Resting state auditory-language cortex connectivity is associated with hallucinations in clinical and biological subtypes of psychotic disorders.


Journal

NeuroImage. Clinical
ISSN: 2213-1582
Titre abrégé: Neuroimage Clin
Pays: Netherlands
ID NLM: 101597070

Informations de publication

Date de publication:
2020
Historique:
received: 07 05 2020
revised: 16 07 2020
accepted: 20 07 2020
pubmed: 4 8 2020
medline: 29 6 2021
entrez: 4 8 2020
Statut: ppublish

Résumé

Auditory hallucinations are prevalent across the major psychotic disorders, but their underlying mechanism is poorly understood. Limited prior work supports a hypothesis of altered auditory/language brain systems. To more definitively assess this, we examined whether alterations in resting state connectivity of auditory and language cortices are associated with hallucination severity in a large sample of individuals in the schizo-bipolar spectrum. Whole brain resting state connectivity of auditory and language cortex (primary auditory cortex, unimodal auditory association cortex, Wernicke's area [speech and heteromodal association cortex] and Broca's area [speech production motor]) was evaluated for 243 subjects with schizophrenia, schizoaffective, or bipolar disorder with psychosis and 186 healthy controls from the Bipolar Schizophrenia Network on Intermediate Phenotypes (B-SNIP) study. Regression analyses were conducted to evaluate whether resting state connectivity of auditory and language cortex was a significant predictor of current overall hallucination severity (information about specific modality of hallucinations experienced was not available). Increased connectivity between lower and higher order regions of left temporal-parietal auditory/language processing cortex was associated with worse hallucination severity for all psychosis patients. Additionally, within bipolar subjects, increased interhemispheric connectivity between higher order temporal-parietal auditory/language regions was related to greater hallucination severity. When patients were categorized by B-SNIP biomarker-based Biotype groups, interhemispheric connectivity between left auditory association cortex and right core auditory cortex was related to greater hallucination severity for Biotype 1 patients. Exploratory analyses resulted in different patterns of connectivity of auditory/language cortex in patients and controls, unrelated to current hallucination severity. Although the findings cannot be precisely attributed to auditory hallucination severity or possible differences in such experiences between groups, increased connectivity among the left hemisphere auditory and receptive language cortex may represent a significant factor contributing to hallucination severity across psychotic disorders, and additional subgroup specific connectivity alterations may also be present.

Sections du résumé

BACKGROUND
Auditory hallucinations are prevalent across the major psychotic disorders, but their underlying mechanism is poorly understood. Limited prior work supports a hypothesis of altered auditory/language brain systems. To more definitively assess this, we examined whether alterations in resting state connectivity of auditory and language cortices are associated with hallucination severity in a large sample of individuals in the schizo-bipolar spectrum.
METHODS
Whole brain resting state connectivity of auditory and language cortex (primary auditory cortex, unimodal auditory association cortex, Wernicke's area [speech and heteromodal association cortex] and Broca's area [speech production motor]) was evaluated for 243 subjects with schizophrenia, schizoaffective, or bipolar disorder with psychosis and 186 healthy controls from the Bipolar Schizophrenia Network on Intermediate Phenotypes (B-SNIP) study. Regression analyses were conducted to evaluate whether resting state connectivity of auditory and language cortex was a significant predictor of current overall hallucination severity (information about specific modality of hallucinations experienced was not available).
RESULTS
Increased connectivity between lower and higher order regions of left temporal-parietal auditory/language processing cortex was associated with worse hallucination severity for all psychosis patients. Additionally, within bipolar subjects, increased interhemispheric connectivity between higher order temporal-parietal auditory/language regions was related to greater hallucination severity. When patients were categorized by B-SNIP biomarker-based Biotype groups, interhemispheric connectivity between left auditory association cortex and right core auditory cortex was related to greater hallucination severity for Biotype 1 patients. Exploratory analyses resulted in different patterns of connectivity of auditory/language cortex in patients and controls, unrelated to current hallucination severity.
CONCLUSIONS
Although the findings cannot be precisely attributed to auditory hallucination severity or possible differences in such experiences between groups, increased connectivity among the left hemisphere auditory and receptive language cortex may represent a significant factor contributing to hallucination severity across psychotic disorders, and additional subgroup specific connectivity alterations may also be present.

Identifiants

pubmed: 32745995
pii: S2213-1582(20)30195-9
doi: 10.1016/j.nicl.2020.102358
pmc: PMC7398970
pii:
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

102358

Subventions

Organisme : NIMH NIH HHS
ID : R01 MH103368
Pays : United States

Informations de copyright

Copyright © 2020 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Auteurs

Victoria T Okuneye (VT)

Department of Psychiatry and Behavioral Neuroscience, University of Chicago, IL, USA.

Shashwath Meda (S)

Department of Psychiatry, Yale University, CT, USA.

Godfrey D Pearlson (GD)

Department of Psychiatry, Yale University, CT, USA.

Brett A Clementz (BA)

Department of Psychology, University of Georgia, GA, USA.

Matcheri S Keshavan (MS)

Department of Psychiatry, Harvard University, MA, USA.

Carol A Tamminga (CA)

Department of Psychiatry, University of Texas Southwestern Medical Center, TX, USA.

Elena Ivleva (E)

Department of Psychiatry, University of Texas Southwestern Medical Center, TX, USA.

John A Sweeney (JA)

Department of Psychiatry and Behavioral Neuroscience, University of Cincinnati, OH, USA.

Elliot S Gershon (ES)

Department of Psychiatry and Behavioral Neuroscience, University of Chicago, IL, USA.

Sarah K Keedy (SK)

Department of Psychiatry and Behavioral Neuroscience, University of Chicago, IL, USA. Electronic address: skeedy@bsd.uchicago.edu.

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