The human primary somatosensory cortex encodes imagined movement in the absence of sensory information

Matiar Jafari,Spencer Sterling Kellis,Tyson Aflalo,Sumner Lee Norman,Charles Yu Liu,Richard Alan Andersen,Michelle Armenta Salas,Kelsie Pejsa,Srinivas Chivukula

doi:10.1038/s42003-020-01484-1

Abstract

Classical systems neuroscience positions primary sensory areas as early feed-forward processing stations for refining incoming sensory information. This view may oversimplify their role given extensive bi-directional connectivity with multimodal cortical and subcortical regions. Here we show that single units in human primary somatosensory cortex encode imagined reaches in a cognitive motor task, but not other sensory–motor variables such as movement plans or imagined arm position. A population reference-frame analysis demonstrates coding relative to the cued starting hand location suggesting that imagined reaching movements are encoded relative to imagined limb position. These results imply a potential role for primary somatosensory cortex in cognitive imagery, engagement during motor production in the absence of sensation or expected sensation, and suggest that somatosensory cortex can provide control signals for future neural prosthetic systems.

Highlights

Classical systems neuroscience positions primary sensory areas as early feed-forward processing stations for refining incoming sensory information
We found that S1 neurons encoded movement direction during motor imagery, but did not encode motor plans or imagined arm position
The paralyzed participant did not move his arm, but instead used motor imagery to imagine moving his right hand to the initial hand cue location and subsequently imagined moving it to the final target. This design allowed us to, one, understand how activity in S1 relates to storing information about arm location, movement plans, and movement execution, and two, characterize the reference frame of these signals, i.e. whether movement variables are coded relative to the initial imagined position of the hand, relative to the eyes, or relative to the body or world

Summary

Introduction

Classical systems neuroscience positions primary sensory areas as early feed-forward processing stations for refining incoming sensory information. A population reference-frame analysis demonstrates coding relative to the cued starting hand location suggesting that imagined reaching movements are encoded relative to imagined limb position These results imply a potential role for primary somatosensory cortex in cognitive imagery, engagement during motor production in the absence of sensation or expected sensation, and suggest that somatosensory cortex can provide control signals for future neural prosthetic systems. S1 neurons project to the spinal cord[6,7], and electrical or optical stimulation of S1 elicits motor movements[2,8,9] These results suggest a direct role of S1 in the production of motor behavior. We found that S1 neurons encoded movement direction during motor imagery, but did not encode motor plans or imagined arm position These results establish engagement of S1 during cognitive-motor behavior in the absence of sensations or expected sensations

Methods

Results

Discussion

Conclusion