Cortically-evoked movement in humans reflects history of prior executions, not plan for upcoming movement

Abstract

Human motor behavior involves planning and execution, but we often perform some actions more frequently. Experimentally manipulating the probability distribution of a movement through intensive repetition toward a certain direction causes physiological bias toward that direction, which can be cortically-evoked by transcranial magnetic stimulation (TMS). However, because movement execution and plan histories were indistinguishable to date, to what extent TMS-evoked biases are due to more frequently executed movement, or recent planning of movement, is unclear. Here, we use novel experimentation to separately manipulate recent history of movement plans and execution, and probe the effects of this on physiological biases using TMS, and on default plan for goal-directed actions using a behavioral timed-response task. At baseline, physiological biases shared similar low-level kinematic properties (direction) to default plan for upcoming movement. However, when recent movement execution history was manipulated via thumb movement repetitions toward a specific direction, we found a significant effect on physiological biases, but not plan-based goal-directed movement. To further determine if physiological biases reflect ongoing motor planning, we biased movement plan history by increasing the likelihood of a specific target location, and found a significant effect on the default plan for goal-directed movements. However, TMS-evoked movement during the preparation period did not become biased toward the most frequent plan. This suggests that physiological biases provide a readout of the default state of M1 population activity in the movement-related space, but not ongoing neural activation in the planning-related space, potentially ruling out relevance of cortically-evoked physiological biases to voluntary movements. HighlightsO_LIStimulating the human motor cortex selectively evoked thumb movements toward a specific direction (physiological bias) C_LIO_LIAt baseline, these physiological biases shared similar low-level kinematics with default plan for voluntary goal-directed movements C_LIO_LIModulating the probability distribution of prior movements had a significant effect on physiological biases C_LIO_LIHowever, biasing history of plans for upcoming movement toward a specific direction had no effect on evoked movement direction C_LIO_LIDuring ongoing planning of voluntary movement, evoked movements maintained the distinct and robust baseline bias, regardless of change in probability distribution of history of upcoming plans C_LI