Neuronal responses in the human primary motor cortex coincide with the subjective onset of movement intention in brain-machine interface-mediated actions

Abstract

Self-initiated behavior is accompanied by the experience of intending our actions. Here, we leverage the unique opportunity to examine the full intentional chain-from intention to action to environmental effects-in a tetraplegic person outfitted with a primary motor cortex (M1) brain-machine interface (BMI) generating real hand movements via neuromuscular electrical stimulation (NMES). This combined BMI-NMES approach allowed us to selectively manipulate each element of the intentional chain (intention, action, effect) while probing subjective experience and performing extra-cellular recordings in human M1. Behaviorally, we reveal a novel form of intentional binding: motor intentions are reflected in a perceived temporal attraction between the onset of intentions and that of actions. Neurally, we demonstrate that evoked spiking activity in M1 largely coincides in time with the onset of the experience of intention and that M1 spike counts and the onset of subjective intention may co-vary on a trial-by-trial basis. Further, population-level dynamics, as indexed by a decoder instantiating movement, reflect intention-action temporal binding. The results fill a significant knowledge gap by relating human spiking activity in M1 with the onset of subjective intention and complement prior human intracranial work examining pre-motor and parietal areas.