Prior Somatic Stimulation Improves Performance of Acquired Motor Skill by Facilitating Functional Connectivity in Cortico-Subcortical Motor Circuits

Abstract

Once people have a well-trained motor skill, their performance becomes stabilized and achieving substantial improvement is difficult. Recently, we have shown that even a plateaued hand motor skill can be upgraded with short-period electrical stimulation to the hand prior to the task. Here, we identify the neuronal substrates underlying the improvement of the plateaued skill by examining the enhanced functional connectivity in the sensory-motor regions that are associated with motor learning. We measured brain activity using functional magnetic resonance imaging and performed psychophysiological interaction analysis. We recruited seven right-handed very-well trained participants, whose motor performance of continuously rotating two balls with their right hands became stabilized at higher performance levels. We prepared two experiments, in each of which they repeated an experimental run 16 times. In each run, they performed this cyclic rotation as many times as possible in 16 s. In the thenar-stimulation experiment, we applied 60-s stimulation to the thenar muscle before each of the 5th - 12th runs, and the others were preceded by ineffective sham stimulation. In the control experiment, the sham was always provided. Thenar stimulation enabled the participants to perform the movements at higher cycles. In association with this performance improvement, we found enhanced activity couplings between the primary motor cortex and the sensorimotor territory of the putamen and between the cerebellum and the primary sensorimotor cortices, without any quantitative activity increase. Neither behavioral change nor these increased activity couplings were observed in the control.Thus, in contrast to the stable neuronal states in the cortico-subcortical motor circuits when the well-learned task is repeated at the later stages of motor skill learning, plastic changes in the motor circuits seem to be required when the plateaued skill is upgraded, and the stimulation may entail a state of readiness for the plastic change that allows subsequent performance improvement.