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A novel environment-evoked transcriptional signature predicts reactivity in single dentate granule neurons

Activity-induced remodeling of neuronal circuits is critical for memory formation. This process relies in part on transcription, but neither the rate of activity nor baseline transcription is equal across neuronal cell types. In this study, we isolated mouse hippocampal populations with different ac...

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Autores principales: Jaeger, Baptiste N., Linker, Sara B., Parylak, Sarah L., Barron, Jerika J., Gallina, Iryna S., Saavedra, Christian D., Fitzpatrick, Conor, Lim, Christina K., Schafer, Simon T., Lacar, Benjamin, Jessberger, Sebastian, Gage, Fred H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6079101/
https://www.ncbi.nlm.nih.gov/pubmed/30082781
http://dx.doi.org/10.1038/s41467-018-05418-8
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author Jaeger, Baptiste N.
Linker, Sara B.
Parylak, Sarah L.
Barron, Jerika J.
Gallina, Iryna S.
Saavedra, Christian D.
Fitzpatrick, Conor
Lim, Christina K.
Schafer, Simon T.
Lacar, Benjamin
Jessberger, Sebastian
Gage, Fred H.
author_facet Jaeger, Baptiste N.
Linker, Sara B.
Parylak, Sarah L.
Barron, Jerika J.
Gallina, Iryna S.
Saavedra, Christian D.
Fitzpatrick, Conor
Lim, Christina K.
Schafer, Simon T.
Lacar, Benjamin
Jessberger, Sebastian
Gage, Fred H.
author_sort Jaeger, Baptiste N.
collection PubMed
description Activity-induced remodeling of neuronal circuits is critical for memory formation. This process relies in part on transcription, but neither the rate of activity nor baseline transcription is equal across neuronal cell types. In this study, we isolated mouse hippocampal populations with different activity levels and used single nucleus RNA-seq to compare their transcriptional responses to activation. One hour after novel environment exposure, sparsely active dentate granule (DG) neurons had a much stronger transcriptional response compared to more highly active CA1 pyramidal cells and vasoactive intestinal polypeptide (VIP) interneurons. Activity continued to impact transcription in DG neurons up to 5 h, with increased heterogeneity. By re-exposing the mice to the same environment, we identified a unique transcriptional signature that selects DG neurons for reactivation upon re-exposure to the same environment. These results link transcriptional heterogeneity to functional heterogeneity and identify a transcriptional correlate of memory encoding in individual DG neurons.
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spelling pubmed-60791012018-08-08 A novel environment-evoked transcriptional signature predicts reactivity in single dentate granule neurons Jaeger, Baptiste N. Linker, Sara B. Parylak, Sarah L. Barron, Jerika J. Gallina, Iryna S. Saavedra, Christian D. Fitzpatrick, Conor Lim, Christina K. Schafer, Simon T. Lacar, Benjamin Jessberger, Sebastian Gage, Fred H. Nat Commun Article Activity-induced remodeling of neuronal circuits is critical for memory formation. This process relies in part on transcription, but neither the rate of activity nor baseline transcription is equal across neuronal cell types. In this study, we isolated mouse hippocampal populations with different activity levels and used single nucleus RNA-seq to compare their transcriptional responses to activation. One hour after novel environment exposure, sparsely active dentate granule (DG) neurons had a much stronger transcriptional response compared to more highly active CA1 pyramidal cells and vasoactive intestinal polypeptide (VIP) interneurons. Activity continued to impact transcription in DG neurons up to 5 h, with increased heterogeneity. By re-exposing the mice to the same environment, we identified a unique transcriptional signature that selects DG neurons for reactivation upon re-exposure to the same environment. These results link transcriptional heterogeneity to functional heterogeneity and identify a transcriptional correlate of memory encoding in individual DG neurons. Nature Publishing Group UK 2018-08-06 /pmc/articles/PMC6079101/ /pubmed/30082781 http://dx.doi.org/10.1038/s41467-018-05418-8 Text en © The Author(s) 2018 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
Jaeger, Baptiste N.
Linker, Sara B.
Parylak, Sarah L.
Barron, Jerika J.
Gallina, Iryna S.
Saavedra, Christian D.
Fitzpatrick, Conor
Lim, Christina K.
Schafer, Simon T.
Lacar, Benjamin
Jessberger, Sebastian
Gage, Fred H.
A novel environment-evoked transcriptional signature predicts reactivity in single dentate granule neurons
title A novel environment-evoked transcriptional signature predicts reactivity in single dentate granule neurons
title_full A novel environment-evoked transcriptional signature predicts reactivity in single dentate granule neurons
title_fullStr A novel environment-evoked transcriptional signature predicts reactivity in single dentate granule neurons
title_full_unstemmed A novel environment-evoked transcriptional signature predicts reactivity in single dentate granule neurons
title_short A novel environment-evoked transcriptional signature predicts reactivity in single dentate granule neurons
title_sort novel environment-evoked transcriptional signature predicts reactivity in single dentate granule neurons
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6079101/
https://www.ncbi.nlm.nih.gov/pubmed/30082781
http://dx.doi.org/10.1038/s41467-018-05418-8
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