Cortical markers of excitation/inhibition balance are associated with sensory responsivity from infancy in longitudinal cohorts enriched for autism and ADHD.

Abstract

Autism and ADHD are characterised by atypical sensory responsivity, and this may be driven by alterations in the balance of cortical excitation to inhibition (E/I). Studies early in development are required to establish when sensory responsivity differences emerge and whether they predict later neurodevelopmental condition outcomes. We utilised data from a prospective longitudinal cohort of infants with and without a family history (FH) of autism and/or ADHD (N = 151; 55% male, 83% white). We extracted electroencephalography (EEG) metrics of E/I balance at 5, 10 and 14 months; the aperiodic exponent of the slope of the power spectrum ('1/f'). Models estimated latent growth curves of parent-reported hyper and hypo-responsivity between 10 - 36 months. Analyses tested associations between developmental trajectories of FH, sensory responsivity, parent-rated neurodevelopmental traits at 3 years and E/I balance. We coded and entered binary variables indexing FH-autism and FH-ADHD in the same model, which allowed us to test for effects of one form of FH whilst adjusting for the impact of the other. Results showed that FH-autism was associated with greater increases in parent-reported hyper-responsivity between 10-36 months (over and above the effects of FH-ADHD), and in univariate models for hyper-responsivity only, the intercept and the slope of hyper-responsivity were positively associated with both autistic and ADHD traits at age 3 years. However, in joint models which included hypo-responsivity, associations between hyper-responsivity and autistic and ADHD traits became non-significant. In these joint models, FH-ADHD was associated with steeper increases in hypo-responsivity (over and above the effects of FH-autism). Higher hypo-responsivity at 10-month baseline was associated with both autistic and ADHD traits at 3 years. A steeper slope of hypo-responsivity predicted ADHD traits at 3 years. Males displayed higher baseline hypo-responsivity. Aperiodic exponent values at 5 and 10, but not 14 months, were associated with hyper-responsivity. Results suggest a dissociation in the type of sensory responsivity associated with a family history of autism as compared to a family of ADHD, and that hypo-responsivity in infancy may be an indicator of later autism and ADHD outcomes. However, better measurement of each domain is required to draw strong conclusions as many hypo-responsivity items overlapped with autistic and ADHD traits. Alterations in E/I balance may contribute to early differences in sensory responsivity but further research is required to determine the directionality of effects.