Primary motor cortical neurons encode functional muscle synergies

Abstract

Many different kinematic and kinetic signals have been proposed as possible variables under the control of the primary motor cortex. Despite the presence of direct projections to motor neurons, muscle activation has received less attention as a controlled variable. Furthermore, although it is well known that descending fibers project to multiple motor pools, an objective, quantitative study of the relation between neuronal modulation and the activity of groups of muscles has not previously been reported. We have recorded the discharge of 310 neurons located in the primary motor cortex of two monkeys, along with the activity of a variety of arm and hand muscles. Data were recorded while the monkey reached to and pressed a series of illuminated buttons. The similarity of a given neuron's discharge with respect to each muscle was determined by calculating the linear cross-correlation between its discharge rate and each rectified, filtered electromyogram. A "functional linkage vector" was then constructed, which expressed the similarity of that neuron's discharge to the entire set of muscles. We discovered discrete groups of functional linkage vectors within the high order muscle space for both monkeys which corresponded to functional properties of the neurons measured by other methods. Several of these groups appeared to represent a functional synergy of muscles, such as those required to extend the limb, press a button, or open the hand in preparation for the press. When the dimensionality of this space was reduced by a principal components analysis, the originally identified clusters of neurons remained well separated. These results are consistent with the hypothesis that the discharge of individual neurons in the primary motor cortex encodes the activity of a relatively small number of functionally relevant groups of muscles. It will be important to determine whether these results will also apply to more complex behavior, and to what extent these functional muscle synergy representations remain fixed across behaviors.

Modelling the control of interceptive actions

“…monoarticular flexor and biarticular extensor), which would have been equally valid from a FLETE perspective and is also consistent with the existence of single corticospinal projections to ␣-motor neurons of several muscles (e.g. McKiernan et al 1998;Holdefer & Miller 2002) as well as with the spinal coding of muscle synergies defined in terms of their angular equilibrium point (e.g. Bizzi et al 1991;Saltiel et al 2001).…”

Evidence of muscle synergies during human grasping

“…Still, although some constraints on the musculotendon system, as well as on the peripheral and central neural system, can be identified, a clear relationship between the finger kinematic constraints and the underlying muscular activity remains to be analysed. As a matter of fact, the source of such kinematic synergies in the human hand remains a matter of debate; indeed, the biomechanical structure of the hand, in which tendons activate multiple digits at the same time, while the related muscles share common bases, is one source for the synergies (see, e.g., [23]); but also the spinal circuitry, mapped only to a small extent to the human hand, co-activates muscles and thus defines synergies [32]; and at the highest level, cortical organisation [21] is suspected to play a dominant but variable role in these.…”

Control of Fast-Reaching Movements by Muscle Synergy Combinations

“…One possibility is that the supraspinal structures recruit and modulate spinally organized synergies (Lukashin et al, 1996;Todorov, 2000) through descending low-dimensional synergy control signals that diverge and are temporally patterned in the spinal network. Either a dedicated spinal circuitry or the same spinal circuitry involved in the generation of rhythmical arm movements (Zehr and Hundza, 2005) might be responsible for this transformation; however, the pyramidal cells in the motor areas of the cerebral cortex influence (Fetz and Cheney, 1980;McKiernan et al, 1998;Park et al, 2004) or are related to (Holdefer and Miller, 2002) multiple muscles and are interconnected thorough intracortical collaterals (Huntley and Jones, 1991;Schneider et al, 2002). Thus muscle synergies also might be directly encoded by the intrinsic and corticospinal pattern of connectivity of pyramidal cells in the cortex.…”