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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...
Autores principales: | , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2019
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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. |
format | Online Article Text |
id | pubmed-6842633 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
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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