Brain-wide spatial mapping of oscillatory activity during naturalistic motor behavior

Understanding oscillatory neural activity associated with motor behavior is greatly contributing to the development of neuroprosthetic systems, robotic interfaces, and advanced neurorehabilitation techniques. Most current knowledge about movement-specific patterns of cortical activity is derived from laboratory experiments using highly standardized, repetitive, and often meaningless movements that are very distinct from natural motor behavior. This is characterized by frequent task switching, diverse kinematics, and endogenous motivation. Whether observed patterns of movement-related neural activity during standard laboratory tasks can be generalized to natural motor behavior is largely unknown. Here, we investigated the spatial, spectral, and temporal features of oscillatory neural activity associated with human motor control in a parkour of everyday movements. We replicated strong and significant decreases in the alpha/beta frequency range before movement onset and further show that this power decrease began about 2 s before movement initiation and reached a nadir around movement onset. In addition to the sustained event-related decrease in the alpha/beta range, we identified brief (4-5 cycles) increases in low-frequency activity (3-5 Hz) that either preceded or peaked at movement onset. These low-frequency increases exhibited much greater focality and lateralization compared with the wide-spread alpha/beta decrease. Together, our results provide a comprehensive account of brain rhythmic electric activity across spatial, spectral, and temporal scales in naturalistic motor behavior. Movement-preceding low-frequency activity has previously been identified as a promising brain stimulation target in patients with stroke. Detectability of low-frequency activity in naturalistic movements may enhance its utility as a target for on-demand brain stimulation in neurorehabilitation.NEW & NOTEWORTHY We here provide a comprehensive account of brain rhythmic electric activity across spatial, spectral, and temporal scales, associated with ecologically valid, freely chosen, auditory cued, and visually guided movements of either hand. New and noteworthy, the brain-wide topography of movement preceding, short-lasting increases in low-frequency activity (3-5 Hz), recently identified as a promising target for on-demand neurostimulation in stroke rehabilitation, is described and compared with classically studied sensorimotor rhythms.