Edge Computing in Nature: Minimal pre-processing of multi-muscle ensembles of spindle signals improves discriminability of limb movements

Multiple proprioceptive signals, like those from muscle spindles, are thought to enable robust estimates of body configuration. Yet, it remains unknown whether spindle signals suffice to discriminate limb movements. Here, a simulated 4-musculotendon, 2-joint planar limb model produced repeated cycle...

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Main Authors: Jasmine A. Berry, Ali Marjaninejad, Francisco J. Valero-Cuevas
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-06-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2023.1183492/full
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author Jasmine A. Berry
Ali Marjaninejad
Francisco J. Valero-Cuevas
Francisco J. Valero-Cuevas
Francisco J. Valero-Cuevas
author_facet Jasmine A. Berry
Ali Marjaninejad
Francisco J. Valero-Cuevas
Francisco J. Valero-Cuevas
Francisco J. Valero-Cuevas
author_sort Jasmine A. Berry
collection DOAJ
description Multiple proprioceptive signals, like those from muscle spindles, are thought to enable robust estimates of body configuration. Yet, it remains unknown whether spindle signals suffice to discriminate limb movements. Here, a simulated 4-musculotendon, 2-joint planar limb model produced repeated cycles of five end-point trajectories in forward and reverse directions, which generated spindle Ia and II afferent signals (proprioceptors for velocity and length, respectively) from each musculotendon. We find that cross-correlation of the 8D time series of raw firing rates (four Ia, four II) cannot discriminate among most movement pairs (∼ 29% accuracy). However, projecting these signals onto their 1st and 2nd principal components greatly improves discriminability of movement pairs (82% accuracy). We conclude that high-dimensional ensembles of muscle proprioceptors can discriminate among limb movements—but only after dimensionality reduction. This may explain the pre-processing of some afferent signals before arriving at the somatosensory cortex, such as processing of cutaneous signals at the cat’s cuneate nucleus.
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spelling doaj.art-76e4bd052fef4463938683ef7a4b32d72023-06-30T09:25:46ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2023-06-011410.3389/fphys.2023.11834921183492Edge Computing in Nature: Minimal pre-processing of multi-muscle ensembles of spindle signals improves discriminability of limb movementsJasmine A. Berry0Ali Marjaninejad1Francisco J. Valero-Cuevas2Francisco J. Valero-Cuevas3Francisco J. Valero-Cuevas4Brain-Body Dynamics Lab, Department of Computer Science, University of Southern California, Los Angeles, CA, United StatesDepartment of Biomedical Engineering, University of Southern California, Los Angeles, CA, United StatesBrain-Body Dynamics Lab, Department of Computer Science, University of Southern California, Los Angeles, CA, United StatesDepartment of Biomedical Engineering, University of Southern California, Los Angeles, CA, United StatesDivision of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA, United StatesMultiple proprioceptive signals, like those from muscle spindles, are thought to enable robust estimates of body configuration. Yet, it remains unknown whether spindle signals suffice to discriminate limb movements. Here, a simulated 4-musculotendon, 2-joint planar limb model produced repeated cycles of five end-point trajectories in forward and reverse directions, which generated spindle Ia and II afferent signals (proprioceptors for velocity and length, respectively) from each musculotendon. We find that cross-correlation of the 8D time series of raw firing rates (four Ia, four II) cannot discriminate among most movement pairs (∼ 29% accuracy). However, projecting these signals onto their 1st and 2nd principal components greatly improves discriminability of movement pairs (82% accuracy). We conclude that high-dimensional ensembles of muscle proprioceptors can discriminate among limb movements—but only after dimensionality reduction. This may explain the pre-processing of some afferent signals before arriving at the somatosensory cortex, such as processing of cutaneous signals at the cat’s cuneate nucleus.https://www.frontiersin.org/articles/10.3389/fphys.2023.1183492/fullmuscle spindle afferentproprioceptionlimb movementtask discriminationdimensionality reductionmusculotendon
spellingShingle Jasmine A. Berry
Ali Marjaninejad
Francisco J. Valero-Cuevas
Francisco J. Valero-Cuevas
Francisco J. Valero-Cuevas
Edge Computing in Nature: Minimal pre-processing of multi-muscle ensembles of spindle signals improves discriminability of limb movements
Frontiers in Physiology
muscle spindle afferent
proprioception
limb movement
task discrimination
dimensionality reduction
musculotendon
title Edge Computing in Nature: Minimal pre-processing of multi-muscle ensembles of spindle signals improves discriminability of limb movements
title_full Edge Computing in Nature: Minimal pre-processing of multi-muscle ensembles of spindle signals improves discriminability of limb movements
title_fullStr Edge Computing in Nature: Minimal pre-processing of multi-muscle ensembles of spindle signals improves discriminability of limb movements
title_full_unstemmed Edge Computing in Nature: Minimal pre-processing of multi-muscle ensembles of spindle signals improves discriminability of limb movements
title_short Edge Computing in Nature: Minimal pre-processing of multi-muscle ensembles of spindle signals improves discriminability of limb movements
title_sort edge computing in nature minimal pre processing of multi muscle ensembles of spindle signals improves discriminability of limb movements
topic muscle spindle afferent
proprioception
limb movement
task discrimination
dimensionality reduction
musculotendon
url https://www.frontiersin.org/articles/10.3389/fphys.2023.1183492/full
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