Motor and cognitive brain circuits of brain-machine interactions

Brain-machine interfaces (BMIs) allow the user to control an external device such as a robotic arm, a cursor, or an avatar in a virtual world through the real-time decoding of brain signals and without the involvement of the musculoskeletal system. Although BMIs hold great promise for providing motor-impaired patients with means of control and interaction with the external world, the neurocognitive mechanisms that are involved in the use of a BMI remain poorly understood. In addition, BMIs allow researchers to investigate and separate the brain processes underlying cognitive functions from those related to motor control and afferent sensory signals that reliably accompany movements. Thus, BMIs are powerful tools for basic and applied neuroscience research. The present work investigates different stages of a BMI-mediated action and targets the subjective, behavioral, and neural signals of BMI control based on electroencephalography (EEG) signals. More specifically, the main study of this thesis has focused on the development of a multimodal imaging platform that allows EEG-based BMI control inside the magnetic resonance imaging (MRI) scanner and during the acquisition of functional MRI (fMRI). This platform has enabled us to exploit both the high temporal resolution of EEG and the high spatial resolution of fMRI to precisely identify the brain mechanisms underlying BMI control and those reflecting the subjective feeling of being in control over a BMI-action (i.e., the sense of agency, SoA). In this study we found an extended cortico-subcortical network involved in operating a motor-imagery BMI. Overall BMI performance was associated with activity in a set of regions including contralateral premotor cortex and the posterior cingulate cortex. Finally, cortical midline regions and the basal ganglia were involved in the subjective sense of controlling the BMI. In a second study, we further investigated whether the ability to control a BMI relates to the ability to perform motor imagery. Despite decades of technical advances, effective BMI-control remains limited to a subset of users. We show that inter-subject variability in BMI proficiency is associated with differences in motor imagery accuracy as captured by subjective and behavioral measurements, pointing to a prominent role of kinesthetic rather than visual imagery. We also identified enhanced lateralized Ό-band oscillations over sensorimotor cortices during motor imagery in high- versus low-aptitude BMI users. Finally, we developed a novel paradigm for joint BMI actions, allowing two users to be jointly engaged in BMI control; our preliminary data provide evidence in support of the hypothesis that joint actions yield BMI-performance improvement even in absence of a physical connection. Our findings also show that during joint BMI-control the SoA over the imagery-mediated actions is significantly enhanced, and is affected by BMI abilities. This work show the potential of applying a multimodal imaging approach to the field of BMI: exploiting our EEG-BMI-fMRI platform we were able to identify, the neural mechanisms involved in motor and cognitive aspects of imagery-mediated BMI. Furthermore, our results enable us to better understand the subjective and behavioral aspects of BMI-actions, and reveal strategies that could potentially reinforce BMI control. Our findings can ultimately be of relevance for the field of neuroprosthetics and make BMI more accessible to a broader range of users.