Neural circuit disruptions of eye gaze processing in autism spectrum disorder and schizophrenia: An activation likelihood estimation meta-analysis.

Amygdala Autism spectrum disorder Cognitive control Eye gaze Lateral prefrontal cortex Schizophrenia

Journal

Schizophrenia research
ISSN: 1573-2509
Titre abrégé: Schizophr Res
Pays: Netherlands
ID NLM: 8804207

Informations de publication

Date de publication:
11 Jan 2024
Historique:
received: 22 02 2023
revised: 07 09 2023
accepted: 05 12 2023
medline: 13 1 2024
pubmed: 13 1 2024
entrez: 12 1 2024
Statut: aheadofprint

Résumé

Impairment in social cognition, particularly eye gaze processing, is a shared feature common to autism spectrum disorder (ASD) and schizophrenia. However, it is unclear if a convergent neural mechanism also underlies gaze dysfunction in these conditions. The present study examined whether this shared eye gaze phenotype is reflected in a profile of convergent neurobiological dysfunction in ASD and schizophrenia. Activation likelihood estimation (ALE) meta-analyses were conducted on peak voxel coordinates across the whole brain to identify spatial convergence. Functional coactivation with regions emerging as significant was assessed using meta-analytic connectivity modeling. Functional decoding was also conducted. Fifty-six experiments (n = 30 with schizophrenia and n = 26 with ASD) from 36 articles met inclusion criteria, which comprised 354 participants with ASD, 275 with schizophrenia and 613 healthy controls (1242 participants in total). In ASD, aberrant activation was found in the left amygdala relative to unaffected controls during gaze processing. In schizophrenia, aberrant activation was found in the right inferior frontal gyrus and supplementary motor area. Across ASD and schizophrenia, aberrant activation was found in the right inferior frontal gyrus and right fusiform gyrus during gaze processing. Functional decoding mapped the left amygdala to domains related to emotion processing and cognition, the right inferior frontal gyrus to cognition and perception, and the right fusiform gyrus to visual perception, spatial cognition, and emotion perception. These regions also showed meta-analytic connectivity to frontoparietal and frontotemporal circuitry. Alterations in frontoparietal and frontotemporal circuitry emerged as neural markers of gaze impairments in ASD and schizophrenia. These findings have implications for advancing transdiagnostic biomarkers to inform targeted treatments for ASD and schizophrenia.

Sections du résumé

BACKGROUND BACKGROUND
Impairment in social cognition, particularly eye gaze processing, is a shared feature common to autism spectrum disorder (ASD) and schizophrenia. However, it is unclear if a convergent neural mechanism also underlies gaze dysfunction in these conditions. The present study examined whether this shared eye gaze phenotype is reflected in a profile of convergent neurobiological dysfunction in ASD and schizophrenia.
METHODS METHODS
Activation likelihood estimation (ALE) meta-analyses were conducted on peak voxel coordinates across the whole brain to identify spatial convergence. Functional coactivation with regions emerging as significant was assessed using meta-analytic connectivity modeling. Functional decoding was also conducted.
RESULTS RESULTS
Fifty-six experiments (n = 30 with schizophrenia and n = 26 with ASD) from 36 articles met inclusion criteria, which comprised 354 participants with ASD, 275 with schizophrenia and 613 healthy controls (1242 participants in total). In ASD, aberrant activation was found in the left amygdala relative to unaffected controls during gaze processing. In schizophrenia, aberrant activation was found in the right inferior frontal gyrus and supplementary motor area. Across ASD and schizophrenia, aberrant activation was found in the right inferior frontal gyrus and right fusiform gyrus during gaze processing. Functional decoding mapped the left amygdala to domains related to emotion processing and cognition, the right inferior frontal gyrus to cognition and perception, and the right fusiform gyrus to visual perception, spatial cognition, and emotion perception. These regions also showed meta-analytic connectivity to frontoparietal and frontotemporal circuitry.
CONCLUSION CONCLUSIONS
Alterations in frontoparietal and frontotemporal circuitry emerged as neural markers of gaze impairments in ASD and schizophrenia. These findings have implications for advancing transdiagnostic biomarkers to inform targeted treatments for ASD and schizophrenia.

Identifiants

pubmed: 38215566
pii: S0920-9964(23)00437-1
doi: 10.1016/j.schres.2023.12.003
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

298-313

Informations de copyright

Copyright © 2023 Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of competing interest The authors declare no competing interests.

Auteurs

Karim Ibrahim (K)

Yale University School of Medicine, Child Study Center, United States of America. Electronic address: karim.ibrahim@yale.edu.

Iciar Iturmendi-Sabater (I)

Yale University School of Medicine, Child Study Center, United States of America.

Maya Vasishth (M)

Yale University School of Medicine, Child Study Center, United States of America.

Daniel S Barron (DS)

Brigham and Women's Hospital, Department of Psychiatry, Anesthesiology and Pain Medicine, United States of America; Harvard Medical School, Department of Psychiatry, United States of America.

MariaRose Guardavaccaro (M)

Yale University School of Medicine, Child Study Center, United States of America.

Melissa C Funaro (MC)

Yale University, Harvey Cushing/John Hay Whitney Medical Library, United States of America.

Avram Holmes (A)

Yale University, Department of Psychology, United States of America; Yale University, Department of Psychiatry, United States of America; Yale University, Wu Tsai Institute, United States of America.

Gregory McCarthy (G)

Yale University, Department of Psychology, United States of America; Yale University, Wu Tsai Institute, United States of America.

Simon B Eickhoff (SB)

Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf, Germany; Institute of Neuroscience and Medicine, Brain and Behaviour (INM-7), Research Centre Jülich, Jülich, Germany.

Denis G Sukhodolsky (DG)

Yale University School of Medicine, Child Study Center, United States of America.

Classifications MeSH