Cited by 159Memory and Neural MechanismsGenomics and Chromatin DynamicsEpigenetics and DNA Methylation

The DOI matches its Crossref record; 67 of the 68 references it cites were found in a registry or an index, and 1 are not checked yet.

Mapping the epigenomic and transcriptomic interplay during memory formation and recall in the hippocampal engram ensemble

Open access

Marco, Asaf, Meharena, Hiruy S., Dileep, Vishnu, Raju, Ravikiran M., Davila-Velderrain, Jose, Zhang, Amy Letao, Adaikkan, Chinnakkaruppan, Young, Jennie Z., Gao, Fan, Kellis, Manolis, Tsai, Li-Huei·2020·Nature Neuroscience

DOI 10.1038/s41593-020-00717-0PMC PMC7686266

Open this paper in CoChat — free account Open PDF

Abstract

The epigenome and three-dimensional (3D) genomic architecture are emerging as key factors in the dynamic regulation of different transcriptional programs required for neuronal functions. In this study, we used an activity-dependent tagging system in mice to determine the epigenetic state, 3D genome architecture and transcriptional landscape of engram cells over the lifespan of memory formation and recall. Our findings reveal that memory encoding leads to an epigenetic priming event, marked by increased accessibility of enhancers without the corresponding transcriptional changes. Memory consolidation subsequently results in spatial reorganization of large chromatin segments and promoter-enhancer interactions. Finally, with reactivation, engram neurons use a subset of de novo long-range interactions, where primed enhancers are brought in contact with their respective promoters to upregulate genes involved in local protein translation in synaptic compartments. Collectively, our work elucidates the comprehensive transcriptional and epigenomic landscape across the lifespan of memory formation and recall in the hippocampal engram ensemble.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1038/s41593-020-00717-0

Cites

67 of 68 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The Sequence Alignment/Map format and SAMtools
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., & 1000 Genome Project Data Processing Subgroup (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp352 · Cited by 62,041
Fast gapped-read alignment with Bowtie 2
Langmead, B., & Salzberg, S. L. (2012) · Nature Methods · doi:10.1038/nmeth.1923 · Cited by 56,400
<tt>edgeR</tt> : a Bioconductor package for differential expression analysis of digital gene expression data
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364
Model-based Analysis of ChIP-Seq (MACS)
Zhang, Y., Liu, T., Meyer, C. A., Eeckhoute, J., Johnson, D. S., Bernstein, B. E., Nusbaum, C., Myers, R. M., Brown, M., Li, W., et al. (2008) · Genome Biology · doi:10.1186/gb-2008-9-9-r137 · Cited by 18,386
Simple Combinations of Lineage-Determining Transcription Factors Prime cis-Regulatory Elements Required for Macrophage and B Cell Identities
Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y. C., Laslo, P., Cheng, J. X., Murre, C., Singh, H., & Glass, C. K. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.05.004 · Cited by 13,382
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
Trapnell, C., Roberts, A., Goff, L. A., Pertea, G. M., Kim, D., Kelley, D. R., Pimentel, H., Salzberg, S. L., Rinn, J. L., & Pachter, L. S. (2012) · Nature Protocols · doi:10.1038/nprot.2012.016 · Cited by 12,145
Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration
Thorvaldsdottir, H., Robinson, J. T., & Mesirov, J. P. (2013) · Briefings in Bioinformatics · doi:10.1093/bib/bbs017 · Cited by 9,049
Comprehensive Mapping of Long-Range Interactions Reveals Folding Principles of the Human Genome
Lieberman-Aiden, E., van Berkum, N. L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A., Amit, I., Lajoie, B. R., Sabo, P. J., Dorschner, M. O., et al. (2009) · Science · doi:10.1126/science.1181369 · Cited by 8,898
A scaling normalization method for differential expression analysis of RNA-seq data
Robinson, M. D., & Oshlack, A. (2010) · Genome Biology · doi:10.1186/gb-2010-11-3-r25 · Cited by 7,876
Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position
Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y., & Greenleaf, W. J. (2013) · Nature Methods · doi:10.1038/nmeth.2688 · Cited by 6,422

Show all 68 references

Sorted by citations

Chromatin accessibility profiling by ATAC-seq
Grandi, F. C., Modi, H., Kampman, L., & Corces, M. R. (2022) · Nature Protocols · doi:10.1038/s41596-022-00692-9 · Cited by 557
Sex hormone fluctuation and increased female risk for depression and anxiety disorders: From clinical evidence to molecular mechanisms
Kundaković, M., & Rocks, D. (2022) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2022.101010 · Cited by 356
A serotonergic axon-cilium synapse drives nuclear signaling to alter chromatin accessibility
Sheu, S.-H., Upadhyayula, S., Dupuy, V., Pang, S., Deng, F., Wan, J., Walpita, D., Pasolli, H. A., Houser, J., Sanchez-Martinez, S., et al. (2022) · Cell · doi:10.1016/j.cell.2022.07.026 · Cited by 162
Neuronal DNA double-strand breaks lead to genome structural variations and 3D genome disruption in neurodegeneration
Dileep, V., Boix, C. A., Mathys, H., Marco, A., Welch, G. M., Meharena, H. S., Loon, A., Jeloka, R., Peng, Z., Bennett, D. A., et al. (2023) · Cell · doi:10.1016/j.cell.2023.08.038 · Cited by 130
Self-citation
Parp1 promotes sleep, which enhances DNA repair in neurons
Zada, D., Sela, Y., Matosevich, N., Monsonego, A., Lerer‐Goldshtein, T., Nir, Y., & Appelbaum, L. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.10.026 · Cited by 117
Understanding the physical basis of memory: Molecular mechanisms of the engram
Luis, C. O. S., & Ryan, T. J. (2022) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2022.101866 · Cited by 114
Multi-Omics Approaches in Immunological Research
Chu, X., Zhang, B., Koeken, V. A. C. M., Gupta, M. K., & Li, Y. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.668045 · Cited by 87
Hippocampal cells segregate positive and negative engrams
Shpokayte, M., McKissick, O. P., Guan, X., Yuan, B., Rahsepar, B., Fernandez, F. R., Ruesch, E. A., Grella, S. L., White, J. A., Liu, X. S., et al. (2022) · Communications Biology · doi:10.1038/s42003-022-03906-8 · Cited by 74
A Synaptic Framework for the Persistence of Memory Engrams
Rao‐Ruiz, P., Visser, E., Mitrić, M. M., Smit, A. B., & van den Oever, M. C. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2021.661476 · Cited by 70
The essence of the engram: Cellular or synaptic?
Han, D. H., Park, P., Choi, D. I., Bliss, T., & Kaang, B. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.05.033 · Cited by 59
The HDAC inhibitor CI-994 acts as a molecular memory aid by facilitating synaptic and intracellular communication after learning
Burns, A. M., Farinelli-Scharly, M., Hugues-Ascery, S., Sanchez-Mut, J. V., Santoni, G., & Gräff, J. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2116797119 · Cited by 49
From Circuits to Chromatin: The Emerging Role of Epigenetics in Mental Health
Mews, P., Calipari, E. S., Day, J. J., Lobo, M. K., Bredy, T. W., & Abel, T. G. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1649-20.2020 · Cited by 42
Hippocampus‐based behavioral, structural, and molecular dynamics across the estrous cycle
Rocks, D., & Kundaković, M. (2022) · Journal of Neuroendocrinology · doi:10.1111/jne.13216 · Cited by 44
Allosteric conformational ensembles have unlimited capacity for integrating information
Biddle, J. W., Martinez-Corral, R., Wong, F., & Gunawardena, J. (2021) · eLife · doi:10.7554/elife.65498 · Cited by 41
Mapping the spatial transcriptomic signature of the hippocampus during memory consolidation
Vanrobaeys, Y. S., Mukherjee, U., Langmack, L., Beyer, S. E., Bahl, E., Lin, L., Michaelson, J. J., Abel, T. G., & Chatterjee, S. (2023) · Nature Communications · doi:10.1038/s41467-023-41715-7 · Cited by 39
Sex-specific multi-level 3D genome dynamics in the mouse brain
Rocks, D., Shukla, M., Ouldibbat, L., Finnemann, S. C., Kalluchi, A., Rowley, M. J., & Kundaković, M. (2022) · Nature Communications · doi:10.1038/s41467-022-30961-w · Cited by 39
Reactivation of Early-Life Stress-Sensitive Neuronal Ensembles Contributes to Lifelong Stress Hypersensitivity
Rodier, J.-A., Mclain, C., Minerva, A. R., Rashford, R. L., Bennett, S. N., Rogers, F. D., & Peña, C. J. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0016-23.2023 · Cited by 40
3D spatial genome organization in the nervous system: From development and plasticity to disease
Fujita, Y., Pather, S. R., Ming, G., & Song, H. (2022) · Neuron · doi:10.1016/j.neuron.2022.06.004 · Cited by 37
Endoplasmic reticulum chaperone genes encode effectors of long-term memory
Chatterjee, S., Bahl, E., Mukherjee, U., Walsh, E. N., Shetty, M. S., Yan, A. L., Vanrobaeys, Y. S., Lederman, J. D., Giese, K.-P., Michaelson, J. J., et al. (2022) · Science Advances · doi:10.1126/sciadv.abm6063 · Cited by 35
Ketamine ameliorates post-traumatic social avoidance by erasing the traumatic memory encoded in VTA-innervated BLA engram cells
Li, M., Yang, X., Yang, J., Li, T., Cui, C., Peng, X., Lei, J., Ren, K., Ming, J., Zhang, P., et al. (2024) · Neuron · doi:10.1016/j.neuron.2024.06.026 · Cited by 34
Transcriptome and epigenome analysis of engram cells: Next-generation sequencing technologies in memory research
Fuentes-Ramos, M., Alaiz-Noya, M., & Barco, Á. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.06.010 · Cited by 31
The central importance of nuclear mechanisms in the storage of memory
Gold, A. R., & Glanzman, D. L. (2021) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2021.04.125 · Cited by 35
Separate orexigenic hippocampal ensembles shape dietary choice by enhancing contextual memory and motivation
Yang, M., Singh, A., de Araujo, A., McDougle, M. J., Ellis, H., Décarie-Spain, L., Kanoski, S. E., & de Lartigue, G. (2025) · Nature Metabolism · doi:10.1038/s42255-024-01194-6 · Cited by 34
Synaptically-targeted long non-coding RNA SLAMR promotes structural plasticity by increasing translation and CaMKII activity
Espadas, I., Wingfield, J. L., Nakahata, Y., Chanda, K., Grinman, E., Ghosh, I., Bauer, K. E., Raveendra, B., Kiebler, M. A., Yasuda, R., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-46972-8 · Cited by 28
Neuronal enhancers fine-tune adaptive circuit plasticity
Griffith, E. C., West, A. E., & Greenberg, M. E. (2024) · Neuron · doi:10.1016/j.neuron.2024.08.002 · Cited by 29
Cell type–specific epigenetic priming of gene expression in nucleus accumbens by cocaine
Mews, P., van der Zee, Y. Y., Kronman, H. G., Gurung, A., Ramakrishnan, A., Browne, C. J., Futamura, R., Estill, M., Ryan, M., Reyes, A. A., et al. (2024) · Science Advances · doi:10.1126/sciadv.ado3514 · Cited by 26
Epigenetic Mechanisms of Brain Sexual DifferentiationPreprint
Gegenhuber, B., & Tollkühn, J. (2022) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a039099 · Cited by 29
SATB2 organizes the 3D genome architecture of cognition in cortical neurons
Wahl, N., Espeso‐Gil, S., Chietera, P., Nagel, A., Laighneach, A., Morris, D. W., Rajarajan, P., Akbarian, S., Dechant, G., & Apostolova, G. (2024) · Molecular Cell · doi:10.1016/j.molcel.2023.12.024 · Cited by 24
Cell-type specific transcriptional adaptations of nucleus accumbens interneurons to amphetamine
Gallegos, D. A., Minto, M. S., Liu, F., Hazlett, M. F., Yousefzadeh, S. A., Bartelt, L. C., & West, A. E. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01466-1 · Cited by 24
MIAOME: Human microbiome affect the host epigenome
Wang, L., Zhang, W., Wu, X., Xiao, L., Cao, L., Zhai, J., Yang, Y., Chen, Q., Liu, H., Zhang, J., et al. (2022) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2022.05.024 · Cited by 25
Neuromorphic Optical Data Storage Enabled by Nanophotonics: A Perspective
Lamon, S., Zhang, Q., Yu, H., & Gu, M. (2024) · ACS Photonics · doi:10.1021/acsphotonics.3c01253 · Cited by 24
The dynamics of chromatin architecture in brain development and function
Harabula, I., & Pombo, A. (2021) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2020.12.008 · Cited by 26
An unbiased AAV-STARR-seq screen revealing the enhancer activity map of genomic regions in the mouse brain in vivo
Chan, Y.-C., Kienle, E., Oti, M., Liddo, A. D., Méndez-Lago, M., Aschauer, D. F., Peter, M., Pagani, M., Arnold, C. D., Vonderheit, A., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-33448-w · Cited by 21
Activation-induced chromatin reorganization in neurons depends on HDAC1 activity
Grabowska, A. K., Sas‐Nowosielska, H., Wojtaś, B., Holm-Kaczmarek, D., Januszewicz, E., Yushkevich, Y., Czaban, I., Trzaskoma, P., Krawczyk, K., Gielniewski, B., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2022.110352 · Cited by 19
Epigenetic and Transcriptional Regulation of Spontaneous and Sensory Activity Dependent Programs During Neuronal Circuit Development
Pumo, G., Kitazawa, T., & Rijli, F. M. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.911023 · Cited by 23
Targeting mitochondrial dynamics of morphine-responsive dopaminergic neurons ameliorates opiate withdrawal
Jiang, C., Huang, H., Yang, X., Le, Q., Liu, X., Ma, L., & Wang, F. (2024) · Journal of Clinical Investigation · doi:10.1172/jci171995 · Cited by 21
Epigenetic Changes and Chromatin Reorganization in Brain Function: Lessons from Fear Memory Ensemble and Alzheimer’s Disease
van Zundert, B., & Montecino, M. A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232012081 · Cited by 21
Decoding brain memory formation by single-cell RNA sequencing
Sardoo, A. M., Zhang, S., Ferraro, T. N., Keck, T. M., & Chen, Y. (2022) · Briefings in Bioinformatics · doi:10.1093/bib/bbac412 · Cited by 20
Remembering through the genome: the role of chromatin states in brain functions and diseases
Arzate‐Mejía, R. G., & Mansuy, I. M. (2023) · Translational Psychiatry · doi:10.1038/s41398-023-02415-4 · Cited by 22
Aging differentially alters the transcriptome and landscape of chromatin accessibility in the male and female mouse hippocampus
Achiro, J. M., Tao, Y., Gao, F., Lin, C.-H., Watanabe, M., Neumann, S., Coppola, G., Black, D. L., & Martin, K. C. (2024) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2024.1334862 · Cited by 21
Self-citation
Cell type-specific chromatin accessibility analysis in the mouse and human brain
Rocks, D., Jarić, I., Tesfa, L., Greally, J. M., Suzuki, M., & Kundaković, M. (2021) · Epigenetics · doi:10.1080/15592294.2021.1896983 · Cited by 18
Comprehensive Analysis of Mouse Hippocampal Lysine Acetylome Mediated by Sea Cucumber Peptides Preventing Memory Impairment
Lu, Z., Xu, X., Li, D., Sun, N., & Lin, S. (2021) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.1c05155 · Cited by 18
Transcription and epigenetic factor dynamics in neuronal activity-dependent gene regulation
Sugo, N., Atsumi, Y., & Yamamoto, N. (2025) · Trends in Genetics · doi:10.1016/j.tig.2024.12.008 · Cited by 18
CBP Is Required for Establishing Adaptive Gene Programs in the Adult Mouse Brain
Lipiński, M., Niñerola, S., Fuentes-Ramos, M., Valor, L. M., del Blanco, B., López‐Atalaya, J. P., & Barco, Á. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0970-22.2022 · Cited by 18
From cellular to fear memory: An epigenetic toolbox to remember
Coda, D. M., & Gräff, J. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102829 · Cited by 17
Histone macroH2A1 is a stronger regulator of hippocampal transcription and memory than macroH2A2 in mice
Singh, G., Stefanelli, G., Narkaj, K., Brimble, M. A., Creighton, S. D., McLean, T. A. B., Hall, M., Mitchnick, K. A., Zakaria, J. M., Phung, T., et al. (2022) · Communications Biology · doi:10.1038/s42003-022-03435-4 · Cited by 20
Stress and the brain transcriptome: Identifying commonalities and clusters in standardized data from published experiments
Stankiewicz, A. M., Jaszczyk, A., Gościk, J., & Juszczak, G. R. (2022) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2022.110558 · Cited by 17
Three-dimensional chromatin organization in brain function and dysfunction
Dileep, V., & Tsai, L.-H. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.04.006 · Cited by 14
Self-citation
Cell-type specific profiling of histone post-translational modifications in the adult mouse striatum
Carpenter, M. D., Fischer, D. K., Zhang, S., Bond, A. M., Czarnecki, K. S., Woolf, M. T., Song, H., & Heller, E. A. (2022) · Nature Communications · doi:10.1038/s41467-022-35384-1 · Cited by 14
The epigenome under pressure: On regulatory adaptation to chronic stress in the brain
Arzate‐Mejía, R. G., Carullo, N. V. N., & Mansuy, I. M. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102832 · Cited by 15
Early-life stress and ovarian hormones alter transcriptional regulation in the nucleus accumbens resulting in sex-specific responses to cocaine
Rocks, D., Jarić, I., Bellia, F., Cham, H., Greally, J. M., Suzuki, M., & Kundaković, M. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113187 · Cited by 15
Cell-type- and locus-specific epigenetic editing of memory expression
Coda, D. M., Watt, L., Glauser, L., Batiuk, M. Y., Burns, A. M., Stahl, C. L., Wong, L. Y., & Gräff, J. (2025) · Nature Genetics · doi:10.1038/s41588-025-02368-y · Cited by 15
Altered Activity-Regulated H3K9 Acetylation at TGF-Beta Signaling Genes During Egocentric Memory in Huntington's Disease
Alcalá‐Vida, R., Lotz, C., Brulé, B., Séguin, J., Decraene, C., Awada, A., Bombardier, A., Cosquer, B., de Vasconcelos, A. P., Brouillet, E., et al. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102363 · Cited by 16
Characterization of transcriptional profiles associated with stress-induced neuronal activation in Arc-GFP mice
Butto, T., Chongtham, M. C., Mungikar, K., Hartwich, D., Linke, M., Ruffini, N., Radyushkin, K., Schweiger, S., Winter, J., & Gerber, S. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02555-z · Cited by 12
All IEGs Are Not Created Equal—Molecular Sorting Within the Memory Engram
Yelhekar, T. D., Meng, M., Doupe, J., & Lin, Y. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-62983-9_6 · Cited by 12
Hippocampal cells multiplex positive and negative engramsPreprint
Shpokayte, M., McKissick, O. P., Guan, X., Yuan, B., Rahsepar, B., Fernandez, F. R., Ruesch, E. A., Grella, S. L., White, J. A., Liu, X. S., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.11.419887 · Cited by 12
Astroengrams: rethinking the cellular substrate for memory
Romero, J. S., & Navarrete, M. (2026) · Nature reviews. Neuroscience · doi:10.1038/s41583-025-01012-2 · Cited by 13
Rapid nucleus-scale reorganization of chromatin in neurons enables transcriptional adaptation for memory consolidation
Peter, M., Aschauer, D. F., Rose, R., Sinning, A., Groessl, F., Kargl, D., Kraitsy, K., Burkard, T. R., Luhmann, H. J., Haubensak, W. E., et al. (2021) · PLoS ONE · doi:10.1371/journal.pone.0244038 · Cited by 11
Epigenetics in Learning and Memory
van Zundert, B., & Montecino, M. A. (2025) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-3-031-75980-2_2 · Cited by 12
The molecular and cellular basis of memory engrams: Mechanisms of synaptic and systems consolidation
Kupke, J., & Oliveira, A. M. M. (2025) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2025.108057 · Cited by 10
Mutant FUS induces chromatin reorganization in the hippocampus and alters memory processes
Tzeplaeff, L., Séguin, J., Gras, S. L., Megat, S., Cosquer, B., Plassard, D., Dieterle, S., Paiva, I., Picchiarelli, G., Decraene, C., et al. (2023) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2023.102483 · Cited by 9
Unveiling Transcriptional and Epigenetic Mechanisms Within Engram Cells: Insights into Memory Formation and Stability
Fuentes-Ramos, M., & Barco, Á. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-62983-9_7 · Cited by 6
The molecular diversity of plasticity mechanisms underlying memory: An evolutionary perspective
Zha, C., & Sossin, W. S. (2022) · Journal of Neurochemistry · doi:10.1111/jnc.15717 · Cited by 10
Hippocampal DNA Methylation Promotes Contextual Fear Memory Persistence by Facilitating Systems Consolidation and Cortical Engram Stabilization
Kupke, J., Loizou, S., Bengtson, C. P., Sticht, C., & Oliveira, A. M. M. (2025) · Biological Psychiatry · doi:10.1016/j.biopsych.2025.01.016 · Cited by 9
Chromatin Remodeling Factor SMARCA5 is Essential for Hippocampal Memory Maintenance via Metabolic Pathways in Mice
Qu, Y., Zhou, N., Zhang, X., Li, Y., & Xu, X. (2023) · Neuroscience Bulletin · doi:10.1007/s12264-023-01032-x · Cited by 8
Serotonin signaling at cilia synapses
DeLong, K., & Sheu, S.-H. (2025) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2025.102994 · Cited by 7
Activity-dependent remodeling of genome architecture in engram cells facilitates memory formation and recall
Marco, A. (2022) · Neural Regeneration Research · doi:10.4103/1673-5374.324834 · Cited by 7
Self-citation
Differential Activation States of Direct Pathway Striatal Output Neurons during l-DOPA-Induced Dyskinesia Development
Figge, D. A., Amaral, H. D. O., Crim, J., Cowell, R. M., Standaert, D. G., & Jaunarajs, K. L. E. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.0050-24.2024 · Cited by 7
3D Genome Plasticity in Normal and Diseased Neurodevelopment
Plaza-Jennings, A. L., Valada, A., & Akbarian, S. (2022) · Genes · doi:10.3390/genes13111999 · Cited by 7
DNA repair enzyme NEIL3 enables a stable neural representation of space by shaping transcription in hippocampal neurons
Kunath, N., Bugaj, A. M., Bigonah, P., Fernández-Berrocal, M. S., Bjørås, M., & Ye, J. (2021) · iScience · doi:10.1016/j.isci.2021.103470 · Cited by 7
Thalamocortical transcriptional gates coordinate memory stabilization
Terceros, A. A., Chen, C. Y., Harada, Y., Eilers, T., Gebremedhin, M., Hamard, P.-J., Koche, R. P., Sharma, R., & Rajasethupathy, P. (2025) · Nature · doi:10.1038/s41586-025-09774-6 · Cited by 6
Altered morphological characteristics and structural covariance connectivity associated with verbal working memory performance in ADHD children
Liang, S., Huang, L., Zhan, S., Zeng, Y., Zhang, Q., Zhang, Y., Wang, X., Peng, L., Lin, B., & Xu, H. (2023) · British Journal of Radiology · doi:10.1259/bjr.20230409 · Cited by 7
Molecular and cellular mechanisms of engram allocation and maintenance
Karaca, K. G., Kupke, J., & Oliveira, A. M. M. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.02.019 · Cited by 7
The elusive transcriptional memory trace
Gil-Martí, B., Barredo, C. G., Pina-Flores, S., Trejo, J. L., Turiégano, E., & Martín, F. A. (2022) · Oxford Open Neuroscience · doi:10.1093/oons/kvac008 · Cited by 5
Kdm4a is an activity downregulated barrier to generate engrams for memory separation
Guo, X., Hong, P., Xiong, S., Yan, Y., Xie, H. B., & Guan, J. (2024) · Nature Communications · doi:10.1038/s41467-024-50218-y · Cited by 7
Brain Metabolic DNA: A Long Story and Some Conclusions
Giuditta, A., Zucconi, G. G., & Sadile, A. G. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-03030-y · Cited by 5
Hippocampal Cannabinoid 1 Receptors Are Modulated Following Cocaine Self-administration in Male Rats
Nogueira, D. D. S., Bourdy, R., Alcalá‐Vida, R., Filliol, D., Andry, V., Goumon, Y., Zwiller, J., Romieu, P., Mérienne, K., Olmstead, M. C., et al. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-02722-9 · Cited by 5
Can 3D diploid genome reconstruction from unphased Hi-C data be salvaged?
Segal, M. R. (2022) · NAR Genomics and Bioinformatics · doi:10.1093/nargab/lqac038 · Cited by 5
Spatially resolved transcriptomic signatures of hippocampal subregions and Arc-expressing ensembles in active place avoidance memory
Vingan, I., Phatarpekar, S., Tung, V. S. K., Hernandez, A. I., Evgrafov, O. V., & Alarcón, J. M. (2024) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2024.1386239 · Cited by 4
Integrating physiological and transcriptomic analyses at the single-neuron level
Yagishita, H., & Sasaki, T. (2024) · Neuroscience Research · doi:10.1016/j.neures.2024.05.003 · Cited by 4
Activity-dependent transcriptional programs in memory regulate motor recovery after stroke
Joy, M. T., & Carmichael, S. T. (2024) · Communications Biology · doi:10.1038/s42003-024-06723-3 · Cited by 4
Molecular and developmental deficits in Smith-Magenis syndrome human stem cell-derived cortical neural models
Lee, Y., Chang, Y., Cho, Y., Kowalczyk, M., Dragoiescu, A., Pacis, A., Kailasam, S., Lefebvre, F., Zhang, Q., Gao, X. J., et al. (2025) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2025.07.020 · Cited by 3
Single-cell resolution spatial transcriptomic signature of the retrosplenial cortex during memory consolidation
Bliese, S., Basu, B., Beyer, S. E., Elsadany, M., Michaelson, J. J., & Chatterjee, S. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03331-3 · Cited by 3
Spatial transcriptomic profiling uncovers the molecular effects of the neurotoxicant polychlorinated biphenyls (PCBs) in the brains of adult mice
Basu, B., Breese, N. M., Lombardi, S., Wang, H. M., Li, X., Tiburcio, D., Niemasz, Z., Beyer, S. E., Dean, L. E., Marek, R. F., et al. (2026) · Molecular Psychiatry · doi:10.1038/s41380-026-03466-x · Cited by 3
Oxytocin attenuates the retrieval of methamphetamine-associated reward memories by enhancing adult hippocampal neurogenesis in mice
Cai, J., Che, X., Deng, Y., Guo, Z., Yin, M., Li, Y., Li, X., Liu, X., Luo, Y., Xu, T., et al. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03222-7 · Cited by 4
Altered postnatal chromatin development in the nucleus accumbens primes lifelong stress sensitivityPreprint
Rashford, R. L., Fang, L. Z., DeBerardine, M., Kim, H. J. J., Hirschfield, L. W., Cervi, E., Barrett, M. R., Thompson, J. M., Creed, M. C., & Peña, C. J. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.04.12.589272 · Cited by 3
Learning induces persistent chromatin loops underlying robust gene expression during memory recallPreprint
Xu, P., Chandradoss, K. R., Lukasak, B. J., Paranjapye, A., Waldman, A. J., Pham, K., Ryu, H.-S., Liu, C., Titus, K. R., Sureka, R., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.30.678146 · Cited by 3
Genetic Mechanisms of Experience-Dependent Neuronal Plasticity
West, A. E. (2025) · Annual Review of Genetics · doi:10.1146/annurev-genet-020325-103824 · Cited by 4
Extended fear learning enhances excitatory and inhibitory synaptic transmission onto amygdala engram cells
Daphne, D., Ahire, A., Singh, S., Wagner, S., Barkai, E., & Reuveni, I. (2025) · Nature Communications · doi:10.1038/s41467-025-64854-5 · Cited by 2
Memory engram synapse 3D macromolecular architecture visualized by cryoCLEM-guided cryoET
Lovatt, C., O’Sullivan, T., Luis, C. O. S., Ryan, T. J., & Frank, R. A. W. (2025) · Structure · doi:10.1016/j.str.2025.10.014 · Cited by 3
Forgetting Is Not the Mere Opposite of Learning
Jang, S. D. (2023) · Molecules and Cells · doi:10.14348/molcells.2023.0072 · Cited by 2
Memory Storage in Distributed Engram Cell Ensembles
Zhang, Y., & Roy, D. S. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-62983-9_3 · Cited by 1
Time-Dependent Transcriptional Dynamics of Contextual Fear Memory Retrieval Reveals the Function of Dipeptidyl Peptidase 9 in Reconsolidation
Guo, W., Li, W., Liu, Y.-C., Zhao, Y., Xu, L., & Qi-xin, Z. (2024) · Neuroscience Bulletin · doi:10.1007/s12264-024-01324-w · Cited by 2
DNA Methylation in Long-Term Memory
Chen, X., Peng, Y., & Liu, X. S. (2025) · Physiology · doi:10.1152/physiol.00032.2024 · Cited by 2
Genome-wide chromatin recording resolves dynamic cell state changes
Takei, Y., Lay, J. A., Linton, J. M., Chadly, D. M., Ochiai, Y., Hadas, R., Perez, A. A., Blanco, M. R., Laurino, P., Guttman, M., et al. (2026) · Cell Systems · doi:10.1016/j.cels.2026.101717 · Cited by 2
Persistent open chromatin state in early-life stress-activated cells of the VTA
Rashford, R. L., DeBerardine, M., Dan, S., Bennett, S. N., & Peña, C. J. (2025) · Scientific Reports · doi:10.1038/s41598-025-21157-5 · Cited by 2
Statistical curve models for inferring 3D chromatin architecture
Tuzhilina, E., Hastie, T. J., & Segal, M. R. (2024) · The Annals of Applied Statistics · doi:10.1214/24-aoas1917 · Cited by 2
Dynamics of transcriptional programs and chromatin accessibility in mouse spermatogonial cells from early postnatal to adult lifePreprint
Lazar-Contes, I., Arzate‐Mejía, R. G., Tanwar, D. K., Steg, L. C., Uzel, K., Feudjio, O. U., Crespo, M., Germain, P., & Mansuy, I. M. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.20.259374 · Cited by 3
Lysine crotonylation acts as an epigenetic switch for glutamate neurotransmission and spatial memory
Mukherjee, U., Basu, B., Suryavanshi, P. S., Beyer, S. E., Ghodsi, S., Robillard, N., Vanrobaeys, Y. S., Taylor, E. B., Glykys, J., Abel, T. G., et al. (2026) · Proceedings of the National Academy of Sciences · doi:10.1101/2025.02.19.639114 · Cited by 1
Programmed DNA breaks drive chromatin reconfiguration and facilitate transcriptional potentiation at neuronal early response genesPreprint
Heady, L., Rueda, R., Segev, A., Morton, K. G., & Madabhushi, R. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.06.652469 · Cited by 2

Authors: Marco, A., Meharena, H. S., Dileep, V., Raju, R. M., Davila-Velderrain, J., Zhang, A. L., Adaikkan, C., Young, J. Z., Gao, F., Kellis, M., & Tsai, L.-H.
Affiliations: Massachusetts Institute of Technology (US)
Boston Children's Hospital (US)
Broad Institute (US)
Corresponding author: Marco, Asaf
Tsai, Li-Huei
ORCID: Marco, Asaf
Meharena, Hiruy S.
Dileep, Vishnu
Raju, Ravikiran M.
Zhang, Amy Letao
Adaikkan, Chinnakkaruppan
Gao, Fan
Kellis, Manolis
Tsai, Li-Huei
Venue: Nature Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2020-10-05
Volume: 23
Issue: 12
Pages: 1606-1617
ISSN: 1097-6256 (ISSN-L)
1546-1726
DOI: 10.1038/s41593-020-00717-0
PMC: PMC7686266
OpenAlex: W3090072122
Cited by: 159
References: 68
Citations by year: 2026: 23 · 2025: 31 · 2024: 30 · 2023: 22 · 2022: 32 · 2021: 19 · 2020: 2
FWCI: 10.07
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Neuroscience (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
Funders: Alzheimer's Association (AARF-19-618751)
JPB Foundation
Cure Alzheimer's Fund
Down Syndrome Research Foundation
National Institutes of Health (NIH T32, T32 grant)
National Institute on Aging (R01AG058002, R01AG062335, RF1AG054012, RF1AG062377, R01AG067151)
National Institute of Mental Health (U01MH119509, R01MH109978)
National Human Genome Research Institute (R01HG008155, U24HG009446)
National Institute of Neurological Disorders and Stroke (U01NS110453, R01NS102730, UG3NS115064)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD098061)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Keywords: memory formation, memory retrieval, epigenome, 3D genome organization, enhancer accessibility, enhancer-promoter interactions, long-range chromatin interactions, memory consolidation, memory reactivation, transcriptional regulation, mRNA translation
MeSH terms: Memory Consolidation, Animals, Brain Mapping, Hippocampus, Memory, Mice, Transgenic, Neurons, Mental Recall, Synapses, Up-Regulation, Mice, Epigenomics, Transcriptome

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Mapping the epigenomic and transcriptomic interplay during memory formation and recall in the hippocampal engram ensemble

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks