Local field potentials in human motor and non-motor brain areas encode the direction of upcoming movements: An intracerebral EEG classification study

Limb movement direction can be inferred from motor cortex activity. In humans, such decoding has been predominantly demonstrated using the spectral power of electrophysiological signals recorded in sensorimotor areas during movement execution. Yet, it remains unclear to what extent intended hand movement direction can be predicted from brain signals recorded during movement planning. Furthermore, whether other oscillatory features beyond power are also involved in direction encoding is not fully understood. Here, we set out to probe the directional-tuning of oscillatory phase, amplitude and Phase-Amplitude Coupling (PAC) during motor planning and execution, using a machine learning framework on multi-site local field potentials (LFPs) in humans. To this end, we recorded intracranial EEG data from implanted epilepsy patients as they performed a four-direction delayed center-out motor task. We found that LFP power significantly predicted hand-movement direction at execution but also during planning. While successful classification during planning primarily involved low-frequency power in a fronto-parietal circuit, decoding during execution was largely mediated by higher frequency activity in motor and premotor areas. Interestingly, LFP phase at very low frequencies (<1.5 Hz) led to significant decoding in premotor brain regions during execution. The machine learning framework also showed PAC to be uniformly modulated across directions through the task. Cross-temporal generalization analyses revealed that several stable brain patterns in prefrontal and premotor brain regions encode directions across both planning and execution. Finally, multivariate classification led to an increase in overall decoding accuracy (>80%) during both planning and execution. The novel insights revealed here extend our understanding of the role of neural oscillations in encoding motor plans.