Causal disconnectomics of motion perception networks: insights from transcranial magnetic stimulation-induced BOLD...

Understanding how focal perturbations trigger large-scale network reorganization is essential for uncovering the neural mechanisms that support perception and behaviour. Here we used a transcranial magnetic stimulation (TMS) perturbational approach by applying brief 10 Hz TMS to early visual areas (EVAs) or the medio-temporal (MT) area in healthy participants while recording concurrent functional magnetic resonance imaging (fMRI). TMS delivered during the early stages of motion processing specifically impaired direction discrimination at both sites, whereas disruption of the later processing phase impaired performances only for the MT condition. Despite a similar local increase in BOLD activity induced by EVA and MT stimulation, the broader network responses diverged significantly. Perturbation of EVA elicited a more robust and efficient pattern of functional reorganization, manifesting as more constrained BOLD changes, consistent with greater resilience to focal disruption. In contrast behavioural impairments induced by MT stimulation were accompanied by a disorganized and less-efficient network configuration, characterized by smaller small-world properties and longer path lengths. The decrease in performances induced by MT stimulation scaled with lower clustering coefficients, implying a more random or decentralized network structure. These findings demonstrate that TMS-fMRI coupling provides a powerful framework for causally mapping the relationships between local neural perturbations, large-scale network dynamics and behavioural performance. KEY POINTS: Transcranial magnetic stimulation (TMS)-induced perturbation of the early visual areas (EVAs) or the medio-temporal (MT) area selectively impairs motion direction discrimination. The TMS perturbation is associated with a context-dependent local upscaling of blood-oxygen-level dependent (BOLD) activity in both areas. The two visual areas exhibit distinct topological networks' adaptation in response to TMS, reflecting different levels of network resilience to a focal lesion. TMS-functional magnetic resonance imaging (fMRI) coupling can be used to assess 'causal disconnectomics' and to precisely map how a local perturbation propagates to large-scale behavioural deficits.