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

IF 3.4 3区医学 Q2 NEUROSCIENCES

Frontiers in Neural Circuits Pub Date : 2024-01-26 DOI:10.3389/fncir.2023.1340298

Elodie Hinnekens, Bastien Berret, Estelle Morard, Manh-Cuong Do, Marianne Barbu-Roth, Caroline Teulier

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Abstract

IntroductionWalking 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.MethodsElectromyographic 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.ResultsToddlers 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.DiscussionThe 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.

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在开发过程中优化模块化，简化多个步骤的行走控制

导言成人的行走依赖于少量模块，从而减少了需要由中枢神经系统（CNS）调节的自由度数量。方法记录了成人（12 人）和幼儿（12 人）在 8 个步态周期中 10 块双侧下肢肌肉的肌电图活动。幼儿在独立行走和由成人搀扶的情况下接受记录。采用这种条件是为了评估运动变异性是否会随着平衡限制的减少而持续存在，这表明运动变异性可能来源于中枢，而不是依赖于外周调节。我们使用非负矩阵因式分解法（Space-by-Time Decomposition method）对基本模块指令进行建模，并比较了幼儿和成人在多步行走过程中的模块组织。讨论研究结果表明，随着机体的发育和实践，运动的模块化控制在幼儿期和成年期之间不断演变。与学步儿童相比，成人似乎可以用较少的模块产生几步的行走。当平衡限制降低时，学步儿童的可变性仍然存在，这表明这与探索能力有关，而不是与矫正机制有关。总之，初学走路者灵活启动运动指令的能力表明，可能的行动范围更广，但区分模块化和非模块化输入仍具有挑战性。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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来源期刊

Frontiers in Neural Circuits NEUROSCIENCES-

CiteScore

6.00

自引率

5.70%

发文量

135

审稿时长

4-8 weeks

期刊介绍： Frontiers in Neural Circuits publishes rigorously peer-reviewed research on the emergent properties of neural circuits - the elementary modules of the brain. Specialty Chief Editors Takao K. Hensch and Edward Ruthazer at Harvard University and McGill University respectively, are supported by an outstanding Editorial Board of international experts. This multidisciplinary open-access journal is at the forefront of disseminating and communicating scientific knowledge and impactful discoveries to researchers, academics and the public worldwide. Frontiers in Neural Circuits launched in 2011 with great success and remains a "central watering hole" for research in neural circuits, serving the community worldwide to share data, ideas and inspiration. Articles revealing the anatomy, physiology, development or function of any neural circuitry in any species (from sponges to humans) are welcome. Our common thread seeks the computational strategies used by different circuits to link their structure with function (perceptual, motor, or internal), the general rules by which they operate, and how their particular designs lead to the emergence of complex properties and behaviors. Submissions focused on synaptic, cellular and connectivity principles in neural microcircuits using multidisciplinary approaches, especially newer molecular, developmental and genetic tools, are encouraged. Studies with an evolutionary perspective to better understand how circuit design and capabilities evolved to produce progressively more complex properties and behaviors are especially welcome. The journal is further interested in research revealing how plasticity shapes the structural and functional architecture of neural circuits.