A multimodal neural signature of face processing in autism within the fusiform gyrus

EU-AIMS LEAP group

doi:10.1038/s44220-024-00349-4

A multimodal neural signature of face processing in autism within the fusiform gyrus

EU-AIMS LEAP group

University of Zurich
Radboud University Nijmegen
Department of Neuroradiology, Heidelberg University Hospital, Heidelberg, Germany
University of London
University Medical Center
Goethe University Frankfurt
University of Cambridge
Human Genetics and Cognitive Functions Unity
Department of Psychology
Psychology and Neuroscience
King's College London

Research output: Contribution to journal › Article › peer-review

18 Citations (Scopus)

100 Downloads (Pure)

Abstract

Atypical face processing is commonly reported in autism. Its neural correlates have been explored extensively across single neuroimaging modalities within key regions of the face processing network, such as the fusiform gyrus (FFG). Nonetheless, it is poorly understood how variation in brain anatomy and function jointly impacts face processing and social functioning. Here we leveraged a large multimodal sample to study the cross-modal signature of face processing within the FFG across four imaging modalities (structural magnetic resonance imaging (MRI), resting-state functional magnetic resonance imaging, task-functional magnetic resonance imaging and electroencephalography) in 204 autistic and nonautistic individuals aged 7-30 years (case-control design). We combined two methodological innovations-normative modeling and linked independent component analysis-to integrate individual-level deviations across modalities and assessed how multimodal components differentiated groups and informed social functioning in autism. Groups differed significantly in a multimodal component driven by bilateral resting-state functional MRI, bilateral structure, right task-functional MRI and left electroencephalography loadings in face-selective and retinotopic FFG. Multimodal components outperformed unimodal ones in differentiating groups. In autistic individuals, multimodal components were associated with cognitive and clinical features linked to social, but not nonsocial, functioning. These findings underscore the importance of elucidating multimodal neural associations of social functioning in autism, offering potential for the identification of mechanistic and prognostic biomarkers.

Original language	English
Pages (from-to)	31-45
Number of pages	15
Journal	Nature Mental Health
Volume	3
Issue number	1
Early online date	2 Jan 2025
DOIs	https://doi.org/10.1038/s44220-024-00349-4
Publication status	Published - 31 Jan 2025

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title = "A multimodal neural signature of face processing in autism within the fusiform gyrus",

abstract = "Atypical face processing is commonly reported in autism. Its neural correlates have been explored extensively across single neuroimaging modalities within key regions of the face processing network, such as the fusiform gyrus (FFG). Nonetheless, it is poorly understood how variation in brain anatomy and function jointly impacts face processing and social functioning. Here we leveraged a large multimodal sample to study the cross-modal signature of face processing within the FFG across four imaging modalities (structural magnetic resonance imaging (MRI), resting-state functional magnetic resonance imaging, task-functional magnetic resonance imaging and electroencephalography) in 204 autistic and nonautistic individuals aged 7-30 years (case-control design). We combined two methodological innovations-normative modeling and linked independent component analysis-to integrate individual-level deviations across modalities and assessed how multimodal components differentiated groups and informed social functioning in autism. Groups differed significantly in a multimodal component driven by bilateral resting-state functional MRI, bilateral structure, right task-functional MRI and left electroencephalography loadings in face-selective and retinotopic FFG. Multimodal components outperformed unimodal ones in differentiating groups. In autistic individuals, multimodal components were associated with cognitive and clinical features linked to social, but not nonsocial, functioning. These findings underscore the importance of elucidating multimodal neural associations of social functioning in autism, offering potential for the identification of mechanistic and prognostic biomarkers.",

author = "Floris, \{Dorothea L\} and Alberto Llera and Mariam Zabihi and Carolin Moessnang and Jones, \{Emily J H\} and Luke Mason and Rianne Haartsen and Holz, \{Nathalie E\} and Ting Mei and Camille Elleaume and Vieira, \{Bruno Hebling\} and Pretzsch, \{Charlotte M\} and Forde, \{Natalie J\} and Sarah Baumeister and Flavio Dell'Acqua and Sarah Durston and Tobias Banaschewski and Christine Ecker and Holt, \{Rosemary J\} and Simon Baron-Cohen and Thomas Bourgeron and Tony Charman and Eva Loth and Murphy, \{Declan G M\} and Buitelaar, \{Jan K\} and Beckmann, \{Christian F\} and Nicolas Langer and \{EU-AIMS LEAP group\}",

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doi = "10.1038/s44220-024-00349-4",

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AU - Floris, Dorothea L

AU - Llera, Alberto

AU - Zabihi, Mariam

AU - Moessnang, Carolin

AU - Jones, Emily J H

AU - Mason, Luke

AU - Haartsen, Rianne

AU - Holz, Nathalie E

AU - Mei, Ting

AU - Elleaume, Camille

AU - Vieira, Bruno Hebling

AU - Pretzsch, Charlotte M

AU - Forde, Natalie J

AU - Baumeister, Sarah

AU - Dell'Acqua, Flavio

AU - Durston, Sarah

AU - Banaschewski, Tobias

AU - Ecker, Christine

AU - Holt, Rosemary J

AU - Baron-Cohen, Simon

AU - Bourgeron, Thomas

AU - Charman, Tony

AU - Loth, Eva

AU - Murphy, Declan G M

AU - Buitelaar, Jan K

AU - Beckmann, Christian F

AU - Langer, Nicolas

AU - EU-AIMS LEAP group

PY - 2025/1/31

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N2 - Atypical face processing is commonly reported in autism. Its neural correlates have been explored extensively across single neuroimaging modalities within key regions of the face processing network, such as the fusiform gyrus (FFG). Nonetheless, it is poorly understood how variation in brain anatomy and function jointly impacts face processing and social functioning. Here we leveraged a large multimodal sample to study the cross-modal signature of face processing within the FFG across four imaging modalities (structural magnetic resonance imaging (MRI), resting-state functional magnetic resonance imaging, task-functional magnetic resonance imaging and electroencephalography) in 204 autistic and nonautistic individuals aged 7-30 years (case-control design). We combined two methodological innovations-normative modeling and linked independent component analysis-to integrate individual-level deviations across modalities and assessed how multimodal components differentiated groups and informed social functioning in autism. Groups differed significantly in a multimodal component driven by bilateral resting-state functional MRI, bilateral structure, right task-functional MRI and left electroencephalography loadings in face-selective and retinotopic FFG. Multimodal components outperformed unimodal ones in differentiating groups. In autistic individuals, multimodal components were associated with cognitive and clinical features linked to social, but not nonsocial, functioning. These findings underscore the importance of elucidating multimodal neural associations of social functioning in autism, offering potential for the identification of mechanistic and prognostic biomarkers.

AB - Atypical face processing is commonly reported in autism. Its neural correlates have been explored extensively across single neuroimaging modalities within key regions of the face processing network, such as the fusiform gyrus (FFG). Nonetheless, it is poorly understood how variation in brain anatomy and function jointly impacts face processing and social functioning. Here we leveraged a large multimodal sample to study the cross-modal signature of face processing within the FFG across four imaging modalities (structural magnetic resonance imaging (MRI), resting-state functional magnetic resonance imaging, task-functional magnetic resonance imaging and electroencephalography) in 204 autistic and nonautistic individuals aged 7-30 years (case-control design). We combined two methodological innovations-normative modeling and linked independent component analysis-to integrate individual-level deviations across modalities and assessed how multimodal components differentiated groups and informed social functioning in autism. Groups differed significantly in a multimodal component driven by bilateral resting-state functional MRI, bilateral structure, right task-functional MRI and left electroencephalography loadings in face-selective and retinotopic FFG. Multimodal components outperformed unimodal ones in differentiating groups. In autistic individuals, multimodal components were associated with cognitive and clinical features linked to social, but not nonsocial, functioning. These findings underscore the importance of elucidating multimodal neural associations of social functioning in autism, offering potential for the identification of mechanistic and prognostic biomarkers.

UR - https://www.scopus.com/pages/publications/85218257999

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DO - 10.1038/s44220-024-00349-4

M3 - Article

C2 - 39802935

SN - 2731-6076

VL - 3

SP - 31

EP - 45

JO - Nature Mental Health

JF - Nature Mental Health

IS - 1

ER -

A multimodal neural signature of face processing in autism within the fusiform gyrus

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