Bottom-up vs. top-down connectivity imbalance in individuals with high-autistic traits: An electroencephalographic study

Front Syst Neurosci. 2022 Aug 12:16:932128. doi: 10.3389/fnsys.2022.932128. eCollection 2022.

Abstract

Brain connectivity is often altered in autism spectrum disorder (ASD). However, there is little consensus on the nature of these alterations, with studies pointing to either increased or decreased connectivity strength across the broad autism spectrum. An important confound in the interpretation of these contradictory results is the lack of information about the directionality of the tested connections. Here, we aimed at disambiguating these confounds by measuring differences in directed connectivity using EEG resting-state recordings in individuals with low and high autistic traits. Brain connectivity was estimated using temporal Granger Causality applied to cortical signals reconstructed from EEG. Between-group differences were summarized using centrality indices taken from graph theory (in degree, out degree, authority, and hubness). Results demonstrate that individuals with higher autistic traits exhibited a significant increase in authority and in degree in frontal regions involved in high-level mechanisms (emotional regulation, decision-making, and social cognition), suggesting that anterior areas mostly receive information from more posterior areas. Moreover, the same individuals exhibited a significant increase in the hubness and out degree over occipital regions (especially the left and right pericalcarine regions, where the primary visual cortex is located), suggesting that these areas mostly send information to more anterior regions. Hubness and authority appeared to be more sensitive indices than the in degree and out degree. The observed brain connectivity differences suggest that, in individual with higher autistic traits, bottom-up signaling overcomes top-down channeled flow. This imbalance may contribute to some behavioral alterations observed in ASD.

Keywords: Autistic Quotient; Granger causality; autism spectrum disorder; bottom-up and top-down connections; hubness and authority; in degree and out degree.