Spinal control of muscle synergies for adult mammalian locomotion

Abstract

Key points The control of locomotion is thought to be generated by activating groups of muscles that perform similar actions, which are termed muscle synergies. Here, we investigated if muscle synergies are controlled at the level of the spinal cord. We did this by comparing muscle activity in the legs of cats during stepping on a treadmill before and after a complete spinal transection that abolishes commands from the brain. We show that muscle synergies were maintained following spinal transection, validating the concept that muscle synergies for locomotion are primarily controlled by circuits of neurons within the spinal cord. Abstract Locomotion is thought to involve the sequential activation of functional modules or muscle synergies. Here, we tested the hypothesis that muscle synergies for locomotion are organized within the spinal cord. We recorded bursts of muscle activity in the same cats (n = 7) before and after spinal transection during tied‐belt locomotion at three speeds and split‐belt locomotion at three left–right speed differences. We identified seven muscles synergies before (intact state) and after (spinal state) spinal transection. The muscles comprising the different synergies were the same in the intact and spinal states as well as at different speeds or left–right speed differences. However, there were some significant shifts in the onsets and offsets of certain synergies as a function of state, speed and left–right speed differences. The most notable difference between the intact and spinal states was a change in the timing between the knee flexor and hip flexor muscle synergies. In the intact state, the knee flexor synergy preceded the hip flexor synergy, whereas in the spinal state both synergies occurred concurrently. Afferent inputs also appear important for the expression of some muscle synergies, specifically those involving biphasic patterns of muscle activity. We propose that muscle synergies for locomotion are primarily organized within the spinal cord, although their full expression and proper timing requires inputs from supraspinal structures and/or limb afferents.

Muscular Activity Modulation During Post-operative Walking With Hybrid Assistive Limb (HAL) in a Patient With Thoracic Myelopathy Due to Ossification of Posterior Longitudinal Ligament: A Case Report

“…Lack of muscle synergies corresponding to posture control is known in spinalized cats (76). The neural implementation of muscle synergies is reported as being housed in the spinal cord (44,77), and the brain is also considered as forming a spatiotemporal pattern of synergies (45). Considering these evidences, increased synergies during walking with HAL suggest, first, that the spinal control of gait is altered with HAL and, second, the myelopathic spinal cord of the patient is activated with HAL to deal with more degrees of control in view / t h g i R ( s u m i x a M s u e t u l G ) t f e L / t h g i R ( s i l a i d e M s u t s a V 11 12 of the simplified synergies of neurological patients (47,51,75,78), together with the adapted activity of the supraspinal networks utilizing the increased synergy of the spinal cord to control gait (36,46).…”

Functional convergence of autonomic and sensorimotor processing in the lateral cerebellum

“…It is known that different rhythmic behaviors can be controlled as muscle synergies by local networks. For instance, coordination between the left and right hind-limb can still take place during locomotion even after the descending connections from the motor cortex and brainstem to the spinal cord are disrupted (Desrochers et al, 2019). Likewise, when cerebellar function is impaired, the basic muscle activities of breathing and related orofacial behaviors can still take place up to a degree (Chen et al, 2005; Abecassis et al, 2017; Bellavance et al, 2017).…”

Modularity in the intact and spinal cat: methods, issues and questions for the future

“…In summary, Desrochers and colleagues () have established a very important set of results, and thereby they have also made more acute the need for fuller answers as to their neural bases, how spinal synergies are first constructed, how they are modified through development, if and how they are used in motor skill construction, and when and how a mammal instead abandons them and strikes out with completely novel muscle compositions. These issues are crucial for application of modularity analyses systematically in neurological disorders such as SCI.…”

“…The paper by Etienne Desrochers and colleagues from the Frigon lab, published in the current issue of The Journal of Physiology (Desrochers et al 2019), is an important contribution. They provide a clear demonstration of a synergy organization in the spinal cord of the cat that is closely similar before and after spinal transection, using the methods of Krouchev and colleagues (2006) of direct component analysis (DCA).…”

“…The data and analysis are excellent demonstrations of spinal synergy structures conserved after spinal cord injury (SCI). Testing over variations in conditions to demonstrate robustness of synergy is a critical feature of the data provided in the work of Desrochers et al 2019. Beyond pattern generation, it now appears that modularity of pattern construction is also likely to be fundamental, and robust to perturbations.…”