Motor planning brings human primary somatosensory cortex into action-specific preparatory states.

Giacomo Ariani,J Andrew Pruszynski,Jörn Diedrichsen

doi:10.7554/elife.69517

Abstract

Motor planning plays a critical role in producing fast and accurate movement. Yet, the neural processes that occur in human primary motor and somatosensory cortex during planning, and how they relate to those during movement execution, remain poorly understood. Here, we used 7T functional magnetic resonance imaging and a delayed movement paradigm to study single finger movement planning and execution. The inclusion of no-go trials and variable delays allowed us to separate what are typically overlapping planning and execution brain responses. Although our univariate results show widespread deactivation during finger planning, multivariate pattern analysis revealed finger-specific activity patterns in contralateral primary somatosensory cortex (S1), which predicted the planned finger action. Surprisingly, these activity patterns were as informative as those found in contralateral primary motor cortex (M1). Control analyses ruled out the possibility that the detected information was an artifact of subthreshold movements during the preparatory delay. Furthermore, we observed that finger-specific activity patterns during planning were highly correlated to those during execution. These findings reveal that motor planning activates the specific S1 and M1 circuits that are engaged during the execution of a finger press, while activity in both regions is overall suppressed. We propose that preparatory states in S1 may improve movement control through changes in sensory processing or via direct influence of spinal motor neurons.

Highlights

Animals are capable of generating a wide variety of dexterous behaviors accurately and effortlessly on a daily basis
The behavioral study of motor planning led to neurophysiological investigations showing the presence of preparatory signals in the patterns of neuronal firing in the dorsal premotor cortex, PMd (Cisek and Kalaska, 2004, 2010; Hoshi and Tanji, 2006), the supplementary motor area, SMA (Hoshi and Tanji, 2004), and the posterior parietal cortex, PPC (Cui and Andersen, 2007, 2011; Andersen and Cui, 2009)
Our analyses indicate that information about single finger actions is already represented during motor planning in the same parts of the primary motor and somatosensory cortices that are engaged during execution of the presses

Summary

Introduction

Animals are capable of generating a wide variety of dexterous behaviors accurately and effortlessly on a daily basis This remarkable ability relies on the motor system reaching the appropriate preparatory state before each movement is initiated. At the level of neural population dynamics (Vyas et al, 2020), motor planning can be understood as bringing the neuronal state towards an ideal preparatory point. Once this state is reached and the execution is triggered, the intrinsic dynamics of the system let the movement unfold (Churchland et al, 2010; Shenoy et al, 2013). The degree to which primary somatosensory cortex (S1) receives information about the planned movement before movement onset is less clear

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