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 co-first authors
Rashi Midha
Dinh Hung Vu
Prasun K Roy
Matthew K Belmonte

Molecular Autism 12:3 (21 January 2021)

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LAY ABSTRACT

Autism, like other complex neuropsychiatric conditions, casts long shadows across the general population: those of us who are not on the autism spectrum nevertheless each have some level of autistic traits, more or less. In this sense the autism spectrum blends into the broader spectrum of cognitive diversity, and studying these shades of autistic-like traits can help us understand non-autistic and autistic minds alike. But are these subtle differences between individual minds also evident between individual brains? And if so, are different types of autistic traits localised in different parts of the brain, or are they amalgamated throughout the brain? Autistic thought and behaviour involve distinct approaches to people, for instance difficulty keeping one's own thoughts separate from what one knows about other people's, and trouble responding when someone tries to start a conversation; and approaches to things, such as laser-focussed attention that sticks onto one phenomenon at a time, and skill at fitting together the bits and pieces of puzzles, mechanical devices, or computer programs. In autism itself these skills and impairments come hand in hand. Outside the autism spectrum, though, each may arise on its own, so that some individuals may be both easygoing around people and mindful of details when it comes to inanimate things. Scanning the brains of thirty non-autistic people, we find that skills in fitting together bits and pieces and in thinking about others' thoughts each come along with more efficient structure of two separate, specific parts of the brain. We also find, though, that trouble responding socially and trouble shifting attention both relate to more efficient functioning of a widespread network of brain regions. Whereas the link between specific skills and efficient brain structure seems straightforward enough, the link between autistic impairments and efficient brain function belies ideology: How is it that more efficient brain networks produce slower attention, and more maladroit social responses? Brain function is a balance between information fed forward from the senses to inform the conscious mind, and control fed back from the conscious mind to regulate the senses; we suggest that these brain scans capture an efficiency of feedforward sensation which may come at the expense of feedback control, reflecting a balance between autistic superiorities and deficits. Whereas specific autism-related skills and impairments in thinking about parts and details and about others' minds seem linked straightforwardly each to specialised structures in the brain, more general social and attentional differences relate to the way the brain functions overall, and may reflect tradeoffs between superiorities and deficits. Knowing about these tradeoffs can help target treatments to remediate autistic deficits without harming autistic skills, and likewise could inform educational strategies to develop skills in the general population.

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.