Cited by 399Neuroscience and Neuropharmacology ResearchMemory and Neural MechanismsNeural dynamics and brain function

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Different Neuronal Activity Patterns Induce Different Gene Expression Programs

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Tyssowski, Kelsey M., DeStefino, Nicholas R., Cho, Jin-Hyung, Dunn, Carissa J., Poston, Robert G., Carty, Crista E., Jones, Richard D., Chang, Sarah M., Romeo, Palmyra, Wurzelmann, Mary K., Ward, James M., Andermann, Mark L., Saha, Ramendra N., Dudek, Serena M., Gray, Jesse M.·2018·Neuron

DOI 10.1016/j.neuron.2018.04.001PMC PMC5934296

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Abstract

A vast number of different neuronal activity patterns could each induce a different set of activity-regulated genes. Mapping this coupling between activity pattern and gene induction would allow inference of a neuron's activity-pattern history from its gene expression and improve our understanding of activity-pattern-dependent synaptic plasticity. In genome-scale experiments comparing brief and sustained activity patterns, we reveal that activity-duration history can be inferred from gene expression profiles. Brief activity selectively induces a small subset of the activity-regulated gene program that corresponds to the first of three temporal waves of genes induced by sustained activity. Induction of these first-wave genes is mechanistically distinct from that of the later waves because it requires MAPK/ERK signaling but does not require de novo translation. Thus, the same mechanisms that establish the multi-wave temporal structure of gene induction also enable different gene sets to be induced by different activity durations.

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Additional file 13 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599762
Additional file 2 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599729
Additional file 19 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599780
Additional file 6 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599741
Additional file 17 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599774
Additional file 4 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599735
Additional file 15 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599768
Additional file 14 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599765
Additional file 7 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599744
Additional file 5 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599738
Additional file 20 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599783
Additional file 9 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599750
Additional file 12 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599759
Additional file 1 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599726
Additional file 8 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599747
Additional file 16 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599771
Additional file 3 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599732
Additional file 10 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599753
Additional file 11 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599756
Additional file 18 of Identification and characterization of transcribed enhancers during cerebellar development through enhancer RNA analysis
Ramirez, M., Robert, R., Yeung, J., Wu, J. P. H., Abdalla-Wyse, A., & Goldowitz, D. (2024) · Figshare · doi:10.6084/m9.figshare.26599777
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Authors: Tyssowski, K. M., DeStefino, N. R., Cho, J.-H., Dunn, C. J., Poston, R. G., Carty, C. E., Jones, R. D., Chang, S. M., Romeo, P., Wurzelmann, M. K., Ward, J. M., Andermann, M. L., Saha, R. N., Dudek, S. M., & Gray, J. M.
Affiliations: Harvard University (US)
University of California, Merced (US)
Beth Israel Deaconess Medical Center (US)
National Institute of Environmental Health Sciences (US)
National Institutes of Health (US)
Corresponding author: Saha, Ramendra N.
Dudek, Serena M.
Gray, Jesse M.
ORCID: Tyssowski, Kelsey M.
Dunn, Carissa J.
Jones, Richard D.
Chang, Sarah M.
Ward, James M.
Andermann, Mark L.
Saha, Ramendra N.
Dudek, Serena M.
Gray, Jesse M.
Venue: Neuron
Publisher: Elsevier BV
Published: 2018-05
Volume: 98
Issue: 3
Pages: 530-546.e11
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2018.04.001
PMC: PMC5934296
OpenAlex: W2950828985
Cited by: 390
References: 177
Citations by year: 2026: 39 · 2025: 51 · 2024: 67 · 2023: 54 · 2022: 50 · 2021: 41 · 2020: 39 · 2019: 34 · 2018: 14
FWCI: 14.57
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 366 d)
Locations: Neuron (publishedVersion)
bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
eScholarship (California Digital Library) (submittedVersion)
Funders: Armenise-Harvard (R01 MH101528-01, R01 MH116223-01)
Kaneb family
Intramural Research Program of the National Institute of Environmental Health Sciences
National Institutes of Health (Z01 ES100221)
NSF Graduate Research Fellowship Program (DGE1144152, DEG1745303)
National Institute of Health NRSA (R00 MH096941)
Canadian Institute of Health Research
NIH New Innovator Award (DP2 DK105570, R01 DK109930)
McKnight Scholar Award
Harvard Brain Science Initiative Bipolar Disorder Seed Grant
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords: neural activity patterns, activity duration, ERK signaling, synaptic plasticity, gene expression profiling
MeSH terms: Animals, Cells, Cultured, Cerebral Cortex, Female, Gene Expression Regulation, Male, Mice, Inbred C57BL, Mice, Inbred ICR, Neurons, Photic Stimulation, Rats, Sprague-Dawley, MAP Kinase Signaling System, Mice, Rats

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Different Neuronal Activity Patterns Induce Different Gene Expression Programs

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