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

Subhadip Paul, Aditi Arora, Rashi Midha, Dinh Vu, Prasun K. Roy, Matthew K. Belmonte*

*Corresponding author for this work

Research output: Contribution to journalArticle

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
Thirty 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.

ResultsSocial impairment was positively associated with functional efficiency (r = .47, p = .006), globally and within temporo-parietal and prefrontal cortices. Delayed orienting of attention likewise was 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.
Original languageEnglish
Article number3
Number of pages18
JournalMolecular Autism
Volume12
Issue number1
DOIs
Publication statusPublished - 21 Jan 2021

Fields of Science and Technology Classification 2012

  • 301 Medical-Theoretical Sciences, Pharmacy

Keywords

  • Autism
  • Dimensional
  • Social
  • Attention
  • Theory-of-mind
  • fMRI
  • DTI
  • Functional connectivity
  • Graph theory

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