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From retina to motoneurons: A substrate for visuomotor transformation in salamanders

The transformation of visual input into motor output is essential to approach a target or avoid a predator. In salamanders, visually guided orientation behaviors have been extensively studied during prey capture. However, the neural circuitry involved is not resolved. Using salamander brain preparat...

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Detalles Bibliográficos
Autores principales: Flaive, Aurélie, Ryczko, Dimitri
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9545292/
https://www.ncbi.nlm.nih.gov/pubmed/35662021
http://dx.doi.org/10.1002/cne.25348
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author Flaive, Aurélie
Ryczko, Dimitri
author_facet Flaive, Aurélie
Ryczko, Dimitri
author_sort Flaive, Aurélie
collection PubMed
description The transformation of visual input into motor output is essential to approach a target or avoid a predator. In salamanders, visually guided orientation behaviors have been extensively studied during prey capture. However, the neural circuitry involved is not resolved. Using salamander brain preparations, calcium imaging and tracing experiments, we describe a neural substrate through which retinal input is transformed into spinal motor output. We found that retina stimulation evoked responses in reticulospinal neurons of the middle reticular nucleus, known to control steering movements in salamanders. Microinjection of glutamatergic antagonists in the optic tectum (superior colliculus in mammals) decreased the reticulospinal responses. Using tracing, we found that retina projected to the dorsal layers of the contralateral tectum, where the dendrites of neurons projecting to the middle reticular nucleus were located. In slices, stimulation of the tectal dorsal layers evoked glutamatergic responses in deep tectal neurons retrogradely labeled from the middle reticular nucleus. We then examined how tectum activation translated into spinal motor output. Tectum stimulation evoked motoneuronal responses, which were decreased by microinjections of glutamatergic antagonists in the contralateral middle reticular nucleus. Reticulospinal fibers anterogradely labeled from tracer injection in the middle reticular nucleus were preferentially distributed in proximity with the dendrites of ipsilateral motoneurons. Our work establishes a neural substrate linking visual and motor centers in salamanders. This retino‐tecto‐reticulo‐spinal circuitry is well positioned to control orienting behaviors. Our study bridges the gap between the behavioral studies and the neural mechanisms involved in the transformation of visual input into motor output in salamanders.
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spelling pubmed-95452922022-10-14 From retina to motoneurons: A substrate for visuomotor transformation in salamanders Flaive, Aurélie Ryczko, Dimitri J Comp Neurol Research Articles The transformation of visual input into motor output is essential to approach a target or avoid a predator. In salamanders, visually guided orientation behaviors have been extensively studied during prey capture. However, the neural circuitry involved is not resolved. Using salamander brain preparations, calcium imaging and tracing experiments, we describe a neural substrate through which retinal input is transformed into spinal motor output. We found that retina stimulation evoked responses in reticulospinal neurons of the middle reticular nucleus, known to control steering movements in salamanders. Microinjection of glutamatergic antagonists in the optic tectum (superior colliculus in mammals) decreased the reticulospinal responses. Using tracing, we found that retina projected to the dorsal layers of the contralateral tectum, where the dendrites of neurons projecting to the middle reticular nucleus were located. In slices, stimulation of the tectal dorsal layers evoked glutamatergic responses in deep tectal neurons retrogradely labeled from the middle reticular nucleus. We then examined how tectum activation translated into spinal motor output. Tectum stimulation evoked motoneuronal responses, which were decreased by microinjections of glutamatergic antagonists in the contralateral middle reticular nucleus. Reticulospinal fibers anterogradely labeled from tracer injection in the middle reticular nucleus were preferentially distributed in proximity with the dendrites of ipsilateral motoneurons. Our work establishes a neural substrate linking visual and motor centers in salamanders. This retino‐tecto‐reticulo‐spinal circuitry is well positioned to control orienting behaviors. Our study bridges the gap between the behavioral studies and the neural mechanisms involved in the transformation of visual input into motor output in salamanders. John Wiley and Sons Inc. 2022-06-03 2022-10 /pmc/articles/PMC9545292/ /pubmed/35662021 http://dx.doi.org/10.1002/cne.25348 Text en © 2022 The Authors. The Journal of Comparative Neurology published by Wiley Periodicals LLC. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Flaive, Aurélie
Ryczko, Dimitri
From retina to motoneurons: A substrate for visuomotor transformation in salamanders
title From retina to motoneurons: A substrate for visuomotor transformation in salamanders
title_full From retina to motoneurons: A substrate for visuomotor transformation in salamanders
title_fullStr From retina to motoneurons: A substrate for visuomotor transformation in salamanders
title_full_unstemmed From retina to motoneurons: A substrate for visuomotor transformation in salamanders
title_short From retina to motoneurons: A substrate for visuomotor transformation in salamanders
title_sort from retina to motoneurons: a substrate for visuomotor transformation in salamanders
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9545292/
https://www.ncbi.nlm.nih.gov/pubmed/35662021
http://dx.doi.org/10.1002/cne.25348
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