Corollary discharge enables proprioception from lateral line sensory feedback.

Animals modulate sensory processing in concert with motor actions. Parallel copies of motor signals, called corollary discharge (CD), prepare the nervous system to process the mixture of externally and self-generated (reafferent) feedback that arises during locomotion. Commonly, CD in the peripheral...

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Autores principales:	Dimitri A Skandalis, Elias T Lunsford, James C Liao
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/cb4a01dc50534a75b53e6e4f9c89e9e8
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id	oai:doaj.org-article:cb4a01dc50534a75b53e6e4f9c89e9e8
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spelling	oai:doaj.org-article:cb4a01dc50534a75b53e6e4f9c89e9e82021-11-25T05:34:16ZCorollary discharge enables proprioception from lateral line sensory feedback.1544-91731545-788510.1371/journal.pbio.3001420https://doaj.org/article/cb4a01dc50534a75b53e6e4f9c89e9e82021-10-01T00:00:00Zhttps://doi.org/10.1371/journal.pbio.3001420https://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Animals modulate sensory processing in concert with motor actions. Parallel copies of motor signals, called corollary discharge (CD), prepare the nervous system to process the mixture of externally and self-generated (reafferent) feedback that arises during locomotion. Commonly, CD in the peripheral nervous system cancels reafference to protect sensors and the central nervous system from being fatigued and overwhelmed by self-generated feedback. However, cancellation also limits the feedback that contributes to an animal's awareness of its body position and motion within the environment, the sense of proprioception. We propose that, rather than cancellation, CD to the fish lateral line organ restructures reafference to maximize proprioceptive information content. Fishes' undulatory body motions induce reafferent feedback that can encode the body's instantaneous configuration with respect to fluid flows. We combined experimental and computational analyses of swimming biomechanics and hair cell physiology to develop a neuromechanical model of how fish can track peak body curvature, a key signature of axial undulatory locomotion. Without CD, this computation would be challenged by sensory adaptation, typified by decaying sensitivity and phase distortions with respect to an input stimulus. We find that CD interacts synergistically with sensor polarization to sharpen sensitivity along sensors' preferred axes. The sharpening of sensitivity regulates spiking to a narrow interval coinciding with peak reafferent stimulation, which prevents adaptation and homogenizes the otherwise variable sensor output. Our integrative model reveals a vital role of CD for ensuring precise proprioceptive feedback during undulatory locomotion, which we term external proprioception.Dimitri A SkandalisElias T LunsfordJames C LiaoPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 19, Iss 10, p e3001420 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Dimitri A Skandalis Elias T Lunsford James C Liao Corollary discharge enables proprioception from lateral line sensory feedback.
description	Animals modulate sensory processing in concert with motor actions. Parallel copies of motor signals, called corollary discharge (CD), prepare the nervous system to process the mixture of externally and self-generated (reafferent) feedback that arises during locomotion. Commonly, CD in the peripheral nervous system cancels reafference to protect sensors and the central nervous system from being fatigued and overwhelmed by self-generated feedback. However, cancellation also limits the feedback that contributes to an animal's awareness of its body position and motion within the environment, the sense of proprioception. We propose that, rather than cancellation, CD to the fish lateral line organ restructures reafference to maximize proprioceptive information content. Fishes' undulatory body motions induce reafferent feedback that can encode the body's instantaneous configuration with respect to fluid flows. We combined experimental and computational analyses of swimming biomechanics and hair cell physiology to develop a neuromechanical model of how fish can track peak body curvature, a key signature of axial undulatory locomotion. Without CD, this computation would be challenged by sensory adaptation, typified by decaying sensitivity and phase distortions with respect to an input stimulus. We find that CD interacts synergistically with sensor polarization to sharpen sensitivity along sensors' preferred axes. The sharpening of sensitivity regulates spiking to a narrow interval coinciding with peak reafferent stimulation, which prevents adaptation and homogenizes the otherwise variable sensor output. Our integrative model reveals a vital role of CD for ensuring precise proprioceptive feedback during undulatory locomotion, which we term external proprioception.
format	article
author	Dimitri A Skandalis Elias T Lunsford James C Liao
author_facet	Dimitri A Skandalis Elias T Lunsford James C Liao
author_sort	Dimitri A Skandalis
title	Corollary discharge enables proprioception from lateral line sensory feedback.
title_short	Corollary discharge enables proprioception from lateral line sensory feedback.
title_full	Corollary discharge enables proprioception from lateral line sensory feedback.
title_fullStr	Corollary discharge enables proprioception from lateral line sensory feedback.
title_full_unstemmed	Corollary discharge enables proprioception from lateral line sensory feedback.
title_sort	corollary discharge enables proprioception from lateral line sensory feedback.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/cb4a01dc50534a75b53e6e4f9c89e9e8
work_keys_str_mv	AT dimitriaskandalis corollarydischargeenablesproprioceptionfromlaterallinesensoryfeedback AT eliastlunsford corollarydischargeenablesproprioceptionfromlaterallinesensoryfeedback AT jamescliao corollarydischargeenablesproprioceptionfromlaterallinesensoryfeedback
_version_	1718414604298616832

Corollary discharge enables proprioception from lateral line sensory feedback.

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