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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Different Patterns of Electrical Activity Lead to Long-term Potentiation by Activating Different Intracellular Pathways
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Calcineurin Signaling Mediates Activity-Dependent Relocation of the Axon Initial Segment
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Long-Distance Integration of Nuclear ERK Signaling Triggered by Activation of a Few Dendritic Spines
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Visible light reduces C. elegans longevity
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Spike Frequency Decoding and Autonomous Activation of Ca2+–Calmodulin-Dependent Protein Kinase II in Dorsal Root Ganglion Neurons
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SnapShot-Seq: A Method for Extracting Genome-Wide, In Vivo mRNA Dynamics from a Single Total RNA Sample
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High-frequency discharge of dentate granule cells, but not long-term potentiation, induces c-fos protein
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Mitogen-Activated Protein Kinase/Extracellular Signal-Regulated Kinase Activation in Somatodendritic Compartments: Roles of Action Potentials, Frequency, and Mode of Calcium Entry
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Nonlinear Decoding and Asymmetric Representation of Neuronal Input Information by CaMKIIα and Calcineurin
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RASopathies: unraveling mechanisms with animal models
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Differential regulation of calcium/calmodulin-dependent protein kinase II and p42 MAP kinase activity by synaptic transmission
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Chromatin kinases act on transcription factors and histone tails in regulation of inducible transcription
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Optogenetic control of nerve growth
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Temporal Control of Immediate Early Gene Induction by Light
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Mitogen activated protein kinase‐dependent activation of c‐Jun and c‐Fos is required for neuronal differentiation but not for growth and stress response in PC12 cells
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Visible light effects on tumoral cells in a culture medium enriched with tryptophan and riboflavin
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Modulation of calcium wave propagation in the dendrites and to the soma of rat hippocampal pyramidal neurons
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Shadow Enhancers Mediate Dynamic Shifts of Gap Gene Expression in the Drosophila Embryo
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Gene networks activated by specific patterns of action potentials in dorsal root ganglia neurons
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Regulation of BDNF-mediated transcription of immediate early gene Arc by intracellular calcium and calmodulin
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TNF-α Preconditioning Protects Neurons via Neuron-Specific Up-Regulation of CREB-Binding Protein
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Autism-like syndrome is induced by pharmacological suppression of BET proteins in young mice
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ERK-Induced Activation of TCF Family of SRF Cofactors Initiates a Chromatin Modification Cascade Associated with Transcription
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DECENT: differential expression with capture efficiency adjustmeNT for single-cell RNA-seq data
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H2O2-Sensitive Isoforms of Drosophila melanogaster TRPA1 Act in Bitter-Sensing Gustatory Neurons to Promote Avoidance of UV During Egg-Laying
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Calcineurin activity is required for depolarization‐induced, CREB‐dependent gene transcription in cortical neurons
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Optogenetic control of signaling in mammalian cells
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ERK2/p42 MAP kinase stimulates both autonomous and SRF‐dependent DNA binding by Elk‐1
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Splitting Hares and Tortoises: A classification of neuronal immediate early gene transcription based on poised RNA polymerase II
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Optogenetic Activation of the Infralimbic Cortex Suppresses the Return of Appetitive Pavlovian-Conditioned Responding Following Extinction
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Steroid Receptors
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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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