Optimization of modularity during development to simplify walking control across multiple steps
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, toddle...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2024-01-01
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| Series: | Frontiers in Neural Circuits |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fncir.2023.1340298/full |
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| author | Elodie Hinnekens Elodie Hinnekens Bastien Berret Bastien Berret Estelle Morard Estelle Morard Manh-Cuong Do Manh-Cuong Do Marianne Barbu-Roth Caroline Teulier Caroline Teulier |
| author_facet | Elodie Hinnekens Elodie Hinnekens Bastien Berret Bastien Berret Estelle Morard Estelle Morard Manh-Cuong Do Manh-Cuong Do Marianne Barbu-Roth Caroline Teulier Caroline Teulier |
| author_sort | Elodie Hinnekens |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-03-08T11:29:35Z |
| format | Article |
| id | doaj.art-f295203807dd43ebb0c0a6716b91526f |
| institution | Directory Open Access Journal |
| issn | 1662-5110 |
| language | English |
| last_indexed | 2024-03-08T11:29:35Z |
| publishDate | 2024-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neural Circuits |
| spelling | doaj.art-f295203807dd43ebb0c0a6716b91526f2024-01-26T04:28:12ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102024-01-011710.3389/fncir.2023.13402981340298Optimization of modularity during development to simplify walking control across multiple stepsElodie Hinnekens0Elodie Hinnekens1Bastien Berret2Bastien Berret3Estelle Morard4Estelle Morard5Manh-Cuong Do6Manh-Cuong Do7Marianne Barbu-Roth8Caroline Teulier9Caroline Teulier10Université Paris-Saclay, CIAMS, Orsay, FranceUniversité Paris-Saclay, CIAMS, Orléans, FranceUniversité Paris-Saclay, CIAMS, Orsay, FranceUniversité Paris-Saclay, CIAMS, Orléans, FranceUniversité Paris-Saclay, CIAMS, Orsay, FranceUniversité Paris-Saclay, CIAMS, Orléans, FranceUniversité Paris-Saclay, CIAMS, Orsay, FranceUniversité Paris-Saclay, CIAMS, Orléans, FranceUniversité Paris Cité, CNRS, Integrative Neuroscience and Cognition Center, Paris, FranceUniversité Paris-Saclay, CIAMS, Orsay, FranceUniversité Paris-Saclay, CIAMS, Orléans, FranceIntroductionWalking 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.https://www.frontiersin.org/articles/10.3389/fncir.2023.1340298/fulldevelopmentwalkingmuscle synergiesmodularitytoddlersvariability |
| spellingShingle | Elodie Hinnekens Elodie Hinnekens Bastien Berret Bastien Berret Estelle Morard Estelle Morard Manh-Cuong Do Manh-Cuong Do Marianne Barbu-Roth Caroline Teulier Caroline Teulier Optimization of modularity during development to simplify walking control across multiple steps Frontiers in Neural Circuits development walking muscle synergies modularity toddlers variability |
| title | Optimization of modularity during development to simplify walking control across multiple steps |
| title_full | Optimization of modularity during development to simplify walking control across multiple steps |
| title_fullStr | Optimization of modularity during development to simplify walking control across multiple steps |
| title_full_unstemmed | Optimization of modularity during development to simplify walking control across multiple steps |
| title_short | Optimization of modularity during development to simplify walking control across multiple steps |
| title_sort | optimization of modularity during development to simplify walking control across multiple steps |
| topic | development walking muscle synergies modularity toddlers variability |
| url | https://www.frontiersin.org/articles/10.3389/fncir.2023.1340298/full |
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