Optimization of modularity during development to simplify walking control across multiple steps

Abstract

Introduction: Walking in adults relies on a small number of modules, reducing the number of degrees of freedom that needs to be regulated by the central nervous system (CNS). While walking in toddlers seems to also involve a small number of modules when considering averaged or single-step data, toddlers produce a high amount of variability across strides, and the extent to which this variability interacts with modularity remains unclear.

Methods: Electromyographic activity from 10 bilateral lower limb muscles was recorded in both adults (n = 12) and toddlers (n = 12) over 8 gait cycles. Toddlers were recorded while walking independently and while being supported by an adult. This condition was implemented to assess if motor variability persisted with reduced balance constraints, suggesting a potential central origin rather than reliance on peripheral regulations. We used non-negative matrix factorization to model the underlying modular command with the Space-by-Time Decomposition method, with or without averaging data, and compared the modular organization of toddlers and adults during multiple walking strides.

Results: Toddlers were more variable in both conditions (i.e. independent walking and supported by an adult) and required significantly more modules to account for their greater stride-by-stride variability. Activations of these modules varied more across strides and were less parsimonious compared to adults, even with diminished balance constraints.

Discussion: The findings suggest that modular control of locomotion evolves between toddlerhood and adulthood as the organism develops and practices. Adults seem to be able to generate several strides of walking with less modules than toddlers. The persistence of variability in toddlers when balance constraints were lowered suggests a link with the ability to explore rather than with corrective mechanisms. In conclusion, the capacity of new walkers to flexibly activate their motor command suggests a broader range of possible actions, though distinguishing between modular and non-modular inputs remains challenging.

Keywords: development; modularity; muscle synergies; toddlers; variability; walking.