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A synaptic corollary discharge signal suppresses midbrain visual processing during saccade-like locomotion

In motor control, the brain not only sends motor commands to the periphery, but also generates concurrent internal signals known as corollary discharge (CD) that influence sensory information processing around the time of movement. CD signals are important for identifying sensory input arising from...

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Autores principales: Ali, Mir Ahsan, Lischka, Katharina, Preuss, Stephanie J., Trivedi, Chintan A., Bollmann, Johann H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10667368/
https://www.ncbi.nlm.nih.gov/pubmed/37996414
http://dx.doi.org/10.1038/s41467-023-43255-6
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author Ali, Mir Ahsan
Lischka, Katharina
Preuss, Stephanie J.
Trivedi, Chintan A.
Bollmann, Johann H.
author_facet Ali, Mir Ahsan
Lischka, Katharina
Preuss, Stephanie J.
Trivedi, Chintan A.
Bollmann, Johann H.
author_sort Ali, Mir Ahsan
collection PubMed
description In motor control, the brain not only sends motor commands to the periphery, but also generates concurrent internal signals known as corollary discharge (CD) that influence sensory information processing around the time of movement. CD signals are important for identifying sensory input arising from self-motion and to compensate for it, but the underlying mechanisms remain unclear. Using whole-cell patch clamp recordings from neurons in the zebrafish optic tectum, we discovered an inhibitory synaptic signal, temporally locked to spontaneous and visually driven locomotion. This motor-related inhibition was appropriately timed to counteract visually driven excitatory input arising from the fish’s own motion, and transiently suppressed tectal spiking activity. High-resolution calcium imaging revealed localized motor-related signals in the tectal neuropil and the upstream torus longitudinalis, suggesting that CD enters the tectum via this pathway. Together, our results show how visual processing is suppressed during self-motion by motor-related phasic inhibition. This may help explain perceptual saccadic suppression observed in many species.
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spelling pubmed-106673682023-11-23 A synaptic corollary discharge signal suppresses midbrain visual processing during saccade-like locomotion Ali, Mir Ahsan Lischka, Katharina Preuss, Stephanie J. Trivedi, Chintan A. Bollmann, Johann H. Nat Commun Article In motor control, the brain not only sends motor commands to the periphery, but also generates concurrent internal signals known as corollary discharge (CD) that influence sensory information processing around the time of movement. CD signals are important for identifying sensory input arising from self-motion and to compensate for it, but the underlying mechanisms remain unclear. Using whole-cell patch clamp recordings from neurons in the zebrafish optic tectum, we discovered an inhibitory synaptic signal, temporally locked to spontaneous and visually driven locomotion. This motor-related inhibition was appropriately timed to counteract visually driven excitatory input arising from the fish’s own motion, and transiently suppressed tectal spiking activity. High-resolution calcium imaging revealed localized motor-related signals in the tectal neuropil and the upstream torus longitudinalis, suggesting that CD enters the tectum via this pathway. Together, our results show how visual processing is suppressed during self-motion by motor-related phasic inhibition. This may help explain perceptual saccadic suppression observed in many species. Nature Publishing Group UK 2023-11-23 /pmc/articles/PMC10667368/ /pubmed/37996414 http://dx.doi.org/10.1038/s41467-023-43255-6 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Ali, Mir Ahsan
Lischka, Katharina
Preuss, Stephanie J.
Trivedi, Chintan A.
Bollmann, Johann H.
A synaptic corollary discharge signal suppresses midbrain visual processing during saccade-like locomotion
title A synaptic corollary discharge signal suppresses midbrain visual processing during saccade-like locomotion
title_full A synaptic corollary discharge signal suppresses midbrain visual processing during saccade-like locomotion
title_fullStr A synaptic corollary discharge signal suppresses midbrain visual processing during saccade-like locomotion
title_full_unstemmed A synaptic corollary discharge signal suppresses midbrain visual processing during saccade-like locomotion
title_short A synaptic corollary discharge signal suppresses midbrain visual processing during saccade-like locomotion
title_sort synaptic corollary discharge signal suppresses midbrain visual processing during saccade-like locomotion
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10667368/
https://www.ncbi.nlm.nih.gov/pubmed/37996414
http://dx.doi.org/10.1038/s41467-023-43255-6
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