Autistic traits and individual brain differences: functional network efficiency reflects attentional and social impairments, structural nodal efficiencies index systemising and theory-of-mind skills

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Paul, S, Arora, A, Midha, R, Vu, D, Roy, PK and Belmonte, MK ORCID: https://orcid.org/0000-0002-4633-9400, 2021. Autistic traits and individual brain differences: functional network efficiency reflects attentional and social impairments, structural nodal efficiencies index systemising and theory-of-mind skills. Molecular Autism, 12: 3. ISSN 2040-2392

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Official URL: https://doi.org/10.1186/s13229-020-00377-8

Abstract

Background: Autism is characterised not only by impaired social cognitive 'empathising' but also by superior rule-based 'systemising'. These cognitive domains intertwine within the categorical diagnosis of autism, yet behavioural genetics suggest largely independent heritability, and separable brain mechanisms. We sought to determine whether quantitative behavioural measures of autistic traits are dimensionally associated with structural and functional brain network integrity, and whether brain bases of autistic traits vary independently across individuals.

Methods: 30 right-handed neurotypical adults (12 females) were administered psychometric (Social Responsiveness Scale, Autism Spectrum Quotient, and Systemising Quotient) and behavioural (Attention Network Test and theory-of-mind reaction time) measures of autistic traits, and structurally (diffusion tensor imaging) and functionally (500 s of 2 Hz eyes-closed resting fMRI) derived graph-theoretic measures of efficiency of information integration were computed throughout the brain and within subregions.

Results: Social impairment was positively associated with functional efficiency (r=.47, p=.006), globally and within temporo-parietal and prefrontal cortices. Delayed orienting of attention likewise associated with greater functional efficiency (r=-.46., p=.0133). Systemising was positively associated with global structural efficiency (r=.38, p=0.018), driven specifically by temporal pole; theory-of-mind reaction time was related to structural efficiency (r=-.40, p=0.0153) within right supramarginal gyrus.

Limitations: Interpretation of these relationships is complicated by the many senses of the term 'connectivity', including, functional, structural, and computational; by the approximation inherent in group functional anatomical parcellations when confronted with individual variation in functional anatomy; and by the validity, sensitivity and specificity of the several survey and experimental behavioural measures applied as correlates of brain structure and function.

Conclusions: Functional connectivities highlight distributed networks associated with domain-general properties such as attentional orienting and social cognition broadly, associating more impaired behaviour with more efficient brain networks that may reflect heightened feedforward information flow subserving autistic strengths and deficits alike. Structural connectivity results highlight specific anatomical nodes of convergence, reflecting cognitive and neuroanatomical independence of systemising and theory-of-mind. In addition, this work shows that individual differences in theory-of-mind related to brain structure can be measured behaviourally, and offers neuroanatomical evidence to pin down the slippery construct of ‘systemising’ as the capacity to construct invariant contextual associations.

Item Type:	Journal article
Publication Title:	Molecular Autism
Creators:	Paul, S., Arora, A., Midha, R., Vu, D., Roy, P.K. and Belmonte, M.K.
Publisher:	BioMed Central
Date:	21 January 2021
Volume:	12
ISSN:	2040-2392
Identifiers:	Number Type 1364668 Other 10.1186/s13229-020-00377-8 DOI
Rights:	© the author(s). This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
Divisions:	Schools > School of Social Sciences
Record created by:	Linda Sullivan
Date Added:	06 Oct 2020 09:40
Last Modified:	31 May 2021 15:07
URI:	https://irep.ntu.ac.uk/id/eprint/41162