Structural and effective brain connectivity underlying biological motion detection

Significance Visual perception of body motion is of substantial value for social cognition and everyday life. By using an integrative approach to brain connectivity, the study sheds light on architecture and functional principles of the underlying cerebro-cerebellar network. This circuity is organized in a parallel rather than hierarchical fashion. This may explain why body-language reading is rather resilient to focal brain damage but severely affected in neuropsychiatric conditions with distributed network alterations. Furthermore, visual sensitivity to body motion is best predicted by specific top-down feedback to the early visual cortex, as well as functional communication (effective connectivity) and presence of white-matter pathways between the right fusiform gyrus and superior temporal sulcus. The findings allow better understanding of the social brain. The perception of actions underwrites a wide range of socio-cognitive functions. Previous neuroimaging and lesion studies identified several components of the brain network for visual biological motion (BM) processing, but interactions among these components and their relationship to behavior remain little understood. Here, using a recently developed integrative analysis of structural and effective connectivity derived from high angular resolution diffusion imaging (HARDI) and functional magnetic resonance imaging (fMRI), we assess the cerebro-cerebellar network for processing of camouflaged point-light BM. Dynamic causal modeling (DCM) informed by probabilistic tractography indicates that the right superior temporal sulcus (STS) serves as an integrator within the temporal module. However, the STS does not appear to be a “gatekeeper” in the functional integration of the occipito-temporal and frontal regions: The fusiform gyrus (FFG) and middle temporal cortex (MTC) are also connected to the right inferior frontal gyrus (IFG) and insula, indicating multiple parallel pathways. BM-specific loops of effective connectivity are seen between the left lateral cerebellar lobule Crus I and right STS, as well as between the left Crus I and right insula. The prevalence of a structural pathway between the FFG and STS is associated with better BM detection. Moreover, a canonical variate analysis shows that the visual sensitivity to BM is best predicted by BM-specific effective connectivity from the FFG to STS and from the IFG, insula, and STS to the early visual cortex. Overall, the study characterizes the architecture of the cerebro-cerebellar network for BM processing and offers prospects for assessing the social brain.

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