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Tactile modulation of memory and anxiety requires dentate granule cells along the dorsoventral axis

Touch can positively influence cognition and emotion, but the underlying mechanisms remain unclear. Here, we report that tactile experience enrichment improves memory and alleviates anxiety by remodeling neurons along the dorsoventral axis of the dentate gyrus (DG) in adult mice. Tactile enrichment...

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Autores principales: Wang, Chi, Liu, Hui, Li, Kun, Wu, Zhen-Zhen, Wu, Chen, Yu, Jing-Ying, Gong, Qian, Fang, Ping, Wang, Xing-Xing, Duan, Shu-Min, Wang, Hao, Gu, Yan, Hu, Ji, Pan, Bing-Xing, Schmidt, Mathias V., Liu, Yi-Jun, Wang, Xiao-Dong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7695841/
https://www.ncbi.nlm.nih.gov/pubmed/33247136
http://dx.doi.org/10.1038/s41467-020-19874-8
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author Wang, Chi
Liu, Hui
Li, Kun
Wu, Zhen-Zhen
Wu, Chen
Yu, Jing-Ying
Gong, Qian
Fang, Ping
Wang, Xing-Xing
Duan, Shu-Min
Wang, Hao
Gu, Yan
Hu, Ji
Pan, Bing-Xing
Schmidt, Mathias V.
Liu, Yi-Jun
Wang, Xiao-Dong
author_facet Wang, Chi
Liu, Hui
Li, Kun
Wu, Zhen-Zhen
Wu, Chen
Yu, Jing-Ying
Gong, Qian
Fang, Ping
Wang, Xing-Xing
Duan, Shu-Min
Wang, Hao
Gu, Yan
Hu, Ji
Pan, Bing-Xing
Schmidt, Mathias V.
Liu, Yi-Jun
Wang, Xiao-Dong
author_sort Wang, Chi
collection PubMed
description Touch can positively influence cognition and emotion, but the underlying mechanisms remain unclear. Here, we report that tactile experience enrichment improves memory and alleviates anxiety by remodeling neurons along the dorsoventral axis of the dentate gyrus (DG) in adult mice. Tactile enrichment induces differential activation and structural modification of neurons in the dorsal and ventral DG, and increases the presynaptic input from the lateral entorhinal cortex (LEC), which is reciprocally connected with the primary somatosensory cortex (S1), to tactile experience-activated DG neurons. Chemogenetic activation of tactile experience-tagged dorsal and ventral DG neurons enhances memory and reduces anxiety respectively, whereas inactivation of these neurons or S1-innervated LEC neurons abolishes the beneficial effects of tactile enrichment. Moreover, adulthood tactile enrichment attenuates early-life stress-induced memory deficits and anxiety-related behavior. Our findings demonstrate that enriched tactile experience retunes the pathway from S1 to DG and enhances DG neuronal plasticity to modulate cognition and emotion.
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spelling pubmed-76958412020-12-03 Tactile modulation of memory and anxiety requires dentate granule cells along the dorsoventral axis Wang, Chi Liu, Hui Li, Kun Wu, Zhen-Zhen Wu, Chen Yu, Jing-Ying Gong, Qian Fang, Ping Wang, Xing-Xing Duan, Shu-Min Wang, Hao Gu, Yan Hu, Ji Pan, Bing-Xing Schmidt, Mathias V. Liu, Yi-Jun Wang, Xiao-Dong Nat Commun Article Touch can positively influence cognition and emotion, but the underlying mechanisms remain unclear. Here, we report that tactile experience enrichment improves memory and alleviates anxiety by remodeling neurons along the dorsoventral axis of the dentate gyrus (DG) in adult mice. Tactile enrichment induces differential activation and structural modification of neurons in the dorsal and ventral DG, and increases the presynaptic input from the lateral entorhinal cortex (LEC), which is reciprocally connected with the primary somatosensory cortex (S1), to tactile experience-activated DG neurons. Chemogenetic activation of tactile experience-tagged dorsal and ventral DG neurons enhances memory and reduces anxiety respectively, whereas inactivation of these neurons or S1-innervated LEC neurons abolishes the beneficial effects of tactile enrichment. Moreover, adulthood tactile enrichment attenuates early-life stress-induced memory deficits and anxiety-related behavior. Our findings demonstrate that enriched tactile experience retunes the pathway from S1 to DG and enhances DG neuronal plasticity to modulate cognition and emotion. Nature Publishing Group UK 2020-11-27 /pmc/articles/PMC7695841/ /pubmed/33247136 http://dx.doi.org/10.1038/s41467-020-19874-8 Text en © The Author(s) 2020 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/.
spellingShingle Article
Wang, Chi
Liu, Hui
Li, Kun
Wu, Zhen-Zhen
Wu, Chen
Yu, Jing-Ying
Gong, Qian
Fang, Ping
Wang, Xing-Xing
Duan, Shu-Min
Wang, Hao
Gu, Yan
Hu, Ji
Pan, Bing-Xing
Schmidt, Mathias V.
Liu, Yi-Jun
Wang, Xiao-Dong
Tactile modulation of memory and anxiety requires dentate granule cells along the dorsoventral axis
title Tactile modulation of memory and anxiety requires dentate granule cells along the dorsoventral axis
title_full Tactile modulation of memory and anxiety requires dentate granule cells along the dorsoventral axis
title_fullStr Tactile modulation of memory and anxiety requires dentate granule cells along the dorsoventral axis
title_full_unstemmed Tactile modulation of memory and anxiety requires dentate granule cells along the dorsoventral axis
title_short Tactile modulation of memory and anxiety requires dentate granule cells along the dorsoventral axis
title_sort tactile modulation of memory and anxiety requires dentate granule cells along the dorsoventral axis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7695841/
https://www.ncbi.nlm.nih.gov/pubmed/33247136
http://dx.doi.org/10.1038/s41467-020-19874-8
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