Dynamic functional connectivity in the right temporoparietal junction captures variations in male autistic trait expression

Laura Bravo Balsa; Ahmad Abu‐Akel; Carmel Mevorach

doi:10.1002/aur.3117

Dynamic functional connectivity in the right temporoparietal junction captures variations in male autistic trait expression

Laura Bravo Balsa^*, Ahmad Abu‐Akel, Carmel Mevorach^*

^*Corresponding author for this work

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Abstract

Autistic individuals can experience difficulties with attention reorienting and Theory of Mind (ToM), which are closely associated with anterior and posterior subdivisions of the right temporoparietal junction. While the link between these processes remains unclear, it is likely subserved by a dynamic crosstalk between these two subdivisions. We, therefore, examined the dynamic functional connectivity (dFC) between the anterior and posterior temporoparietal junction, as a biological marker of attention and ToM, to test its contribution to the manifestation of autistic trait expression in Autism Spectrum Condition (ASC). Two studies were conducted, exploratory (14 ASC, 15 TD) and replication (29 ASC, 29 TD), using resting‐state fMRI data and the Social Responsiveness Scale (SRS) from the Autism Brain Imaging Data Exchange repository. Dynamic Independent Component Analysis was performed in both datasets using the CONN toolbox. An additional sliding‐window analysis was performed in the replication study to explore different connectivity states (from highly negatively to highly positively correlated). Dynamic FC was reduced in ASC compared to TD adults in both the exploratory and replication datasets and was associated with increased SRS scores (especially in ASC). Regression analyses revealed that decreased SRS autistic expression was predicted by engagement of highly negatively correlated states, while engagement of highly positively correlated states predicted increased expression. These findings provided consistent evidence that the difficulties observed in ASC are associated with altered patterns of dFC between brain regions subserving attention reorienting and ToM processes and may serve as a biomarker of autistic trait expression.

Original language	English
Pages (from-to)	702-715
Number of pages	14
Journal	Autism Research
Volume	17
Issue number	4
Early online date	8 Mar 2024
DOIs	https://doi.org/10.1002/aur.3117
Publication status	E-pub ahead of print - 8 Mar 2024

Bibliographical note

ACKNOWLEDGMENTS
Ahmad Abu-Akel was supported by the Maof Fellowship for the Integration of Outstanding Faculty, Council for Higher Education (2023–2025). Resting-state fMRI and phenotypic data were obtained from the open-access Autism Brain Imaging Data Exchange repository (ABIDE; http://fcon_1000.projects.nitrc.org/indi/abide/) (Di Martino et al., 2014; Martino et al., 2017). Data preprocessing and denoising were performed using batch scripts obtained from the CONN toolbox Handbook (Nieto-Castanon, 2020). An in-house Python script to compute dynamic FC indices is available online at https://github.com/laurabravo97/dynamic_functional_connectivity_analysis. A preprint version of this paper is available on bioRxiv https://biorxiv.org/cgi/content/short/2023.06.05.543654v1.

Keywords

right temporoparietal junction (TPJ)
attention reorienting
theory of mind (ToM)
dynamic functional connectivity (dFC)
resting‐state fMRI (RSfMRI)
autism spectrum condition (ASC)
mentalizing

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Cite this

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title = "Dynamic functional connectivity in the right temporoparietal junction captures variations in male autistic trait expression",

abstract = "Autistic individuals can experience difficulties with attention reorienting and Theory of Mind (ToM), which are closely associated with anterior and posterior subdivisions of the right temporoparietal junction. While the link between these processes remains unclear, it is likely subserved by a dynamic crosstalk between these two subdivisions. We, therefore, examined the dynamic functional connectivity (dFC) between the anterior and posterior temporoparietal junction, as a biological marker of attention and ToM, to test its contribution to the manifestation of autistic trait expression in Autism Spectrum Condition (ASC). Two studies were conducted, exploratory (14 ASC, 15 TD) and replication (29 ASC, 29 TD), using resting‐state fMRI data and the Social Responsiveness Scale (SRS) from the Autism Brain Imaging Data Exchange repository. Dynamic Independent Component Analysis was performed in both datasets using the CONN toolbox. An additional sliding‐window analysis was performed in the replication study to explore different connectivity states (from highly negatively to highly positively correlated). Dynamic FC was reduced in ASC compared to TD adults in both the exploratory and replication datasets and was associated with increased SRS scores (especially in ASC). Regression analyses revealed that decreased SRS autistic expression was predicted by engagement of highly negatively correlated states, while engagement of highly positively correlated states predicted increased expression. These findings provided consistent evidence that the difficulties observed in ASC are associated with altered patterns of dFC between brain regions subserving attention reorienting and ToM processes and may serve as a biomarker of autistic trait expression.",

keywords = "right temporoparietal junction (TPJ), attention reorienting, theory of mind (ToM), dynamic functional connectivity (dFC), resting‐state fMRI (RSfMRI), autism spectrum condition (ASC), mentalizing",

author = "{Bravo Balsa}, Laura and Ahmad Abu‐Akel and Carmel Mevorach",

note = "ACKNOWLEDGMENTS Ahmad Abu-Akel was supported by the Maof Fellowship for the Integration of Outstanding Faculty, Council for Higher Education (2023–2025). Resting-state fMRI and phenotypic data were obtained from the open-access Autism Brain Imaging Data Exchange repository (ABIDE; http://fcon_1000.projects.nitrc.org/indi/abide/) (Di Martino et al., 2014; Martino et al., 2017). Data preprocessing and denoising were performed using batch scripts obtained from the CONN toolbox Handbook (Nieto-Castanon, 2020). An in-house Python script to compute dynamic FC indices is available online at https://github.com/laurabravo97/dynamic_functional_connectivity_analysis. A preprint version of this paper is available on bioRxiv https://biorxiv.org/cgi/content/short/2023.06.05.543654v1.",

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AU - Abu‐Akel, Ahmad

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N2 - Autistic individuals can experience difficulties with attention reorienting and Theory of Mind (ToM), which are closely associated with anterior and posterior subdivisions of the right temporoparietal junction. While the link between these processes remains unclear, it is likely subserved by a dynamic crosstalk between these two subdivisions. We, therefore, examined the dynamic functional connectivity (dFC) between the anterior and posterior temporoparietal junction, as a biological marker of attention and ToM, to test its contribution to the manifestation of autistic trait expression in Autism Spectrum Condition (ASC). Two studies were conducted, exploratory (14 ASC, 15 TD) and replication (29 ASC, 29 TD), using resting‐state fMRI data and the Social Responsiveness Scale (SRS) from the Autism Brain Imaging Data Exchange repository. Dynamic Independent Component Analysis was performed in both datasets using the CONN toolbox. An additional sliding‐window analysis was performed in the replication study to explore different connectivity states (from highly negatively to highly positively correlated). Dynamic FC was reduced in ASC compared to TD adults in both the exploratory and replication datasets and was associated with increased SRS scores (especially in ASC). Regression analyses revealed that decreased SRS autistic expression was predicted by engagement of highly negatively correlated states, while engagement of highly positively correlated states predicted increased expression. These findings provided consistent evidence that the difficulties observed in ASC are associated with altered patterns of dFC between brain regions subserving attention reorienting and ToM processes and may serve as a biomarker of autistic trait expression.

AB - Autistic individuals can experience difficulties with attention reorienting and Theory of Mind (ToM), which are closely associated with anterior and posterior subdivisions of the right temporoparietal junction. While the link between these processes remains unclear, it is likely subserved by a dynamic crosstalk between these two subdivisions. We, therefore, examined the dynamic functional connectivity (dFC) between the anterior and posterior temporoparietal junction, as a biological marker of attention and ToM, to test its contribution to the manifestation of autistic trait expression in Autism Spectrum Condition (ASC). Two studies were conducted, exploratory (14 ASC, 15 TD) and replication (29 ASC, 29 TD), using resting‐state fMRI data and the Social Responsiveness Scale (SRS) from the Autism Brain Imaging Data Exchange repository. Dynamic Independent Component Analysis was performed in both datasets using the CONN toolbox. An additional sliding‐window analysis was performed in the replication study to explore different connectivity states (from highly negatively to highly positively correlated). Dynamic FC was reduced in ASC compared to TD adults in both the exploratory and replication datasets and was associated with increased SRS scores (especially in ASC). Regression analyses revealed that decreased SRS autistic expression was predicted by engagement of highly negatively correlated states, while engagement of highly positively correlated states predicted increased expression. These findings provided consistent evidence that the difficulties observed in ASC are associated with altered patterns of dFC between brain regions subserving attention reorienting and ToM processes and may serve as a biomarker of autistic trait expression.

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KW - dynamic functional connectivity (dFC)

KW - resting‐state fMRI (RSfMRI)

KW - autism spectrum condition (ASC)

KW - mentalizing

U2 - 10.1002/aur.3117

DO - 10.1002/aur.3117

M3 - Article

SN - 1939-3792

VL - 17

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EP - 715

JO - Autism Research

JF - Autism Research

IS - 4

ER -

Dynamic functional connectivity in the right temporoparietal junction captures variations in male autistic trait expression

Abstract

Bibliographical note

Keywords

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