Epigenetic Priming of Memory Updating during Reconsolidation to Attenuate Remote Fear Memories
Open accessAbstract
Traumatic events generate some of the most enduring forms of memories. Despite the elevated lifetime prevalence of anxiety disorders, effective strategies to attenuate long-term traumatic memories are scarce. The most efficacious treatments to diminish recent (i.e., day-old) traumata capitalize on memory updating mechanisms during reconsolidation that are initiated upon memory recall. Here, we show that, in mice, successful reconsolidation-updating paradigms for recent memories fail to attenuate remote (i.e., month-old) ones. We find that, whereas recent memory recall induces a limited period of hippocampal neuroplasticity mediated, in part, by S-nitrosylation of HDAC2 and histone acetylation, such plasticity is absent for remote memories. However, by using an HDAC2-targeting inhibitor (HDACi) during reconsolidation, even remote memories can be persistently attenuated. This intervention epigenetically primes the expression of neuroplasticity-related genes, which is accompanied by higher metabolic, synaptic, and structural plasticity. Thus, applying HDACis during memory reconsolidation might constitute a treatment option for remote traumata.
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CI-994 is an orally active class I HDAC inhibitor.
“CI-994 is an orally active class I HDAC inhibitor that has undergone several phase II/III clinical trials on cancer treatment.”
From CI-994 is a dual modulator of class I HDACs and Wnt/β-catenin signaling for the treatment of Alzheimer's disease (2026) · cites this paper as [17]
The Results section, “By Using HDAC2-Targeting HDAC Inhibitors,” identifies CI-994 as a selective class I HDAC inhibitor. Our copy does not establish that it is orally active; the Results and Experimental Procedures describe intraperitoneal administration instead. (LLM, conf=0.87)
Experimental — accuracy not yet measuredCI-994 is a cognitive enhancer / improves cognitive function.
“CI-994 can cross the blood–brain barrier and is a cognitive enhancer.”
From CI-994 is a dual modulator of class I HDACs and Wnt/β-catenin signaling for the treatment of Alzheimer's disease (2026) · cites this paper as [17]
The Results section ('By Using HDAC2-Targeting HDAC Inhibitors, Remote Fear Memories Can Be Attenuated'; page unavailable) reports sustained CI-994 levels in the brain after systemic administration, supporting brain penetration. It also reports improved extinction of remote fear memories when CI-994 was paired with memory recall and extinction training, but does not establish that CI-994 generally improves cognitive function or acts as a cognitive enhancer on its own. (LLM, conf=0.88)
Experimental — accuracy not yet measuredCI-994 is a molecular memory aid and promotes memory formation and cognitive function in vivo.
“CI-994 is a molecular memory aid and promotes memory formation and cognitive function in vivo [9, 17, 21–24].”
From CI-994 is a dual modulator of class I HDACs and Wnt/β-catenin signaling for the treatment of Alzheimer's disease (2026) · cites this paper as [17]
The Results section, “By Using HDAC2-Targeting HDAC Inhibitors, Remote Fear Memories Can Be Attenuated” (page unavailable), reports that CI-994 combined with recall and extinction training produced persistent extinction of remote fear memories in mice. This supports a role in memory updating in vivo, but not the broader claim that CI-994 promotes memory formation and cognitive function generally; the Results also state that the inhibitor alone had no behavioral effect. (LLM, conf=0.86)
Experimental — accuracy not yet measuredCI-994 is an orally bioavailable specific class I HDAC inhibitor which can cross the blood-brain barrier.
“CI-994 is an orally bioavailable specific class I HDAC inhibitor which can across the blood–brain barrier [16, 17].”
From CI-994 is a dual modulator of class I HDACs and Wnt/β-catenin signaling for the treatment of Alzheimer's disease (2026) · cites this paper as [17]
The Results section (“By Using HDAC2-Targeting HDAC Inhibitors, Remote Fear Memories Can Be Attenuated”; page unavailable) identifies CI-994 as a selective class I HDAC inhibitor and reports substantial brain levels after systemic administration, supporting its ability to reach the brain. It does not establish oral bioavailability: the reported administration was intraperitoneal. (LLM, conf=0.90)
Experimental — accuracy not yet measuredCI-994 acts as a memory enhancer in mouse models of neurodegenerative disorders.
“CI-994 acts as a memory enhancer and alleviates cognitive deficits in mouse models of neurodegenerative disorders [9, 17, 21–24].”
From CI-994 is a dual modulator of class I HDACs and Wnt/β-catenin signaling for the treatment of Alzheimer's disease (2026) · cites this paper as [17]
The Results section, “By Using HDAC2-Targeting HDAC Inhibitors, Remote Fear Memories Can Be Attenuated” (page unavailable), reports that CI-994 combined with extinction training persistently attenuated remote fear memories in fear-conditioned mice. This supports an effect on memory updating, but not the claim that CI-994 enhances memory in mouse models of neurodegenerative disorders; the passages found do not report such models. (LLM, conf=0.83)
Experimental — accuracy not yet measured
CI-994 can cross the blood-brain barrier.
“CI-994 can cross the blood–brain barrier and is a cognitive enhancer.”
From CI-994 is a dual modulator of class I HDACs and Wnt/β-catenin signaling for the treatment of Alzheimer's disease (2026) · cites this paper as [17]
CI-994 alleviates cognitive deficits in mouse models of neurodegenerative disorders.
“CI-994 acts as a memory enhancer and alleviates cognitive deficits in mouse models of neurodegenerative disorders [9, 17, 21–24].”
From CI-994 is a dual modulator of class I HDACs and Wnt/β-catenin signaling for the treatment of Alzheimer's disease (2026) · cites this paper as [17]
The Results section, “By Using HDAC2-Targeting HDAC Inhibitors, Remote Fear Memories Can Be Attenuated” (page unavailable), reports that CI-994 combined with extinction training persistently attenuated fear responses in conditioned mice. Our copy does not report alleviation of cognitive deficits in mouse models of neurodegenerative disorders; searches for “neurodegenerative” and “cognitive deficits” found no such result. (LLM, conf=0.72)
Experimental — accuracy not yet measured
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- Authors
- Gräff, J., Joseph, N. F., Horn, M. E., Samiei, A., Meng, J., Seo, J., Rei, D., Bero, A. W., Phan, T. X., Wagner, F., Holson, E., Xu, J., Sun, J., Neve, R. L., Mach, R. H., Haggarty, S. J., & Tsai, L.-H.
- Affiliations
- Broad Institute (US)
- Howard Hughes Medical Institute (US)
- Massachusetts Institute of Technology (US)
- Washington University in St. Louis (US)
- Corresponding author
- Tsai, Li-Huei
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2014-01
- Volume
- 156
- Issue
- 1-2
- Pages
- 261-276
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC3986862
- OpenAlex
- W2021415039
- Cited by
- 357
- References
- 75
- Citations by year
- 2026: 13 · 2025: 22 · 2024: 21 · 2023: 20 · 2022: 28 · 2021: 27 · 2020: 25 · 2019: 22 · 2018: 45 · 2017: 32 · 2016: 34 · 2015: 32 · 2014: 36
- FWCI
- 22.87
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health
- National Institute on Aging
- National Institute on Drug Abuse (R01DA028301)
- National Institute of Neurological Disorders and Stroke (NS078839, R03NS090214, R01NS078839)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Social Sciences › Psychology › Clinical Psychology › Posttraumatic Stress Disorder Research
- Keywords
- memory reconsolidation, HDAC2, S-nitrosylation, histone acetylation, hippocampal plasticity, histone deacetylase inhibitors, anxiety disorders, memory retrieval, synaptic plasticity
- MeSH terms
- Animals, Fear, Hippocampus, Male, Mice, Inbred C57BL, Neuronal Plasticity, Epigenesis, Genetic, Mice, Histone Deacetylase 2, Histone Deacetylase Inhibitors, Memory, Long-Term, Transcriptome
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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 ›
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