SZ, focusing on cardiac interoceptive signaling.MethodsForty-two SZ and 29 non-clinical participants (healthy controls; HC) performed an intentional binding task to measure SoA during concurrent heartbeat recording. The effect of cardiac interoceptive signals on SoA was measured by the difference in intentional binding effect during systole and diastole. This measure was standardized based on the overall intentional binding effect to control for non-cardiac factors, and then compared between SZ and HC.ResultsOur study revealed a significant difference between SZ and HC groups, with opposite effects of cardiac systole on SoA. Specifically, cardiac systole disrupted SoA in SZ, contrasting with the enhanced SoA in HC. Across the SZ group, the extent to which SoA was disrupted by cardiac systole correlated significantly with a clinical proxy for symptom instability, namely the number of hospital admissions for hallucinations and delusions. Furthermore, the disruption was particularly observed in patients with severe hallucinations.ConclusionsThis study revealed a disturbance in the impact of cardiac interoceptive signals on an implicit index of SoA in schizophrenia. This supports the notion that pathophysiological disruption of the central integration of interoceptive information increases vulnerability to disturbances in self-representation and the associated expression of schizophrenic symptoms. |
| format | Article |
| id | doaj-art-dc07da98cc944852be189d59bfe8726c |
| institution | OA Journals |
| issn | 1664-0640 |
| language | English |
| publishDate | 2024-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Psychiatry |
| spelling | doaj-art-dc07da98cc944852be189d59bfe8726c2025-08-20T01:55:08ZengFrontiers Media S.A.Frontiers in Psychiatry1664-06402024-09-011510.3389/fpsyt.2024.14415851441585Altered sense of agency in schizophrenia: the aberrant effect of cardiac interoceptive signalsAkihiro Koreki0Akihiro Koreki1Akihiro Koreki2Yuri Terasawa3Atsuo Nuruki4Hiroki Oi5Hugo Critchley6Mahinda Yogarajah7Mitsumoto Onaya8Department of Psychiatry, NHO Shimofusa Psychiatric Medical Center, Chiba, JapanDepartment of Psychiatry, NHO Chibahigashi Hospital, Chiba, JapanDepartment of Neuropsychiatry, Keio University School of Medicine, Tokyo, JapanDepartment of Psychology, Keio University, Tokyo, JapanCenter for General Education, Institute for Comprehensive Education, Kagoshima University, Kagoshima, JapanDepartment of Neuropsychiatry, Keio University School of Medicine, Tokyo, JapanDepartment of Clinical Neuroscience, Brighton and Sussex Medical School, Sussex University, Brighton, United KingdomDepartment of Clinical & Experimental Epilepsy, University College London (UCL) Queen Square Institute of Neurology, London, United KingdomDepartment of Psychiatry, NHO Shimofusa Psychiatric Medical Center, Chiba, JapanBackgroundSchizophrenia (SZ) is characterized by abnormalities in self-representation, including a disturbed sense of agency (SoA). The continuous processing of sensory information concerning the internal state of the body (interoception) is argued to be fundamental to neural representations of the self. We, therefore, tested if aberrant interoception underpins disturbances in SoA in SZ, focusing on cardiac interoceptive signaling.MethodsForty-two SZ and 29 non-clinical participants (healthy controls; HC) performed an intentional binding task to measure SoA during concurrent heartbeat recording. The effect of cardiac interoceptive signals on SoA was measured by the difference in intentional binding effect during systole and diastole. This measure was standardized based on the overall intentional binding effect to control for non-cardiac factors, and then compared between SZ and HC.ResultsOur study revealed a significant difference between SZ and HC groups, with opposite effects of cardiac systole on SoA. Specifically, cardiac systole disrupted SoA in SZ, contrasting with the enhanced SoA in HC. Across the SZ group, the extent to which SoA was disrupted by cardiac systole correlated significantly with a clinical proxy for symptom instability, namely the number of hospital admissions for hallucinations and delusions. Furthermore, the disruption was particularly observed in patients with severe hallucinations.ConclusionsThis study revealed a disturbance in the impact of cardiac interoceptive signals on an implicit index of SoA in schizophrenia. This supports the notion that pathophysiological disruption of the central integration of interoceptive information increases vulnerability to disturbances in self-representation and the associated expression of schizophrenic symptoms.https://www.frontiersin.org/articles/10.3389/fpsyt.2024.1441585/fullbraininteroceptionheartschizophreniasense of agencyself |
| spellingShingle | Akihiro Koreki Akihiro Koreki Akihiro Koreki Yuri Terasawa Atsuo Nuruki Hiroki Oi Hugo Critchley Mahinda Yogarajah Mitsumoto Onaya Altered sense of agency in schizophrenia: the aberrant effect of cardiac interoceptive signals Frontiers in Psychiatry brain interoception heart schizophrenia sense of agency self |
| title | Altered sense of agency in schizophrenia: the aberrant effect of cardiac interoceptive signals |
| title_full | Altered sense of agency in schizophrenia: the aberrant effect of cardiac interoceptive signals |
| title_fullStr | Altered sense of agency in schizophrenia: the aberrant effect of cardiac interoceptive signals |
| title_full_unstemmed | Altered sense of agency in schizophrenia: the aberrant effect of cardiac interoceptive signals |
| title_short | Altered sense of agency in schizophrenia: the aberrant effect of cardiac interoceptive signals |
| title_sort | altered sense of agency in schizophrenia the aberrant effect of cardiac interoceptive signals |
| topic | brain interoception heart schizophrenia sense of agency self |
| url | https://www.frontiersin.org/articles/10.3389/fpsyt.2024.1441585/full |
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