Abstract
BackgroundHypersensitivity, stereotyped behaviors and attentional problems in autism spectrum disorder (ASD) are compatible with inefficient filtering of undesired or irrelevant sensory information at early stages of neural processing. This could stem from the persistent overconnectivity between primary sensory regions and deep brain nuclei in both children and adults with ASD – as reported by several previous studies – which could reflect a decreased or arrested maturation of brain connectivity. However, it has not yet been investigated whether this overconnectivity can be modelled as an excessive directional influence of subcortical brain activity on primary sensory cortical regions in ASD, with respect to age-matched typically developing (TD) individuals. MethodsTo this aim, we used dynamic causal modelling to estimate (1) the directional influence of subcortical activity on cortical processing and (2) the functional segregation of primary sensory cortical regions from subcortical activity in 166 participants with ASD and 193 TD participants from the Autism Brain Imaging Data Exchange (ABIDE). We then specifically tested the hypothesis that the age-related changes of these indicators of brain connectivity would differ between the two groups. ResultsWe found that in TD participants age was significantly associated with decreased influence of subcortical activity on cortical processing, paralleled by an increased functional segregation of cortical sensory processing from subcortical activity. Instead these effects were highly reduced and mostly absent in ASD participants, suggesting a delayed or arrested development of the segregation between subcortical and cortical sensory processing in ASD. ConclusionThis atypical configuration of subcortico-cortical connectivity in ASD can result in an excessive amount of unprocessed sensory input relayed to the cortex, which is likely to impact cognitive functioning in everyday situations where it is beneficial to limit the influence of basic sensory information on cognitive processing, such as activities requiring focused attention or social interactions.
Highlights
During the transition from childhood to adulthood our brain de velops the ability to determine behavior on the basis of abstract repre sentations and long-term plans, which are not primarily driven by current sensory stimuli, emotions and interoceptive feelings
We evaluated the relationship between effective connectivity and behavioural symptoms that are often observed in association with autism spectrum disorder (ASD), in a subsample of individuals for which Social Responsiveness Scale (SRS (Constantino et al, 2003)) scores are provided in the Autism Brain Imaging Data Exchange (ABIDE) dataset (n = 219)
In our previous investigation on this sample from the ABIDE dataset (Cerliani et al, 2015) we reported that resting-state functional con nectivity between subcortical and primary sensory regions was increased in ASD with respect to typically developing (TD) participants (Fig. S2)
Summary
During the transition from childhood to adulthood our brain de velops the ability to determine behavior on the basis of abstract repre sentations and long-term plans, which are not primarily driven by current sensory stimuli, emotions and interoceptive feelings. Recent neuroimaging studies suggest that functional integration in ASD is highly driven by current sensory in formation In this respect, Hong and colleagues (Hong et al, 2019) showed that the functional segregation – measured as the order of stepwise functional connectivity (Sepulcre et al, 2012) – between pri mary sensory and transmodal cortices is significantly reduced in autism spectrum disorders (ASD). Hypersensitivity, stereotyped behaviors and attentional problems in autism spectrum disorder (ASD) are compatible with inefficient filtering of undesired or irrelevant sensory information at early stages of neural processing This could stem from the persistent overconnectivity between primary sensory regions and deep brain nuclei in both children and adults with ASD – as reported by several previous studies – which could reflect a decreased or arrested maturation of brain connectivity. Conclusion: This atypical configuration of subcortico-cortical connectivity in ASD can result in an excessive amount of unprocessed sensory input relayed to the cortex, which is likely to impact cognitive functioning in everyday situations where it is beneficial to limit the influence of basic sensory information on cognitive pro cessing, such as activities requiring focused attention or social interactions
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