Motor primitives are determined in early development and are then robustly conserved into adulthood

Abstract

Motor patterns in legged vertebrates show modularity in both young and adult animals, comprising motor synergies or primitives. Are such spinal modules observed in young mammals conserved into adulthood or altered? Conceivably, early circuit modules alter radically through experience and descending pathways' activity. We analyze lumbar motor patterns of intact adult rats and the same rats after spinal transection and compare these with adult rats spinal transected 5 days postnatally, before most motor experience, using only rats that never developed hind limb weight bearing. We use independent component analysis (ICA) to extract synergies from electromyography (EMG). ICA information-based methods identify both weakly active and strongly active synergies. We compare all spatial synergies and their activation/drive strengths as proxies of spinal modules and their underlying circuits. Remarkably, we find that spatial primitives/synergies of adult injured and neonatal injured rats differed insignificantly, despite different developmental histories. However, intact rats possess some synergies that differ significantly, although modestly, in spatial structure. Rats injured as adults were more similar in modularity to rats that had neonatal spinal transection than to themselves before injury. We surmise that spinal circuit modules for spatial synergy patterns may be determined early, before postnatal day 5 (P5), and remain largely unaltered by subsequent development or weight-bearing experience. An alternative explanation but equally important is that, after complete spinal transection, both neonatal and mature adult spinal cords rapidly converge to common synergy sets. This fundamental or convergent synergy circuitry, fully determined by P5, is revealed after spinal cord transection.motor primitives | muscle synergies | pattern generation | spinal cord injury | development M otor patterns can show significant modularity in legged vertebrates. Modularity can take several forms (1). Here, we examine modular motor drives in spinal systems. This approach combines both structural and functional neural components. The fundamental idea is that basic movement is largely composed of small numbers of synergies or motor primitives, which act as building blocks (1-5). Synergies for this study are defined as spatial synergies (1), which each represent a premotor drive to motor pools, causing covarying muscle activity in a specific balance. Such drives could arise from a well-defined neural substrate of sets of neurons with specific premotor connectivity. Indeed, some data in frogs and monkeys support this idea (6, 7). Such modularity could arise as follows: first, directly through evolutionarily determined processes in development; second, through plastic online optimizations during development; third, de novo during motor skill learning; or fourth, via some combinations of these (1,2,4,8). The collection of synergies resulting from any of these processes can form a library of compositional elements useful both for new movement con...

Plasticity of muscle synergies through fractionation and merging during development and training of human runners

“…7c). Recent data from multiple model vertebrates have shown convincingly that locomotor W's and C(t)'s are encoded by spinal interneuronal networks 8,19,44,45 . Results from human survivors of stroke 46,47 and spinal cord injury 48 also partially support the subcortical origin of the locomotor synergies.…”

“…It has been argued that these constraints assume a modular architecture that facilitates the coordination and execution of diverse motor behaviors 6 . Recent studies have shown that for at least some of these modular constraints, called motor primitives or motor modules, their structures appear to be either inborn 7 or determined very early in life 8 . Indeed, many of them remain rather invariant over most of the life span 5,8 or even across species 7 .…”

Distinct locomotor precursors in newborn babies

“…Neurophysiological studies in frogs (2,13,14), mice (15), rats (16,17), cats (18), and monkeys (8) support the idea that the temporal activation patterns and the muscle synergies derived from EMG recordings reflect the output of spinal networks of premotor interneurons. Indeed, the modular EMG organization is preserved after complete spinal cord lesions in animals (19)(20)(21) and humans (22,23).…”

“…They include four main sequential activations of muscle synergies timed at a specific phase of the step cycle, corresponding to limb touch-down, propulsion, lift-off, and swing (7,11,15,17,22,27). While the neuromuscular modules of adult locomotion have been thoroughly investigated (9,17,20,22,28,29), there is still limited knowledge about their development since birth (11,21,30,31). Here we consider the development of human locomotion.…”

Learning compositional sequences with multiple time scales through a hierarchical network of spiking neurons

“…Hierarchical temporal structures might arise during development in a variety of ways (Dominici et al 2011;Yang et al 2019). One way is that a single protosequence is learnt first.…”