TY - JOUR
T1 - Atypically high influence of subcortical activity on primary sensory regions in autism
AU - Lorenzini, Luigi
AU - van Wingen, Guido
AU - Cerliani, Leonardo
N1 - Funding Information: This work was supported by the Netherlands Organization for Scientific research (NWO/ZonMw Vidi 016.156.318) Publisher Copyright: © 2021 The Author(s)
PY - 2021/1/1
Y1 - 2021/1/1
N2 - Background: 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. 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. Methods: To 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. Results: We 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. 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 processing, such as activities requiring focused attention or social interactions.
AB - Background: 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. 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. Methods: To 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. Results: We 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. 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 processing, such as activities requiring focused attention or social interactions.
KW - Autism Spectrum Disorder
KW - Brain Connectivity
KW - Brain maturation
KW - Dynamic Causal Modelling
KW - Primary sensory cortex
KW - Subcortical nuclei
UR - http://www.scopus.com/inward/record.url?scp=85118697465&partnerID=8YFLogxK
U2 - https://doi.org/10.1016/j.nicl.2021.102839
DO - https://doi.org/10.1016/j.nicl.2021.102839
M3 - Article
C2 - 34624634
SN - 2213-1582
VL - 32
JO - NeuroImage: Clinical
JF - NeuroImage: Clinical
M1 - 102839
ER -