A neurophysiologically interpretable deep neural network predicts complex movement components from brain activity

The effective decoding of movement from non-invasive electroencephalography (EEG) is essential for informing several therapeutic interventions, from neurorehabilitation robots to neural prosthetics. Deep neural networks are most suitable for decoding real-time data but their use in EEG is hindered by the gross classes of motor tasks in the currently available datasets, which are solvable even with network architectures that do not require specialized design considerations. Moreover, the weak association with the underlying neurophysiology limits the generalizability of modern networks for EEG inference. Here, we present a neurophysiologically interpretable 3-dimensional convolutional neural network (3D-CNN) that captured the spatiotemporal dependencies in brain areas that get co-activated during movement. The 3D-CNN received topography-preserving EEG inputs, and predicted complex components of hand movements performed on a plane using a back-drivable rehabilitation robot, namely (a) the reaction time (RT) for responding to stimulus (slow or fast), (b) the mode of movement (active or passive, depending on whether there was an assistive force provided by the apparatus), and (c) the orthogonal directions of the movement (left, right, up, or down). We validated the 3D-CNN on a new dataset that we acquired from an in-house motor experiment, where it achieved average leave-one-subject-out test accuracies of 79.81%, 81.23%, and 82.00% for RT, active vs. passive, and direction classifications, respectively. Our proposed method outperformed the modern 2D-CNN architecture by a range of 1.1% to 6.74% depending on the classification task. Further, we identified the EEG sensors and time segments crucial to the classification decisions of the network, which aligned well with the current neurophysiological knowledge on brain activity in motor planning and execution tasks. Our results demonstrate the importance of biological relevance in networks for an accurate decoding of EEG, suggesting that the real-time classification of other complex brain activities may now be within our reach.