Goal-directed action preparation in humans entails a mixture of corticospinal neural computations

Abstract

The seemingly effortless ability of humans to transition from thinking about actions to initiating them relies on sculpting corticospinal (CS) output from the primary motor cortex. The present study tested whether canonical additive and multiplicative neural computations, well-described in sensory systems, generalize to the CS pathway during human action preparation. We used non-invasive brain stimulation to measure CS input–output across varying action preparation contexts during instructed-delay finger response tasks. Goal-directed action preparation was marked by increased multiplicative gain of CS projections to task-relevant muscles and additive suppression of CS projections to non-selected and task-irrelevant muscles. Individuals who modulated CS gain to a greater extent were faster to initiate prepared responses. Our findings provide physiological evidence of combined additive suppression and gain modulation in the human motor system. We propose that these computations support action preparation by enhancing the contrast between selected motor representations and surrounding background activity to facilitate response selection and execution.

Key points

• Neural computations determine what information is transmitted through brain circuits.
• We investigated whether the motor system uses computations similar to those observed in sensory systems by non-invasively stimulating the corticospinal pathway in humans during goal-directed action preparation.
• We discovered physiological evidence indicating that corticospinal projections to behaviourally relevant muscles exhibit non-linear gain computations, whereas projections to behaviourally irrelevant muscles exhibit linear suppression.
• Our findings suggest that certain computational principles generalize to the human motor system and serve to enhance the contrast between relevant and background neural activity.
• These results indicate that neural computations during goal-directed action preparation may support motor control by increasing signal-to-noise within the corticospinal pathway.