Distinct locomotor precursors in newborn babies

Abstract

Mature locomotion involves modular spinal drives generating a set of fundamental patterns of motoneuron activation, each timed at a specific phase of locomotor cycles and associated with a stable muscle synergy. How locomotor modules develop and to what extent they depend on prior experience or intrinsic programs remains unclear. To address these issues, we herein leverage the presence at birth of two types of locomotor-like movements, spontaneous kicking and weight-bearing stepping. The former is expressed thousands of times in utero and postnatally, whereas the latter is elicited de novo by placing the newborn on the ground for the first time. We found that the neuromuscular modules of stepping and kicking differ substantially. Neonates kicked with an adult-like number of temporal activation patterns, which lacked a stable association with systematic muscle synergies across movements. However, on the ground neonates stepped with fewer temporal patterns but all structured in stable synergies. Since kicking and ground-stepping coexist at birth, switching between the two behaviors may depend on a dynamic reconfiguration of the underlying neural circuits as a function of sensory feedback from surface contact. We tracked the development of ground-stepping in 4- to 48-mo-old infants and found that, after the age of 6 mo, the number of temporal patterns increased progressively, reaching adult-like conformation only after independent walking was established. We surmise that mature locomotor modules may derive by combining the multiple patterns of repeated kicking, on the one hand, with synergies resulting from fractionation of those revealed by sporadic weight-bearing stepping, on the other hand.

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

“…For a development untinged by training, gradual fractionations of muscle synergies could be a maturation process that generates control flexibility so that running can be performed under a variety of circumstances 2,31 despite variations of plant properties during development, even though after fractionation running may not be most efficiently executed. Interestingly, synergy fractionation has very recently been demonstrated during the early development of stepping 32 , suggesting that fractionation may contribute to the developmental reorganization of motor patterns for multiple modes of locomotion. After the plant properties stabilize, to run more efficiently training is required to sculpt new motor patterns.…”

Maturation of the Locomotor Circuitry in Children With Cerebral Palsy

“…In sum, how intrinsic spinal locomotor circuits are remodeled after a perinatal brain injury needs to be better understood since they play a key role in locomotor dysfunction in CP and in developing locomotor neuromuscular pattern generation in general, taking into consideration a substantial ongoing reorganization of the locomotor output in TD infants during the first year of life ( Dominici et al, 2011 ; Ivanenko et al, 2013 ; Sylos-Labini et al, 2020 ). Also, the efficacy to repair supraspinal (CST) connections to the spinal cord is strongly reduced after the critical period and is insufficient to restore significant function unless promoted ( Friel et al, 2014 ).…”

“…The development of efficient and independent walking is an important therapeutic goal for children with CP ( Willoughby et al, 2009 ; Smania et al, 2011 ; Degelean et al, 2012 ; Drużbicki et al, 2013 ; Willerslev-Olsen et al, 2015 ; Graham et al, 2016 ; Lerner et al, 2017 ). This may include advances in biotechnology to unveil new information about the impaired locomotor output or infant general movements for the early diagnosis of CP ( Zhu et al, 2015 ; Redd et al, 2019 ; Airaksinen et al, 2020 ; Sylos-Labini et al, 2020 ), to develop central pattern generator-modulating therapies ( Solopova et al, 2017 ) and to enhance walking. For example, initially shown to be effective for mammalian gait retraining (e.g., Barbeau and Rossignol, 1987 ; van den Brand et al, 2015 ; von Zitzewitz et al, 2016 ), a therapeutic intervention for gait retraining with partial body weight support using a harness system ( McNevin et al, 2000 ) or water immersion ( Oliveira et al, 2014 ) may improve walking capacity in children with CP ( Day et al, 2004 ; Azizi et al, 2017 ).…”

Spinal motoneurons of the human newborn are highly synchronized during leg movements

“…Although humans have limited motor abilities at birth, CPGs allow newborns to eat, breathe, and step or kick automatically (7,8). Moreover, neonates are endowed with a set of primitive reflexes involving fast movements, which are important for protection, nutrition, and survival or are simply phylogenetic rudiments (9).…”