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bioRxiv · 10.1101/2024.07.08.602530

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 output from primary motor cortex. This study tested whether canonical additive and multiplicative neural computations, well-described in sensory systems, generalize to the corticospinal pathway during human action preparation. We used non-invasive brain stimulation to measure corticospinal input-output across varying action preparation contexts during instructed-delay finger response tasks. Goal-directed action preparation was marked by increased multiplicative gain of corticospinal projections to task-relevant muscles and additive suppression of corticospinal projections to non-selected and task-irrelevant muscles. Individuals who modulated corticospinal 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 these computations support action preparation by enhancing the contrast between selected motor representations and surrounding background activity to facilitate response selection and execution. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=108 SRC="FIGDIR/small/602530v4_figa1.gif" ALT="Figure 1"> View larger version (25K): org.highwire.dtl.DTLVardef@9f2444org.highwire.dtl.DTLVardef@5f6eforg.highwire.dtl.DTLVardef@196f41corg.highwire.dtl.DTLVardef@1746035_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOC_FLOATNO Goal-directed action preparation shapes corticospinal output across selected, nonselected, and task-irrelevant motor representations. This study examined whether additive and multiplicative neural computations, common in sensory systems, occur within the corticospinal pathway during action preparation. We probed corticospinal input-output during the performance of various instructed-delay response tasks by applying a range of transcranial magnetic stimulation (TMS) intensities (input) over the primary motor cortex and measuring the resultant motor-evoked potentials (output) from the hand. We found that goal-directed action preparation increases corticospinal gain multiplicatively in task-relevant motor representations while additively suppressing nonselected and irrelevant representations. Greater gain modulation predicted faster responses, highlighting how these computations can enhance signal-to-noise (SNR) to enable efficient action selection and execution in the human motor system. C_FIG Key pointsO_LINeural computations determine what information is transmitted through brain circuits. C_LIO_LIWe investigated whether the motor system uses computations similar to those observed in sensory systems by noninvasively stimulating the corticospinal pathway in humans during goal-directed action preparation. C_LIO_LIWe discovered physiological evidence that corticospinal projections to behaviorally relevant muscles exhibit nonlinear gain computations, while projections to behaviorally irrelevant muscles exhibit linear suppression. C_LIO_LIOur findings suggest that certain computational principles generalize to the human motor system and serve to enhance the contrast between relevant and background neural activity. C_LIO_LIThese results indicate that neural computations during goal-directed action preparation may support motor control by increasing signal-to-noise within the corticospinal pathway. C_LI

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BibTeXRIS

Wadsley, C. G., Nguyen, T., Horton, C., Greenhouse, I.. 2024-07-11. Goal-directed action preparation in humans entails a mixture of corticospinal neural computations. https://doi.org/10.1101/2024.07.08.602530

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