Contribution of Afferent Feedback to Adaptive Hindlimb Walking in Cats: A Neuromusculoskeletal Modeling Study

Mammalian locomotion is generated by central pattern generators (CPGs) in the spinal cord, which produce alternating flexor and extensor activities controlling the locomotor movements of each limb. Afferent feedback signals from the limbs are integrated by the CPGs to provide adaptive control of loc...

Full description

Bibliographic Details
Main Authors: Yongi Kim, Shinya Aoi, Soichiro Fujiki, Simon M. Danner, Sergey N. Markin, Jessica Ausborn, Ilya A. Rybak, Dai Yanagihara, Kei Senda, Kazuo Tsuchiya
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-04-01
Series:Frontiers in Bioengineering and Biotechnology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fbioe.2022.825149/full
_version_ 1818366592778502144
author Yongi Kim
Shinya Aoi
Soichiro Fujiki
Simon M. Danner
Sergey N. Markin
Jessica Ausborn
Ilya A. Rybak
Dai Yanagihara
Kei Senda
Kazuo Tsuchiya
author_facet Yongi Kim
Shinya Aoi
Soichiro Fujiki
Simon M. Danner
Sergey N. Markin
Jessica Ausborn
Ilya A. Rybak
Dai Yanagihara
Kei Senda
Kazuo Tsuchiya
author_sort Yongi Kim
collection DOAJ
description Mammalian locomotion is generated by central pattern generators (CPGs) in the spinal cord, which produce alternating flexor and extensor activities controlling the locomotor movements of each limb. Afferent feedback signals from the limbs are integrated by the CPGs to provide adaptive control of locomotion. Responses of CPG-generated neural activity to afferent feedback stimulation have been previously studied during fictive locomotion in immobilized cats. Yet, locomotion in awake, behaving animals involves dynamic interactions between central neuronal circuits, afferent feedback, musculoskeletal system, and environment. To study these complex interactions, we developed a model simulating interactions between a half-center CPG and the musculoskeletal system of a cat hindlimb. Then, we analyzed the role of afferent feedback in the locomotor adaptation from a dynamic viewpoint using the methods of dynamical systems theory and nullcline analysis. Our model reproduced limb movements during regular cat walking as well as adaptive changes of these movements when the foot steps into a hole. The model generates important insights into the mechanism for adaptive locomotion resulting from dynamic interactions between the CPG-based neural circuits, the musculoskeletal system, and the environment.
first_indexed 2024-12-13T22:38:37Z
format Article
id doaj.art-2edbff31f39544258a077b846c691a94
institution Directory Open Access Journal
issn 2296-4185
language English
last_indexed 2024-12-13T22:38:37Z
publishDate 2022-04-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Bioengineering and Biotechnology
spelling doaj.art-2edbff31f39544258a077b846c691a942022-12-21T23:28:55ZengFrontiers Media S.A.Frontiers in Bioengineering and Biotechnology2296-41852022-04-011010.3389/fbioe.2022.825149825149Contribution of Afferent Feedback to Adaptive Hindlimb Walking in Cats: A Neuromusculoskeletal Modeling StudyYongi Kim0Shinya Aoi1Soichiro Fujiki2Simon M. Danner3Sergey N. Markin4Jessica Ausborn5Ilya A. Rybak6Dai Yanagihara7Kei Senda8Kazuo Tsuchiya9Department of Aeronautics and Astronautics, Graduate School of Engineering, Kyoto University, Kyoto Daigaku-Katsura, Kyoto, JapanDepartment of Aeronautics and Astronautics, Graduate School of Engineering, Kyoto University, Kyoto Daigaku-Katsura, Kyoto, JapanDepartment of Physiology, School of Medicine, Dokkyo Medical University, Tochigi, JapanDepartment of Neurobiology and Anatomy, Drexel University College of Medicine, Philadelphia, PA, United StatesDepartment of Neurobiology and Anatomy, Drexel University College of Medicine, Philadelphia, PA, United StatesDepartment of Neurobiology and Anatomy, Drexel University College of Medicine, Philadelphia, PA, United StatesDepartment of Neurobiology and Anatomy, Drexel University College of Medicine, Philadelphia, PA, United StatesDepartment of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, JapanDepartment of Aeronautics and Astronautics, Graduate School of Engineering, Kyoto University, Kyoto Daigaku-Katsura, Kyoto, JapanDepartment of Aeronautics and Astronautics, Graduate School of Engineering, Kyoto University, Kyoto Daigaku-Katsura, Kyoto, JapanMammalian locomotion is generated by central pattern generators (CPGs) in the spinal cord, which produce alternating flexor and extensor activities controlling the locomotor movements of each limb. Afferent feedback signals from the limbs are integrated by the CPGs to provide adaptive control of locomotion. Responses of CPG-generated neural activity to afferent feedback stimulation have been previously studied during fictive locomotion in immobilized cats. Yet, locomotion in awake, behaving animals involves dynamic interactions between central neuronal circuits, afferent feedback, musculoskeletal system, and environment. To study these complex interactions, we developed a model simulating interactions between a half-center CPG and the musculoskeletal system of a cat hindlimb. Then, we analyzed the role of afferent feedback in the locomotor adaptation from a dynamic viewpoint using the methods of dynamical systems theory and nullcline analysis. Our model reproduced limb movements during regular cat walking as well as adaptive changes of these movements when the foot steps into a hole. The model generates important insights into the mechanism for adaptive locomotion resulting from dynamic interactions between the CPG-based neural circuits, the musculoskeletal system, and the environment.https://www.frontiersin.org/articles/10.3389/fbioe.2022.825149/fullwalkingcatneuromusculoskeletal modelcentral pattern generatorafferent feedback
spellingShingle Yongi Kim
Shinya Aoi
Soichiro Fujiki
Simon M. Danner
Sergey N. Markin
Jessica Ausborn
Ilya A. Rybak
Dai Yanagihara
Kei Senda
Kazuo Tsuchiya
Contribution of Afferent Feedback to Adaptive Hindlimb Walking in Cats: A Neuromusculoskeletal Modeling Study
Frontiers in Bioengineering and Biotechnology
walking
cat
neuromusculoskeletal model
central pattern generator
afferent feedback
title Contribution of Afferent Feedback to Adaptive Hindlimb Walking in Cats: A Neuromusculoskeletal Modeling Study
title_full Contribution of Afferent Feedback to Adaptive Hindlimb Walking in Cats: A Neuromusculoskeletal Modeling Study
title_fullStr Contribution of Afferent Feedback to Adaptive Hindlimb Walking in Cats: A Neuromusculoskeletal Modeling Study
title_full_unstemmed Contribution of Afferent Feedback to Adaptive Hindlimb Walking in Cats: A Neuromusculoskeletal Modeling Study
title_short Contribution of Afferent Feedback to Adaptive Hindlimb Walking in Cats: A Neuromusculoskeletal Modeling Study
title_sort contribution of afferent feedback to adaptive hindlimb walking in cats a neuromusculoskeletal modeling study
topic walking
cat
neuromusculoskeletal model
central pattern generator
afferent feedback
url https://www.frontiersin.org/articles/10.3389/fbioe.2022.825149/full
work_keys_str_mv AT yongikim contributionofafferentfeedbacktoadaptivehindlimbwalkingincatsaneuromusculoskeletalmodelingstudy
AT shinyaaoi contributionofafferentfeedbacktoadaptivehindlimbwalkingincatsaneuromusculoskeletalmodelingstudy
AT soichirofujiki contributionofafferentfeedbacktoadaptivehindlimbwalkingincatsaneuromusculoskeletalmodelingstudy
AT simonmdanner contributionofafferentfeedbacktoadaptivehindlimbwalkingincatsaneuromusculoskeletalmodelingstudy
AT sergeynmarkin contributionofafferentfeedbacktoadaptivehindlimbwalkingincatsaneuromusculoskeletalmodelingstudy
AT jessicaausborn contributionofafferentfeedbacktoadaptivehindlimbwalkingincatsaneuromusculoskeletalmodelingstudy
AT ilyaarybak contributionofafferentfeedbacktoadaptivehindlimbwalkingincatsaneuromusculoskeletalmodelingstudy
AT daiyanagihara contributionofafferentfeedbacktoadaptivehindlimbwalkingincatsaneuromusculoskeletalmodelingstudy
AT keisenda contributionofafferentfeedbacktoadaptivehindlimbwalkingincatsaneuromusculoskeletalmodelingstudy
AT kazuotsuchiya contributionofafferentfeedbacktoadaptivehindlimbwalkingincatsaneuromusculoskeletalmodelingstudy