Dual dimensionality reduction reveals independent encoding of motor features in a muscle synergy for insect flight control.

What are the features of movement encoded by changing motor commands? Do motor commands encode movement independently or can they be represented in a reduced set of signals (i.e. synergies)? Motor encoding poses a computational and practical challenge because many muscles typically drive movement, a...

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Main Authors: Simon Sponberg, Thomas L Daniel, Adrienne L Fairhall
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-04-01
Series:PLoS Computational Biology
Online Access:http://europepmc.org/articles/PMC4412410?pdf=render
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author Simon Sponberg
Thomas L Daniel
Adrienne L Fairhall
author_facet Simon Sponberg
Thomas L Daniel
Adrienne L Fairhall
author_sort Simon Sponberg
collection DOAJ
description What are the features of movement encoded by changing motor commands? Do motor commands encode movement independently or can they be represented in a reduced set of signals (i.e. synergies)? Motor encoding poses a computational and practical challenge because many muscles typically drive movement, and simultaneous electrophysiology recordings of all motor commands are typically not available. Moreover, during a single locomotor period (a stride or wingstroke) the variation in movement may have high dimensionality, even if only a few discrete signals activate the muscles. Here, we apply the method of partial least squares (PLS) to extract the encoded features of movement based on the cross-covariance of motor signals and movement. PLS simultaneously decomposes both datasets and identifies only the variation in movement that relates to the specific muscles of interest. We use this approach to explore how the main downstroke flight muscles of an insect, the hawkmoth Manduca sexta, encode torque during yaw turns. We simultaneously record muscle activity and turning torque in tethered flying moths experiencing wide-field visual stimuli. We ask whether this pair of muscles acts as a muscle synergy (a single linear combination of activity) consistent with their hypothesized function of producing a left-right power differential. Alternatively, each muscle might individually encode variation in movement. We show that PLS feature analysis produces an efficient reduction of dimensionality in torque variation within a wingstroke. At first, the two muscles appear to behave as a synergy when we consider only their wingstroke-averaged torque. However, when we consider the PLS features, the muscles reveal independent encoding of torque. Using these features we can predictably reconstruct the variation in torque corresponding to changes in muscle activation. PLS-based feature analysis provides a general two-sided dimensionality reduction that reveals encoding in high dimensional sensory or motor transformations.
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spelling doaj.art-801e689394c34f459fac7664015ca4612022-12-21T18:30:52ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582015-04-01114e100416810.1371/journal.pcbi.1004168Dual dimensionality reduction reveals independent encoding of motor features in a muscle synergy for insect flight control.Simon SponbergThomas L DanielAdrienne L FairhallWhat are the features of movement encoded by changing motor commands? Do motor commands encode movement independently or can they be represented in a reduced set of signals (i.e. synergies)? Motor encoding poses a computational and practical challenge because many muscles typically drive movement, and simultaneous electrophysiology recordings of all motor commands are typically not available. Moreover, during a single locomotor period (a stride or wingstroke) the variation in movement may have high dimensionality, even if only a few discrete signals activate the muscles. Here, we apply the method of partial least squares (PLS) to extract the encoded features of movement based on the cross-covariance of motor signals and movement. PLS simultaneously decomposes both datasets and identifies only the variation in movement that relates to the specific muscles of interest. We use this approach to explore how the main downstroke flight muscles of an insect, the hawkmoth Manduca sexta, encode torque during yaw turns. We simultaneously record muscle activity and turning torque in tethered flying moths experiencing wide-field visual stimuli. We ask whether this pair of muscles acts as a muscle synergy (a single linear combination of activity) consistent with their hypothesized function of producing a left-right power differential. Alternatively, each muscle might individually encode variation in movement. We show that PLS feature analysis produces an efficient reduction of dimensionality in torque variation within a wingstroke. At first, the two muscles appear to behave as a synergy when we consider only their wingstroke-averaged torque. However, when we consider the PLS features, the muscles reveal independent encoding of torque. Using these features we can predictably reconstruct the variation in torque corresponding to changes in muscle activation. PLS-based feature analysis provides a general two-sided dimensionality reduction that reveals encoding in high dimensional sensory or motor transformations.http://europepmc.org/articles/PMC4412410?pdf=render
spellingShingle Simon Sponberg
Thomas L Daniel
Adrienne L Fairhall
Dual dimensionality reduction reveals independent encoding of motor features in a muscle synergy for insect flight control.
PLoS Computational Biology
title Dual dimensionality reduction reveals independent encoding of motor features in a muscle synergy for insect flight control.
title_full Dual dimensionality reduction reveals independent encoding of motor features in a muscle synergy for insect flight control.
title_fullStr Dual dimensionality reduction reveals independent encoding of motor features in a muscle synergy for insect flight control.
title_full_unstemmed Dual dimensionality reduction reveals independent encoding of motor features in a muscle synergy for insect flight control.
title_short Dual dimensionality reduction reveals independent encoding of motor features in a muscle synergy for insect flight control.
title_sort dual dimensionality reduction reveals independent encoding of motor features in a muscle synergy for insect flight control
url http://europepmc.org/articles/PMC4412410?pdf=render
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AT thomasldaniel dualdimensionalityreductionrevealsindependentencodingofmotorfeaturesinamusclesynergyforinsectflightcontrol
AT adriennelfairhall dualdimensionalityreductionrevealsindependentencodingofmotorfeaturesinamusclesynergyforinsectflightcontrol