Altered brain long-range functional interactions underlying the link between aberrant self-experience and self-other relationship in first-episode schizophrenia

Sjoerd J H Ebisch, Dante Mantini, G. Northoff, Anatolia Salone, Domenico De Berardis, Filippo Maria Aria Ferri, Filippo Maria Aria Ferro, Massimo Di Giannantonio, Gian Luca Uca Romani, Gian Luca Uca Gallese

Research output: Contribution to journalArticle

25 Citations (Scopus)

Abstract

Self-experience anomalies are elementary features of schizophrenic pathology. Such deficits can have a profound impact on self-other relationship, but how they are related through aberrant brain function remains poorly understood. In this functional magnetic resonance imaging (fMRI) study, we provide new evidence for a cortical link between aberrant selfexperience and social cognition in first-episode schizophrenia (FES). As identified in previous studies, ventral premotor cortex (vPMC) and posterior insula (pIC) are candidate brain regions underlying disturbances in both self-experience and self-other relationship due to their processing of predominantly externally guided (vPMC; goal-oriented behavior) and internally guided (pIC; interoception) stimuli. Results from functional interaction analysis in a sample of 24 FES patients and 22 healthy controls show aberrant functional interactions (background/intrinsic connectivity) of right vPMC and bilateral pIC with posterior cingulate cortex (PCC), a midline region that has been shown central in mediating self-experience. More specifically, our results show increased functional coupling between vPMC and PCC, which positively correlated with basic symptoms (subjective self-experience disturbances). pIC showed reduced functional coupling with PCC and postcentral gyrus and increased functional interactions with anterior insula. Taken together, our results suggest an imbalance in the processing between internally and externally guided information and its abnormal integration with self-referential processing as mediated by PCC. Due to our correlation findings, we suggest this imbalance to be closely related to basic symptoms in FES and thus anomalous self-experience. The findings further disentangle the cortical basis of how selfexperience anomalies may pervade the social domain. © The Author 2013.
Original languageEnglish
Pages (from-to)1072-1082
Number of pages11
JournalSchizophrenia Bulletin
Volume40
Issue number5
DOIs
Publication statusPublished - 2014
Externally publishedYes

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Gyrus Cinguli
Motor Cortex
Schizophrenia
Brain
Somatosensory Cortex
Cognition
Magnetic Resonance Imaging
Pathology

Keywords

  • Connectivity
  • Functional magnetic resonance imaging
  • Posterior cingulate cortex
  • Posterior insula
  • Psychosis
  • Ventral premotor cortex
  • adult
  • anterior insula
  • article
  • BOLD signal
  • brain region
  • clinical article
  • consensus
  • controlled study
  • female
  • functional magnetic resonance imaging
  • functional neuroimaging
  • human
  • insula
  • left hemisphere
  • male
  • personal experience
  • postcentral gyrus
  • posterior cingulate
  • posterior insula
  • posterior parietal cortex
  • premotor cortex
  • priority journal
  • right hemisphere
  • schizophrenia
  • self experience
  • social cognition
  • social interaction
  • somatosensory cortex
  • brain cortex
  • cingulate gyrus
  • connectome
  • ego
  • motor cortex
  • nuclear magnetic resonance imaging
  • pathophysiology
  • perception
  • Adult
  • Cerebral Cortex
  • Connectome
  • Ego
  • Female
  • Gyrus Cinguli
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Motor Cortex
  • Schizophrenia
  • Social Perception

Cite this

Altered brain long-range functional interactions underlying the link between aberrant self-experience and self-other relationship in first-episode schizophrenia. / Ebisch, Sjoerd J H; Mantini, Dante; Northoff, G.; Salone, Anatolia; De Berardis, Domenico; Ferri, Filippo Maria Aria; Ferro, Filippo Maria Aria; Di Giannantonio, Massimo; Romani, Gian Luca Uca; Gallese, Gian Luca Uca.

In: Schizophrenia Bulletin, Vol. 40, No. 5, 2014, p. 1072-1082.

Research output: Contribution to journalArticle

Ebisch, SJH, Mantini, D, Northoff, G, Salone, A, De Berardis, D, Ferri, FMA, Ferro, FMA, Di Giannantonio, M, Romani, GLU & Gallese, GLU 2014, 'Altered brain long-range functional interactions underlying the link between aberrant self-experience and self-other relationship in first-episode schizophrenia', Schizophrenia Bulletin, vol. 40, no. 5, pp. 1072-1082. https://doi.org/10.1093/schbul/sbt153
Ebisch, Sjoerd J H ; Mantini, Dante ; Northoff, G. ; Salone, Anatolia ; De Berardis, Domenico ; Ferri, Filippo Maria Aria ; Ferro, Filippo Maria Aria ; Di Giannantonio, Massimo ; Romani, Gian Luca Uca ; Gallese, Gian Luca Uca. / Altered brain long-range functional interactions underlying the link between aberrant self-experience and self-other relationship in first-episode schizophrenia. In: Schizophrenia Bulletin. 2014 ; Vol. 40, No. 5. pp. 1072-1082.
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title = "Altered brain long-range functional interactions underlying the link between aberrant self-experience and self-other relationship in first-episode schizophrenia",
abstract = "Self-experience anomalies are elementary features of schizophrenic pathology. Such deficits can have a profound impact on self-other relationship, but how they are related through aberrant brain function remains poorly understood. In this functional magnetic resonance imaging (fMRI) study, we provide new evidence for a cortical link between aberrant selfexperience and social cognition in first-episode schizophrenia (FES). As identified in previous studies, ventral premotor cortex (vPMC) and posterior insula (pIC) are candidate brain regions underlying disturbances in both self-experience and self-other relationship due to their processing of predominantly externally guided (vPMC; goal-oriented behavior) and internally guided (pIC; interoception) stimuli. Results from functional interaction analysis in a sample of 24 FES patients and 22 healthy controls show aberrant functional interactions (background/intrinsic connectivity) of right vPMC and bilateral pIC with posterior cingulate cortex (PCC), a midline region that has been shown central in mediating self-experience. More specifically, our results show increased functional coupling between vPMC and PCC, which positively correlated with basic symptoms (subjective self-experience disturbances). pIC showed reduced functional coupling with PCC and postcentral gyrus and increased functional interactions with anterior insula. Taken together, our results suggest an imbalance in the processing between internally and externally guided information and its abnormal integration with self-referential processing as mediated by PCC. Due to our correlation findings, we suggest this imbalance to be closely related to basic symptoms in FES and thus anomalous self-experience. The findings further disentangle the cortical basis of how selfexperience anomalies may pervade the social domain. {\circledC} The Author 2013.",
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author = "Ebisch, {Sjoerd J H} and Dante Mantini and G. Northoff and Anatolia Salone and {De Berardis}, Domenico and Ferri, {Filippo Maria Aria} and Ferro, {Filippo Maria Aria} and {Di Giannantonio}, Massimo and Romani, {Gian Luca Uca} and Gallese, {Gian Luca Uca}",
note = "Cited By :12 Export Date: 11 May 2016 CODEN: SCZBB Correspondence Address: Ebisch, S.J.H.; Department of Neuroscience and Imaging, G. d'Annunzio University, Via dei Vestini, 33, 66013 Chieti, Italy; email: sjoerdebisch@yahoo.com Funding Details: 320030-146531, SNSF, Swiss National Science Foundation References: Bleuler, E., Dementia praecox oder gruppe der schizophrenien (1911) Handbuch der Psychiatrie, , In: Aschaffenburg G, ed. Leipzig, Germany: Deuticke; Minkowski, E., (1927) La Schizophr{\'e}nie. 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A tri-dimensional view (2013) Neurosci Biobehav Rev., 37, pp. 726-738; Northoff, G., (2013) Unlocking the Brain., 1. , Coding. Oxford, UK: Oxford University Press; Northoff, G., (2013) Unlocking the brain., 2. , Consciousness. Oxford, UK: Oxford University Press; Lui, S., Li, T., Deng, W., Short-term effects of antipsychotic treatment on cerebral function in drug-naive first-episode schizophrenia revealed by {"}resting state{"} functional magnetic resonance imaging (2010) Arch Gen Psychiatry., 67, pp. 783-792; Sambataro, F., Blasi, G., Fazio, L., Treatment with olanzapine is associated with modulation of the default mode network in patients with schizophrenia (2010) Neuropsychopharmacology., 35, pp. 904-912",
year = "2014",
doi = "10.1093/schbul/sbt153",
language = "English",
volume = "40",
pages = "1072--1082",
journal = "Schizophrenia Bulletin",
issn = "0586-7614",
publisher = "Oxford University Press",
number = "5",

}

TY - JOUR

T1 - Altered brain long-range functional interactions underlying the link between aberrant self-experience and self-other relationship in first-episode schizophrenia

AU - Ebisch, Sjoerd J H

AU - Mantini, Dante

AU - Northoff, G.

AU - Salone, Anatolia

AU - De Berardis, Domenico

AU - Ferri, Filippo Maria Aria

AU - Ferro, Filippo Maria Aria

AU - Di Giannantonio, Massimo

AU - Romani, Gian Luca Uca

AU - Gallese, Gian Luca Uca

N1 - Cited By :12 Export Date: 11 May 2016 CODEN: SCZBB Correspondence Address: Ebisch, S.J.H.; Department of Neuroscience and Imaging, G. d'Annunzio University, Via dei Vestini, 33, 66013 Chieti, Italy; email: sjoerdebisch@yahoo.com Funding Details: 320030-146531, SNSF, Swiss National Science Foundation References: Bleuler, E., Dementia praecox oder gruppe der schizophrenien (1911) Handbuch der Psychiatrie, , In: Aschaffenburg G, ed. Leipzig, Germany: Deuticke; Minkowski, E., (1927) La Schizophrénie. 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A tri-dimensional view (2013) Neurosci Biobehav Rev., 37, pp. 726-738; Northoff, G., (2013) Unlocking the Brain., 1. , Coding. Oxford, UK: Oxford University Press; Northoff, G., (2013) Unlocking the brain., 2. , Consciousness. Oxford, UK: Oxford University Press; Lui, S., Li, T., Deng, W., Short-term effects of antipsychotic treatment on cerebral function in drug-naive first-episode schizophrenia revealed by "resting state" functional magnetic resonance imaging (2010) Arch Gen Psychiatry., 67, pp. 783-792; Sambataro, F., Blasi, G., Fazio, L., Treatment with olanzapine is associated with modulation of the default mode network in patients with schizophrenia (2010) Neuropsychopharmacology., 35, pp. 904-912

PY - 2014

Y1 - 2014

N2 - Self-experience anomalies are elementary features of schizophrenic pathology. Such deficits can have a profound impact on self-other relationship, but how they are related through aberrant brain function remains poorly understood. In this functional magnetic resonance imaging (fMRI) study, we provide new evidence for a cortical link between aberrant selfexperience and social cognition in first-episode schizophrenia (FES). As identified in previous studies, ventral premotor cortex (vPMC) and posterior insula (pIC) are candidate brain regions underlying disturbances in both self-experience and self-other relationship due to their processing of predominantly externally guided (vPMC; goal-oriented behavior) and internally guided (pIC; interoception) stimuli. Results from functional interaction analysis in a sample of 24 FES patients and 22 healthy controls show aberrant functional interactions (background/intrinsic connectivity) of right vPMC and bilateral pIC with posterior cingulate cortex (PCC), a midline region that has been shown central in mediating self-experience. More specifically, our results show increased functional coupling between vPMC and PCC, which positively correlated with basic symptoms (subjective self-experience disturbances). pIC showed reduced functional coupling with PCC and postcentral gyrus and increased functional interactions with anterior insula. Taken together, our results suggest an imbalance in the processing between internally and externally guided information and its abnormal integration with self-referential processing as mediated by PCC. Due to our correlation findings, we suggest this imbalance to be closely related to basic symptoms in FES and thus anomalous self-experience. The findings further disentangle the cortical basis of how selfexperience anomalies may pervade the social domain. © The Author 2013.

AB - Self-experience anomalies are elementary features of schizophrenic pathology. Such deficits can have a profound impact on self-other relationship, but how they are related through aberrant brain function remains poorly understood. In this functional magnetic resonance imaging (fMRI) study, we provide new evidence for a cortical link between aberrant selfexperience and social cognition in first-episode schizophrenia (FES). As identified in previous studies, ventral premotor cortex (vPMC) and posterior insula (pIC) are candidate brain regions underlying disturbances in both self-experience and self-other relationship due to their processing of predominantly externally guided (vPMC; goal-oriented behavior) and internally guided (pIC; interoception) stimuli. Results from functional interaction analysis in a sample of 24 FES patients and 22 healthy controls show aberrant functional interactions (background/intrinsic connectivity) of right vPMC and bilateral pIC with posterior cingulate cortex (PCC), a midline region that has been shown central in mediating self-experience. More specifically, our results show increased functional coupling between vPMC and PCC, which positively correlated with basic symptoms (subjective self-experience disturbances). pIC showed reduced functional coupling with PCC and postcentral gyrus and increased functional interactions with anterior insula. Taken together, our results suggest an imbalance in the processing between internally and externally guided information and its abnormal integration with self-referential processing as mediated by PCC. Due to our correlation findings, we suggest this imbalance to be closely related to basic symptoms in FES and thus anomalous self-experience. The findings further disentangle the cortical basis of how selfexperience anomalies may pervade the social domain. © The Author 2013.

KW - Connectivity

KW - Functional magnetic resonance imaging

KW - Posterior cingulate cortex

KW - Posterior insula

KW - Psychosis

KW - Ventral premotor cortex

KW - adult

KW - anterior insula

KW - article

KW - BOLD signal

KW - brain region

KW - clinical article

KW - consensus

KW - controlled study

KW - female

KW - functional magnetic resonance imaging

KW - functional neuroimaging

KW - human

KW - insula

KW - left hemisphere

KW - male

KW - personal experience

KW - postcentral gyrus

KW - posterior cingulate

KW - posterior insula

KW - posterior parietal cortex

KW - premotor cortex

KW - priority journal

KW - right hemisphere

KW - schizophrenia

KW - self experience

KW - social cognition

KW - social interaction

KW - somatosensory cortex

KW - brain cortex

KW - cingulate gyrus

KW - connectome

KW - ego

KW - motor cortex

KW - nuclear magnetic resonance imaging

KW - pathophysiology

KW - perception

KW - Adult

KW - Cerebral Cortex

KW - Connectome

KW - Ego

KW - Female

KW - Gyrus Cinguli

KW - Humans

KW - Magnetic Resonance Imaging

KW - Male

KW - Motor Cortex

KW - Schizophrenia

KW - Social Perception

U2 - 10.1093/schbul/sbt153

DO - 10.1093/schbul/sbt153

M3 - Article

C2 - 24191160

VL - 40

SP - 1072

EP - 1082

JO - Schizophrenia Bulletin

JF - Schizophrenia Bulletin

SN - 0586-7614

IS - 5

ER -