From the motor cortex to the movement and back again.

Wondimu W Teka,Khaldoun C Hamade,Yaroslav I Molkov,Sergey N Markin,Taegyo Kim,William H Barnett,Ilya A Rybak,Mikhail A Lebedev

doi:10.1371/journal.pone.0179288

Wondimu W Teka, Khaldoun C Hamade + Show 6 more

Open Access

https://doi.org/10.1371/journal.pone.0179288

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Abstract

The motor cortex controls motor behaviors by generating movement-specific signals and transmitting them through spinal cord circuits and motoneurons to the muscles. Precise and well-coordinated muscle activation patterns are necessary for accurate movement execution. Therefore, the activity of cortical neurons should correlate with movement parameters. To investigate the specifics of such correlations among activities of the motor cortex, spinal cord network and muscles, we developed a model for neural control of goal-directed reaching movements that simulates the entire pathway from the motor cortex through spinal cord circuits to the muscles controlling arm movements. In this model, the arm consists of two joints (shoulder and elbow), whose movements are actuated by six muscles (4 single-joint and 2 double-joint flexors and extensors). The muscles provide afferent feedback to the spinal cord circuits. Cortical neurons are defined as cortical "controllers" that solve an inverse problem based on a proposed straight-line trajectory to a target position and a predefined bell-shaped velocity profile. Thus, the controller generates a motor program that produces a task-specific activation of low-level spinal circuits that in turn induce the muscle activation realizing the intended reaching movement. Using the model, we describe the mechanisms of correlation between cortical and motoneuronal activities and movement direction and other movement parameters. We show that the directional modulation of neuronal activity in the motor cortex and the spinal cord may result from direction-specific dynamics of muscle lengths. Our model suggests that directional modulation first emerges at the level of muscle forces, augments at the motoneuron level, and further increases at the level of the motor cortex due to the dependence of frictional forces in the joints, contractility of the muscles and afferent feedback on muscle lengths and/or velocities.

Highlights

Even simple arm movements such as reaching require complex interactions among the central and peripheral nervous systems, and skeletal muscles to generate the intended arm movements
The Arm module is modeled as a mechanical system of two rigid segments and two joints controlled by six Hill-type muscles, namely: the shoulder flexor (SF) and extensor (SE), the elbow flexor (EF) and extensor (EE), and the two-joint extensor (BE) and flexor (BF)
We proposed mechanistic explanation of the fact that during planar reaching arm movements directional dependence of time-averaged activity of cortical neurons originates from the anisotropy of average muscle lengths and velocities

Summary

Introduction

Even simple arm movements such as reaching require complex interactions among the central and peripheral nervous systems, and skeletal muscles to generate the intended arm movements. Reaching is broadly defined as the arm’s movement starting at some initial position in space and ending at a target position. In experiments, unperturbed reaching movement usually occurs along a straight-line trajectory with a bellshaped velocity profile [5]. Reaching movements result from complex concurrent or sequential activation patterns of multiple muscles used to accelerate and slow down and stop the arm along the intended trajectory. To generate the required muscle activation patterns, the motor cortex needs to solve a corresponding “inverse problem” and, based on this solution, provide the appropriate dynamical inputs to the spinal circuits [6,7,8]

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