Single-neuron activity in the human supplementary motor area underlying preparation for action

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Abstract
The supplementary motor area (SMA) is considered critical in the planning, initiation, and execution of motor acts. Despite decades of research, including electrical stimulation mapping in patients undergoing neurosurgery, the contribution of this region to the generation of motor behavior has remained enigmatic. This is a study of single-neuron responses at various stages of a motor task during depth electrode recording in the SMA, pre-SMA, and medial temporal lobe of humans, with the goal of elucidating the disparate roles of neurons in these regions during movements. The patients were undergoing evaluation for epilepsy surgery requiring implantation of intracranial depth electrodes. Single-unit recordings were made during both the execution and mental imagery of finger apposition sequences. Only medial frontal neurons responded selectively to specific features of the motor plan, such as which hand performed the motor activity or the complexity of the sequence. Neuron activity progressively increased before the patient was given a "go" cue for the execution of movements; this activity peaked earlier in the pre-SMA than in the SMA proper. We observed similar patterns of activation during motor imagery and actual movement, but only neurons in the SMA differentiated between imagined and real movements. These results provide support at the single-neuron level for the role of the medial frontal cortex in the temporal organization and planning of movements in humans.