Neurons in red nucleus and primary motor cortex exhibit similar responses to mechanical perturbations applied to the upper-limb during posture.

Troy M Herter,Tomohiko Takei,Stephen H Scott,Douglas P Munoz

doi:10.3389/fnint.2015.00029

Troy M Herter, Tomohiko Takei + Show 2 more

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https://doi.org/10.3389/fnint.2015.00029

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Abstract

Primary motor cortex (M1) and red nucleus (RN) are brain regions involved in limb motor control. Both structures are highly interconnected with the cerebellum and project directly to the spinal cord, although the contribution of RN is smaller than M1. It remains uncertain whether RN and M1 serve similar or distinct roles during posture and movement. Many neurons in M1 respond rapidly to mechanical disturbances of the limb, but it remains unclear whether RN neurons also respond to such limb perturbations. We have compared discharges of single neurons in RN (n = 49) and M1 (n = 109) of one monkey during a postural perturbation task. Neural responses to whole-limb perturbations were examined by transiently applying (300 ms) flexor or extensor torques to the shoulder and/or elbow while the monkeys attempted to maintain a static hand posture. Relative to baseline discharges before perturbation onset, perturbations evoked rapid (<100 ms) changes of neural discharges in many RN (28 of 49, 57%) and M1 (43 of 109, 39%) neurons. In addition to exhibiting a greater proportion of perturbation-related neurons, RN neurons also tended to exhibit higher peak discharge frequencies in response to perturbations than M1 neurons. Importantly, neurons in both structures exhibited similar response latencies and tuning properties (preferred torque directions and tuning widths) in joint-torque space. Proximal arm muscles also displayed similar tuning properties in joint-torque space. These results suggest that RN is more sensitive than M1 to mechanical perturbations applied during postural control but both structures may play a similar role in feedback control of posture.

Highlights

IntroductionIt is well established that primary motor cortex (M1) and red nucleus (RN) form parallel pathways for motor control as both structures have axonal projections to the spinal cord including direct connections to motoneurons (Fetz and Cheney, 1980; Buys et al, 1986; Cheney et al, 1991; Mewes and Cheney, 1991, 1994; Belhaj-Saif et al, 1998; McKiernan et al, 1998; Park et al, 2004)
The goal of the present study was to investigate whether mechanical perturbations evoke rapid sensorimotor responses in red nucleus (RN) neurons that are similar to those observed in M1 neurons and upper-limb muscles
Perturbation responses in RN neurons were qualitatively similar to those observed in M1, with broad tuning and preferred torque directions biased towards whole limb flexor torques and whole limb extensor torques

Summary

Introduction

It is well established that primary motor cortex (M1) and red nucleus (RN) form parallel pathways for motor control as both structures have axonal projections to the spinal cord including direct connections to motoneurons (Fetz and Cheney, 1980; Buys et al, 1986; Cheney et al, 1991; Mewes and Cheney, 1991, 1994; Belhaj-Saif et al, 1998; McKiernan et al, 1998; Park et al, 2004). Neural activity M1 is correlated with the timing and magnitude of upper-limb muscle activity (Smith et al, 1975; Bennett and Lemon, 1996; Scott, 1997; Holdefer and Miller, 2002), as is the activity of neurons in RN (Miller et al, 1993; Mewes and Cheney, 1994; Miller and Houk, 1995; Belhaj-Saif et al, 1998; Miller and Sinkjaer, 1998). Neural activity in M1 can reflect either kinematic (motion) or kinetic (forces) features of movement (reviewed in Scott, 2003), a feature that is observed in RN (Kohlerman et al, 1982; Gibson et al, 1985a,b; Kennedy, 1987; Cheney et al, 1988; Mewes and Cheney, 1994). More recent studies suggest that RN may be specialized for controlling grasping movements coupled with reaching (Sinkjaer et al, 1995; van Kan and McCurdy, 2001, 2002a,b)

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