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

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 resti...

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Autores principales: Okuneye, Victoria T., Meda, Shashwath, Pearlson, Godfrey D., Clementz, Brett A., Keshavan, Matcheri S., Tamminga, Carol A., Ivleva, Elena, Sweeney, John A., Gershon, Elliot S., Keedy, Sarah K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7398970/
https://www.ncbi.nlm.nih.gov/pubmed/32745995
http://dx.doi.org/10.1016/j.nicl.2020.102358
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author Okuneye, Victoria T.
Meda, Shashwath
Pearlson, Godfrey D.
Clementz, Brett A.
Keshavan, Matcheri S.
Tamminga, Carol A.
Ivleva, Elena
Sweeney, John A.
Gershon, Elliot S.
Keedy, Sarah K.
author_facet Okuneye, Victoria T.
Meda, Shashwath
Pearlson, Godfrey D.
Clementz, Brett A.
Keshavan, Matcheri S.
Tamminga, Carol A.
Ivleva, Elena
Sweeney, John A.
Gershon, Elliot S.
Keedy, Sarah K.
author_sort Okuneye, Victoria T.
collection PubMed
description 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.
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spelling pubmed-73989702020-08-06 Resting state auditory-language cortex connectivity is associated with hallucinations in clinical and biological subtypes of psychotic disorders Okuneye, Victoria T. Meda, Shashwath Pearlson, Godfrey D. Clementz, Brett A. Keshavan, Matcheri S. Tamminga, Carol A. Ivleva, Elena Sweeney, John A. Gershon, Elliot S. Keedy, Sarah K. Neuroimage Clin Regular Article 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. Elsevier 2020-07-22 /pmc/articles/PMC7398970/ /pubmed/32745995 http://dx.doi.org/10.1016/j.nicl.2020.102358 Text en © 2020 The Authors http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Regular Article
Okuneye, Victoria T.
Meda, Shashwath
Pearlson, Godfrey D.
Clementz, Brett A.
Keshavan, Matcheri S.
Tamminga, Carol A.
Ivleva, Elena
Sweeney, John A.
Gershon, Elliot S.
Keedy, Sarah K.
Resting state auditory-language cortex connectivity is associated with hallucinations in clinical and biological subtypes of psychotic disorders
title Resting state auditory-language cortex connectivity is associated with hallucinations in clinical and biological subtypes of psychotic disorders
title_full Resting state auditory-language cortex connectivity is associated with hallucinations in clinical and biological subtypes of psychotic disorders
title_fullStr Resting state auditory-language cortex connectivity is associated with hallucinations in clinical and biological subtypes of psychotic disorders
title_full_unstemmed Resting state auditory-language cortex connectivity is associated with hallucinations in clinical and biological subtypes of psychotic disorders
title_short Resting state auditory-language cortex connectivity is associated with hallucinations in clinical and biological subtypes of psychotic disorders
title_sort resting state auditory-language cortex connectivity is associated with hallucinations in clinical and biological subtypes of psychotic disorders
topic Regular Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7398970/
https://www.ncbi.nlm.nih.gov/pubmed/32745995
http://dx.doi.org/10.1016/j.nicl.2020.102358
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