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Arm movements induced by noninvasive optogenetic stimulation of the motor cortex in the common marmoset

Optogenetics is now a fundamental tool for investigating the relationship between neuronal activity and behavior. However, its application to the investigation of motor control systems in nonhuman primates is rather limited, because optogenetic stimulation of cortical neurons in nonhuman primates ha...

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Autores principales: Ebina, Teppei, Obara, Keitaro, Watakabe, Akiya, Masamizu, Yoshito, Terada, Shin-Ichiro, Matoba, Ryota, Takaji, Masafumi, Hatanaka, Nobuhiko, Nambu, Atsushi, Mizukami, Hiroaki, Yamamori, Tetsuo, Matsuzaki, Masanori
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6842633/
https://www.ncbi.nlm.nih.gov/pubmed/31636197
http://dx.doi.org/10.1073/pnas.1903445116
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author Ebina, Teppei
Obara, Keitaro
Watakabe, Akiya
Masamizu, Yoshito
Terada, Shin-Ichiro
Matoba, Ryota
Takaji, Masafumi
Hatanaka, Nobuhiko
Nambu, Atsushi
Mizukami, Hiroaki
Yamamori, Tetsuo
Matsuzaki, Masanori
author_facet Ebina, Teppei
Obara, Keitaro
Watakabe, Akiya
Masamizu, Yoshito
Terada, Shin-Ichiro
Matoba, Ryota
Takaji, Masafumi
Hatanaka, Nobuhiko
Nambu, Atsushi
Mizukami, Hiroaki
Yamamori, Tetsuo
Matsuzaki, Masanori
author_sort Ebina, Teppei
collection PubMed
description Optogenetics is now a fundamental tool for investigating the relationship between neuronal activity and behavior. However, its application to the investigation of motor control systems in nonhuman primates is rather limited, because optogenetic stimulation of cortical neurons in nonhuman primates has failed to induce or modulate any hand/arm movements. Here, we used a tetracycline-inducible gene expression system carrying CaMKII promoter and the gene encoding a Channelrhodopsin-2 variant with fast kinetics in the common marmoset, a small New World monkey. In an awake state, forelimb movements could be induced when Channelrhodopsin-2−expressing neurons in the motor cortex were illuminated by blue laser light with a spot diameter of 1 mm or 2 mm through a cranial window without cortical invasion. Forelimb muscles responded 10 ms to 50 ms after photostimulation onset. Long-duration (500 ms) photostimulation induced discrete forelimb movements that could be markerlessly tracked with charge-coupled device cameras and a deep learning algorithm. Long-duration photostimulation mapping revealed that the primary motor cortex is divided into multiple domains that can induce hand and elbow movements in different directions. During performance of a forelimb movement task, movement trajectories were modulated by weak photostimulation, which did not induce visible forelimb movements at rest, around the onset of task-relevant movement. The modulation was biased toward the movement direction induced by the strong photostimulation. Combined with calcium imaging, all-optical interrogation of motor circuits should be possible in behaving marmosets.
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spelling pubmed-68426332019-11-15 Arm movements induced by noninvasive optogenetic stimulation of the motor cortex in the common marmoset Ebina, Teppei Obara, Keitaro Watakabe, Akiya Masamizu, Yoshito Terada, Shin-Ichiro Matoba, Ryota Takaji, Masafumi Hatanaka, Nobuhiko Nambu, Atsushi Mizukami, Hiroaki Yamamori, Tetsuo Matsuzaki, Masanori Proc Natl Acad Sci U S A Biological Sciences Optogenetics is now a fundamental tool for investigating the relationship between neuronal activity and behavior. However, its application to the investigation of motor control systems in nonhuman primates is rather limited, because optogenetic stimulation of cortical neurons in nonhuman primates has failed to induce or modulate any hand/arm movements. Here, we used a tetracycline-inducible gene expression system carrying CaMKII promoter and the gene encoding a Channelrhodopsin-2 variant with fast kinetics in the common marmoset, a small New World monkey. In an awake state, forelimb movements could be induced when Channelrhodopsin-2−expressing neurons in the motor cortex were illuminated by blue laser light with a spot diameter of 1 mm or 2 mm through a cranial window without cortical invasion. Forelimb muscles responded 10 ms to 50 ms after photostimulation onset. Long-duration (500 ms) photostimulation induced discrete forelimb movements that could be markerlessly tracked with charge-coupled device cameras and a deep learning algorithm. Long-duration photostimulation mapping revealed that the primary motor cortex is divided into multiple domains that can induce hand and elbow movements in different directions. During performance of a forelimb movement task, movement trajectories were modulated by weak photostimulation, which did not induce visible forelimb movements at rest, around the onset of task-relevant movement. The modulation was biased toward the movement direction induced by the strong photostimulation. Combined with calcium imaging, all-optical interrogation of motor circuits should be possible in behaving marmosets. National Academy of Sciences 2019-11-05 2019-10-21 /pmc/articles/PMC6842633/ /pubmed/31636197 http://dx.doi.org/10.1073/pnas.1903445116 Text en Copyright © 2019 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Ebina, Teppei
Obara, Keitaro
Watakabe, Akiya
Masamizu, Yoshito
Terada, Shin-Ichiro
Matoba, Ryota
Takaji, Masafumi
Hatanaka, Nobuhiko
Nambu, Atsushi
Mizukami, Hiroaki
Yamamori, Tetsuo
Matsuzaki, Masanori
Arm movements induced by noninvasive optogenetic stimulation of the motor cortex in the common marmoset
title Arm movements induced by noninvasive optogenetic stimulation of the motor cortex in the common marmoset
title_full Arm movements induced by noninvasive optogenetic stimulation of the motor cortex in the common marmoset
title_fullStr Arm movements induced by noninvasive optogenetic stimulation of the motor cortex in the common marmoset
title_full_unstemmed Arm movements induced by noninvasive optogenetic stimulation of the motor cortex in the common marmoset
title_short Arm movements induced by noninvasive optogenetic stimulation of the motor cortex in the common marmoset
title_sort arm movements induced by noninvasive optogenetic stimulation of the motor cortex in the common marmoset
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6842633/
https://www.ncbi.nlm.nih.gov/pubmed/31636197
http://dx.doi.org/10.1073/pnas.1903445116
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