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Dendritic calcium signals in rhesus macaque motor cortex drive an optical brain-computer interface

Calcium imaging is a powerful tool for recording from large populations of neurons in vivo. Imaging in rhesus macaque motor cortex can enable the discovery of fundamental principles of motor cortical function and can inform the design of next generation brain-computer interfaces (BCIs). Surface two-...

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Autores principales: Trautmann, Eric M., O’Shea, Daniel J., Sun, Xulu, Marshel, James H., Crow, Ailey, Hsueh, Brian, Vesuna, Sam, Cofer, Lucas, Bohner, Gergő, Allen, Will, Kauvar, Isaac, Quirin, Sean, MacDougall, Matthew, Chen, Yuzhi, Whitmire, Matthew P., Ramakrishnan, Charu, Sahani, Maneesh, Seidemann, Eyal, Ryu, Stephen I., Deisseroth, Karl, Shenoy, Krishna V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8211867/
https://www.ncbi.nlm.nih.gov/pubmed/34140486
http://dx.doi.org/10.1038/s41467-021-23884-5
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author Trautmann, Eric M.
O’Shea, Daniel J.
Sun, Xulu
Marshel, James H.
Crow, Ailey
Hsueh, Brian
Vesuna, Sam
Cofer, Lucas
Bohner, Gergő
Allen, Will
Kauvar, Isaac
Quirin, Sean
MacDougall, Matthew
Chen, Yuzhi
Whitmire, Matthew P.
Ramakrishnan, Charu
Sahani, Maneesh
Seidemann, Eyal
Ryu, Stephen I.
Deisseroth, Karl
Shenoy, Krishna V.
author_facet Trautmann, Eric M.
O’Shea, Daniel J.
Sun, Xulu
Marshel, James H.
Crow, Ailey
Hsueh, Brian
Vesuna, Sam
Cofer, Lucas
Bohner, Gergő
Allen, Will
Kauvar, Isaac
Quirin, Sean
MacDougall, Matthew
Chen, Yuzhi
Whitmire, Matthew P.
Ramakrishnan, Charu
Sahani, Maneesh
Seidemann, Eyal
Ryu, Stephen I.
Deisseroth, Karl
Shenoy, Krishna V.
author_sort Trautmann, Eric M.
collection PubMed
description Calcium imaging is a powerful tool for recording from large populations of neurons in vivo. Imaging in rhesus macaque motor cortex can enable the discovery of fundamental principles of motor cortical function and can inform the design of next generation brain-computer interfaces (BCIs). Surface two-photon imaging, however, cannot presently access somatic calcium signals of neurons from all layers of macaque motor cortex due to photon scattering. Here, we demonstrate an implant and imaging system capable of chronic, motion-stabilized two-photon imaging of neuronal calcium signals from macaques engaged in a motor task. By imaging apical dendrites, we achieved optical access to large populations of deep and superficial cortical neurons across dorsal premotor (PMd) and gyral primary motor (M1) cortices. Dendritic signals from individual neurons displayed tuning for different directions of arm movement. Combining several technical advances, we developed an optical BCI (oBCI) driven by these dendritic signalswhich successfully decoded movement direction online. By fusing two-photon functional imaging with CLARITY volumetric imaging, we verified that many imaged dendrites which contributed to oBCI decoding originated from layer 5 output neurons, including a putative Betz cell. This approach establishes new opportunities for studying motor control and designing BCIs via two photon imaging.
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spelling pubmed-82118672021-07-01 Dendritic calcium signals in rhesus macaque motor cortex drive an optical brain-computer interface Trautmann, Eric M. O’Shea, Daniel J. Sun, Xulu Marshel, James H. Crow, Ailey Hsueh, Brian Vesuna, Sam Cofer, Lucas Bohner, Gergő Allen, Will Kauvar, Isaac Quirin, Sean MacDougall, Matthew Chen, Yuzhi Whitmire, Matthew P. Ramakrishnan, Charu Sahani, Maneesh Seidemann, Eyal Ryu, Stephen I. Deisseroth, Karl Shenoy, Krishna V. Nat Commun Article Calcium imaging is a powerful tool for recording from large populations of neurons in vivo. Imaging in rhesus macaque motor cortex can enable the discovery of fundamental principles of motor cortical function and can inform the design of next generation brain-computer interfaces (BCIs). Surface two-photon imaging, however, cannot presently access somatic calcium signals of neurons from all layers of macaque motor cortex due to photon scattering. Here, we demonstrate an implant and imaging system capable of chronic, motion-stabilized two-photon imaging of neuronal calcium signals from macaques engaged in a motor task. By imaging apical dendrites, we achieved optical access to large populations of deep and superficial cortical neurons across dorsal premotor (PMd) and gyral primary motor (M1) cortices. Dendritic signals from individual neurons displayed tuning for different directions of arm movement. Combining several technical advances, we developed an optical BCI (oBCI) driven by these dendritic signalswhich successfully decoded movement direction online. By fusing two-photon functional imaging with CLARITY volumetric imaging, we verified that many imaged dendrites which contributed to oBCI decoding originated from layer 5 output neurons, including a putative Betz cell. This approach establishes new opportunities for studying motor control and designing BCIs via two photon imaging. Nature Publishing Group UK 2021-06-17 /pmc/articles/PMC8211867/ /pubmed/34140486 http://dx.doi.org/10.1038/s41467-021-23884-5 Text en © The Author(s) 2021 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
Trautmann, Eric M.
O’Shea, Daniel J.
Sun, Xulu
Marshel, James H.
Crow, Ailey
Hsueh, Brian
Vesuna, Sam
Cofer, Lucas
Bohner, Gergő
Allen, Will
Kauvar, Isaac
Quirin, Sean
MacDougall, Matthew
Chen, Yuzhi
Whitmire, Matthew P.
Ramakrishnan, Charu
Sahani, Maneesh
Seidemann, Eyal
Ryu, Stephen I.
Deisseroth, Karl
Shenoy, Krishna V.
Dendritic calcium signals in rhesus macaque motor cortex drive an optical brain-computer interface
title Dendritic calcium signals in rhesus macaque motor cortex drive an optical brain-computer interface
title_full Dendritic calcium signals in rhesus macaque motor cortex drive an optical brain-computer interface
title_fullStr Dendritic calcium signals in rhesus macaque motor cortex drive an optical brain-computer interface
title_full_unstemmed Dendritic calcium signals in rhesus macaque motor cortex drive an optical brain-computer interface
title_short Dendritic calcium signals in rhesus macaque motor cortex drive an optical brain-computer interface
title_sort dendritic calcium signals in rhesus macaque motor cortex drive an optical brain-computer interface
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8211867/
https://www.ncbi.nlm.nih.gov/pubmed/34140486
http://dx.doi.org/10.1038/s41467-021-23884-5
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