Adaptive brain changes to virtual lesions interfering with visual processing

Abstract

Introduction: Understanding the causal relationship between a focal lesion and brain network (re)organization is a crucial step in order to accurately predict the resulting symptoms of the lesion and implement personalized rehabilitation strategies. Transcranial magnetic stimulation (TMS) can be used to create local and transient neural perturbations, the so-called virtual lesion approach. In this study, we tested how a virtual lesion applied to the Early Visual Areas (EVA) or the extrastriate, motion-sensitive, medio-temporal area (hMT+/V5) in different contexts affects behavior and changes neuronal network activity and organisation, assessed with functional magnetic resonance imaging (fMRI). Methods: We applied short trains of 10 Hz TMS to healthy participants over the EVA or hMT+/MT. This was done both at rest and at relevant times during a motion discrimination task, while concurrent fMRI was performed. Regional BOLD activity was analysed using a general linear model (GLM) and functional brain networks were assessed using independent component analysis (ICA). Motion direction discrimination and motion awareness were related to the imaging data. Results: TMS applied over the EVA and hMT+/V5 induced transient modulation of motion perception and discrimination. Comparing resting versus active states, both TMS sites showed a common suppression of local and remote brain activity at rest while an over-activation of the stimulated areas and related networks were found during the task. More subtly, distinct dynamic and topological TMS-induced networks properties could be revealed depending on the exact visual processing stages TMS was applied at. In particular, brain networks associated with EVA stimulation showed a clear context-dependency and were spatially more restricted than for hMT+/V5 stimulation. Discussion: The present findings highlight the possibility of interfering with distinct visual processing stages and the possibility of imaging the local and remote neural correlates of the behavioral impact. They also confirm the complexity of TMS effects on BOLD activity, switching from signal suppression at rest to irrelevant neural noise addition during active visual processing, even differing throughout the time course of information processing. Moreover, the networks analyses suggest that the EVA might be more resilient to focal perturbations by means of a virtual lesion than hMT+/V5. As a critical processing center, the EVA may be important for maintaining stability in the visual network, whereas the perturbation of a more specialized region such as hMT+/V5 has greater impact on local and network activity, as well as on behavior. These findings add to the understanding of visual motion processing and especially to the impact and potential mechanism of focal lesions in this system.