Is functional brain connectivity atypical in autism? A systematic review of EEG and MEG studies

Abstract

BackgroundAlthough it is well recognized that autism is associated with altered patterns of over- and under-connectivity, specifics are still a matter of debate. Little has been done so far to synthesize available literature using whole-brain electroencephalography (EEG) and magnetoencephalography (MEG) recordings.Objectives1) To systematically review the literature on EEG/MEG functional and effective connectivity in autism spectrum disorder (ASD), 2) to synthesize and critically appraise findings related with the hypothesis that ASD is characterized by long-range underconnectivity and local overconnectivity, and 3) to provide, based on the literature, an analysis of tentative factors that are likely to mediate association between ASD and atypical connectivity (e.g., development, topography, lateralization).MethodsLiterature reviews were done using PubMed and PsychInfo databases. Abstracts were screened, and only relevant articles were analyzed based on the objectives of this paper. Special attention was paid to the methodological characteristics that could have created variability in outcomes reported between studies.ResultsOur synthesis provides relatively strong support for long-range underconnectivity in ASD, whereas the status of local connectivity remains unclear. This observation was also mirrored by a similar relationship with lower frequencies being often associated with underconnectivity and higher frequencies being associated with both under- and over-connectivity. Putting together these observations, we propose that ASD is characterized by a general trend toward an under-expression of lower-band wide-spread integrative processes compensated by more focal, higher-frequency, locally specialized, and segregated processes. Further investigation is, however, needed to corroborate the conclusion and its generalizability across different tasks. Of note, abnormal lateralization in ASD, specifically an elevated left-over-right EEG and MEG functional connectivity ratio, has been also reported consistently across studies.ConclusionsThe large variability in study samples and methodology makes a systematic quantitative analysis (i.e. meta-analysis) of this body of research impossible. Nevertheless, a general trend supporting the hypothesis of long-range functional underconnectivity can be observed. Further research is necessary to more confidently determine the status of the hypothesis of short-range overconnectivity. Frequency-band specific patterns and their relationships with known symptoms of autism also need to be further clarified.

The stability flexibility tradeoff and the dark side of detail

“…From the neural perspective, the heterogenous behavioral traits of ASD are not thought to stem from specific regions of the brain, but rather from atypical connectivity between brain regions. Atypical connectivity has been identified in numerous studies across multiple brain networks in ASD using various neuroimaging methods, including structural and functional MRI, EEG and MEG, and fNIRS (for reviews, see Hull et al, 2017;O'Reilly, Lewis, & Elsabbagh, 2017;Rane et al, 2015;Zhang & Roeyers, 2019). Although the findings of altered connectivity in ASD are vast, one finding that is particularly relevant to the current design is that Inflexibility of neural circuitry has been linked to behavioral inflexibility in ASD.…”

Extreme male developmental trajectories of homotopic brain connectivity in autism

“…Altered connectivity between brain areas is increasingly understood to be a characteristic feature of ASD (Geschwind & Levitt, 2007). There is considerable evidence that brain connectivity in ASD is associated with cognitive and affective alterations in this group (Hull, Jacokes, Torgerson, Irimia, & Van Horn, 2017;O'Reilly, Lewis, & Elsabbagh, 2017;Picci, Gotts, & Scherf, 2016;Rane et al, 2015). Both functional overconnectivity and underconnectivity, as well as normal levels of connectivity have been reported in ASD population (Cerliani et al, 2015;Cheng, Rolls, Gu, Zhang, & Feng, 2015;Di Martino et al, 2014;Monk et al, 2009;Vissers, Cohen, & Geurts, 2012).…”

Test‐retest reliability of EEG network characteristics in infants

“…Functional brain networks and characteristics have been used in the past to study differences between typical and atypical brain development. In autism spectrum disorder (ASD) for example, global connectivity (the averaged connection strengths of the whole brain network) tends to be deteriorated at lower frequencies, which is compensated by increased global connectivity at higher frequencies (Boersma et al, 2013;O'Reilly, Lewis, & Elsabbagh, 2017;Orekhova et al, 2014;Peters et al, 2013;Righi, Tierney, Tager-Flusberg, & Nelson, 2014). Similarly in children with attention-deficit hyperactivity disorder show an increase in frontal low alpha connectivity and a decrease in frontal high alpha connectivity (Murias, Swanson, & Srinivasan, 2007).…”