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Modulation of deep neural circuits with sonogenetics

Noninvasive control of neuronal activity in the deep brain can be illuminating for probing brain function and treating dysfunctions. Here, we present a sonogenetic approach for controlling distinct mouse behavior with circuit specificity and subsecond temporal resolution. Targeted neurons in subcort...

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Autores principales: Xian, Quanxiang, Qiu, Zhihai, Murugappan, Suresh, Kala, Shashwati, Wong, Kin Fung, Li, Danni, Li, Guofeng, Jiang, Yizhou, Wu, Yong, Su, Min, Hou, Xuandi, Zhu, Jiejun, Guo, Jinghui, Qiu, Weibao, Sun, Lei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10235981/
https://www.ncbi.nlm.nih.gov/pubmed/37216521
http://dx.doi.org/10.1073/pnas.2220575120
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author Xian, Quanxiang
Qiu, Zhihai
Murugappan, Suresh
Kala, Shashwati
Wong, Kin Fung
Li, Danni
Li, Guofeng
Jiang, Yizhou
Wu, Yong
Su, Min
Hou, Xuandi
Zhu, Jiejun
Guo, Jinghui
Qiu, Weibao
Sun, Lei
author_facet Xian, Quanxiang
Qiu, Zhihai
Murugappan, Suresh
Kala, Shashwati
Wong, Kin Fung
Li, Danni
Li, Guofeng
Jiang, Yizhou
Wu, Yong
Su, Min
Hou, Xuandi
Zhu, Jiejun
Guo, Jinghui
Qiu, Weibao
Sun, Lei
author_sort Xian, Quanxiang
collection PubMed
description Noninvasive control of neuronal activity in the deep brain can be illuminating for probing brain function and treating dysfunctions. Here, we present a sonogenetic approach for controlling distinct mouse behavior with circuit specificity and subsecond temporal resolution. Targeted neurons in subcortical regions were made to express a mutant large conductance mechanosensitive ion channel (MscL-G22S), enabling ultrasound to trigger activity in MscL-expressing neurons in the dorsal striatum and increase locomotion in freely moving mice. Ultrasound stimulation of MscL-expressing neurons in the ventral tegmental area could activate the mesolimbic pathway to trigger dopamine release in the nucleus accumbens and modulate appetitive conditioning. Moreover, sonogenetic stimulation of the subthalamic nuclei of Parkinson’s disease model mice improved their motor coordination and mobile time. Neuronal responses to ultrasound pulse trains were rapid, reversible, and repeatable. We also confirmed that the MscL-G22S mutant is more effective to sensitize neurons to ultrasound compared to the wild-type MscL. Altogether, we lay out a sonogenetic approach which can selectively manipulate targeted cells to activate defined neural pathways, affect specific behaviors, and relieve symptoms of neurodegenerative disease.
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spelling pubmed-102359812023-06-03 Modulation of deep neural circuits with sonogenetics Xian, Quanxiang Qiu, Zhihai Murugappan, Suresh Kala, Shashwati Wong, Kin Fung Li, Danni Li, Guofeng Jiang, Yizhou Wu, Yong Su, Min Hou, Xuandi Zhu, Jiejun Guo, Jinghui Qiu, Weibao Sun, Lei Proc Natl Acad Sci U S A Biological Sciences Noninvasive control of neuronal activity in the deep brain can be illuminating for probing brain function and treating dysfunctions. Here, we present a sonogenetic approach for controlling distinct mouse behavior with circuit specificity and subsecond temporal resolution. Targeted neurons in subcortical regions were made to express a mutant large conductance mechanosensitive ion channel (MscL-G22S), enabling ultrasound to trigger activity in MscL-expressing neurons in the dorsal striatum and increase locomotion in freely moving mice. Ultrasound stimulation of MscL-expressing neurons in the ventral tegmental area could activate the mesolimbic pathway to trigger dopamine release in the nucleus accumbens and modulate appetitive conditioning. Moreover, sonogenetic stimulation of the subthalamic nuclei of Parkinson’s disease model mice improved their motor coordination and mobile time. Neuronal responses to ultrasound pulse trains were rapid, reversible, and repeatable. We also confirmed that the MscL-G22S mutant is more effective to sensitize neurons to ultrasound compared to the wild-type MscL. Altogether, we lay out a sonogenetic approach which can selectively manipulate targeted cells to activate defined neural pathways, affect specific behaviors, and relieve symptoms of neurodegenerative disease. National Academy of Sciences 2023-05-22 2023-05-30 /pmc/articles/PMC10235981/ /pubmed/37216521 http://dx.doi.org/10.1073/pnas.2220575120 Text en Copyright © 2023 the Author(s). Published by PNAS. 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
Xian, Quanxiang
Qiu, Zhihai
Murugappan, Suresh
Kala, Shashwati
Wong, Kin Fung
Li, Danni
Li, Guofeng
Jiang, Yizhou
Wu, Yong
Su, Min
Hou, Xuandi
Zhu, Jiejun
Guo, Jinghui
Qiu, Weibao
Sun, Lei
Modulation of deep neural circuits with sonogenetics
title Modulation of deep neural circuits with sonogenetics
title_full Modulation of deep neural circuits with sonogenetics
title_fullStr Modulation of deep neural circuits with sonogenetics
title_full_unstemmed Modulation of deep neural circuits with sonogenetics
title_short Modulation of deep neural circuits with sonogenetics
title_sort modulation of deep neural circuits with sonogenetics
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10235981/
https://www.ncbi.nlm.nih.gov/pubmed/37216521
http://dx.doi.org/10.1073/pnas.2220575120
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