{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T04:21:24Z","timestamp":1787026884961,"version":"build-2736575974"},"reference-count":81,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,12,3]],"date-time":"2025-12-03T00:00:00Z","timestamp":1764720000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Integr. Neurosci."],"abstract":"<jats:p>\n                    Acquired spatial representations are not static. Each re-exposure to the spatial environment stimulates retrieval of the stored experience followed by information re-encoding, including updating if the environment has changed. It remains unclear if the same neurons are involved in these three events. Here, we used a multiplexed fluorescence\n                    <jats:italic>in situ<\/jats:italic>\n                    hybridization (FISH) approach that detected \u201ctime-locked\u201d nuclear immediate early gene (IEG) expression to identify hippocampal neuronal ensembles that were engaged in the acquisition of a spatial representation, as well as its subsequent stabilization and\/or updating. Responses were assessed in distal CA1 (dCA1) and proximal CA1 (pCA1) of the dorsal hippocampus of male rats. Homer1a was used to detect neuronal recruitment triggered by novel learning of a holeboard environment (HB). cFos and Arc expression were used to detect ensemble stability and\/or expansion, or ensemble remodeling, respectively, that was triggered by animal exposure to the now familiar HB that included novel objects (HBO) 25 min after the initial HB exposure. Novel HB exposure resulted in nuclear Homer1a expression in both dCA1 and pCA1. Subsequent HBO triggered significant cFos and Arc expression only in dCA1. IEG co-labeling (Homer1a\/cFos, Homer1a\/Arc and Homer1a\/cFos\/Arc) was also only evident in dCA1, reflecting both re-iteration and remodeling of dCA1, but not pCA1 ensembles.\n                  <\/jats:p>\n                  <jats:p>In sum, we show that the contiguous acquisition and updating of spatial representations recruits distinct populations of CA1-neurons reflecting ensemble selection and stabilization, as well as ensemble remodeling. Moreover, whereas dCA1 and pCA1 are involved in the acquisition of the original spatial representation, only dCA1 is engaged in representation updating related to changes in spatial content information.<\/jats:p>","DOI":"10.3389\/fnint.2025.1660536","type":"journal-article","created":{"date-parts":[[2025,12,3]],"date-time":"2025-12-03T06:33:25Z","timestamp":1764743605000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":1,"title":["Multiplexed detection of nuclear immediate early gene expression reveals hippocampal neuronal subpopulations that engage in the acquisition and updating of spatial experience"],"prefix":"10.3389","volume":"19","author":[{"given":"Thu-Huong","family":"Hoang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Denise","family":"Manahan-Vaughan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2025,12,3]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"811","DOI":"10.1002\/hipo.23506","article-title":"The medial entorhinal cortex is necessary for the stimulus control over hippocampal place fields by distal, but not proximal, landmarks.","volume":"33","author":"Allison","year":"2023","journal-title":"Hippocampus"},{"key":"B2","doi-asserted-by":"publisher","first-page":"571","DOI":"10.1016\/0306-4522(89)90424-7","article-title":"The three-dimensional organization of the hippocampal formation: A review of anatomical data.","volume":"31","author":"Amaral","year":"1989","journal-title":"Neuroscience"},{"key":"B3","doi-asserted-by":"publisher","first-page":"8710","DOI":"10.1523\/jneurosci.20-23-08710.2000","article-title":"Dendritic and axonal targeting of Type 5 metabotropic glutamate receptor is regulated by homer1 proteins and neuronal excitation.","volume":"20","author":"Ango","year":"2000","journal-title":"J. Neurosci."},{"key":"B4","doi-asserted-by":"publisher","first-page":"640","DOI":"10.1016\/j.celrep.2018.09.064","article-title":"Long-Term consolidation of ensemble neural plasticity patterns in hippocampal area CA1.","volume":"25","author":"Attardo","year":"2018","journal-title":"Cell Rep."},{"key":"B5","doi-asserted-by":"publisher","first-page":"112999","DOI":"10.1016\/j.celrep.2023.112999","article-title":"Adaptive expression of engrams by retroactive interference.","volume":"42","author":"Autore","year":"2023","journal-title":"Cell Rep."},{"key":"B6","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1523\/JNEUROSCI.22-01-00167.2002","article-title":"Synaptic activity-induced conversion of intronic to exonic sequence in Homer 1 immediate early gene expression.","volume":"22","author":"Bottai","year":"2002","journal-title":"J. Neurosci."},{"key":"B7","doi-asserted-by":"publisher","first-page":"284","DOI":"10.1038\/386284a0","article-title":"Homer: A protein that selectively binds metabotropic glutamate receptors","volume":"386","author":"Brakeman","year":"1997","journal-title":"Nature"},{"key":"B8","doi-asserted-by":"publisher","first-page":"783","DOI":"10.1002\/hipo.20929","article-title":"The influence of objects on place field expression and size in distal hippocampal CA1.","volume":"21","author":"Burke","year":"2011","journal-title":"Hippocampus"},{"key":"B9","doi-asserted-by":"publisher","first-page":"803574","DOI":"10.3389\/fnbeh.2021.803574","article-title":"Bidirectional regulation of hippocampal synaptic plasticity and modulation of cumulative spatial memory by dopamine D2-Like receptors.","volume":"15","author":"Caragea","year":"2021","journal-title":"Front. Behav. Neurosci."},{"key":"B10","doi-asserted-by":"publisher","first-page":"92","DOI":"10.1016\/j.neurobiolaging.2022.12.007","article-title":"Ensemble-specific deficit in neuronal intrinsic excitability in aged mice","volume":"123","author":"Chen","year":"2022","journal-title":"Neurobiol. Aging"},{"key":"B11","doi-asserted-by":"publisher","first-page":"736","DOI":"10.1016\/j.neuron.2019.08.017","article-title":"Input-Specific metaplasticity in the visual cortex requires homer1a-mediated mGluR5 signaling.","volume":"104","author":"Chokshi","year":"2019","journal-title":"Neuron"},{"key":"B12","doi-asserted-by":"publisher","first-page":"445","DOI":"10.1016\/j.neuron.2006.08.033","article-title":"Arc\/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking.","volume":"52","author":"Chowdhury","year":"2006","journal-title":"Neuron"},{"key":"B13","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1159\/000500267","article-title":"Regulation and function of activity-dependent homer in synaptic plasticity.","volume":"5","author":"Clifton","year":"2019","journal-title":"Mol. Neuropsychiatry"},{"key":"B14","doi-asserted-by":"publisher","first-page":"54","DOI":"10.1523\/JNEUROSCI.0741-19.2019","article-title":"Five decades of hippocampal place cells and EEG rhythms in behaving rats.","volume":"40","author":"Colgin","year":"2020","journal-title":"J. Neurosci."},{"key":"B15","doi-asserted-by":"publisher","first-page":"477","DOI":"10.1016\/0306-4522(94)00355-9","article-title":"Pattern and time course of immediate early gene expression in rat brain following acute stress.","volume":"64","author":"Cullinan","year":"1995","journal-title":"Neuroscience"},{"key":"B16","doi-asserted-by":"publisher","first-page":"460","DOI":"10.1016\/j.tics.2011.08.005","article-title":"On the usefulness of \u2018what\u2019 and \u2018where\u2019 pathways in vision.","volume":"15","author":"de Haan","year":"2011","journal-title":"Trends Cogn. Sci."},{"key":"B17","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1016\/s0091-3057(81)80015-9","article-title":"Sexual dimorphism in the hormonal control of aggressive behavior of rats.","volume":"14","author":"DeBold","year":"1981","journal-title":"Pharmacol. Biochem. Behav."},{"key":"B18","doi-asserted-by":"publisher","first-page":"113414","DOI":"10.1016\/j.bbr.2021.113414","article-title":"Spatial working memory in rats: Crucial role of the hippocampus in the allothetic place avoidance alternation task demanding stimuli segregation.","volume":"412","author":"Duda","year":"2021","journal-title":"Behav. Brain Res."},{"key":"B19","doi-asserted-by":"publisher","first-page":"4481","DOI":"10.1523\/jneurosci.4944-13.2014","article-title":"Selective localization ofArcmRNA in dendrites involves activity- and translation-dependent mRNA degradation.","volume":"34","author":"Farris","year":"2014","journal-title":"J. Neurosci."},{"key":"B20","volume-title":"The endothelium: Multiple functions of the endothelial cells - focus on endothelium-derived vasoactive mediators.","author":"F\u00e9l\u00e9tou","year":"2011"},{"key":"B21","doi-asserted-by":"publisher","first-page":"428","DOI":"10.1038\/s41583-024-00817-x","article-title":"Remapping revisited: How the hippocampus represents different spaces.","volume":"25","author":"Fenton","year":"2024","journal-title":"Nat. Rev. Neurosci."},{"key":"B22","doi-asserted-by":"publisher","first-page":"R559","DOI":"10.1016\/j.cub.2024.05.007","article-title":"Engrams.","volume":"34","author":"Frankland","year":"2024","journal-title":"Curr. Biol."},{"key":"B23","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1002\/hipo.22072","article-title":"Endogenous hippocampal LTD that is enabled by spatial object recognition requires activation of NMDA receptors and the metabotropic glutamate receptor, mGlu5.","volume":"23","author":"Goh","year":"2013","journal-title":"Hippocampus"},{"key":"B24","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1002\/hipo.23395","article-title":"London taxi drivers: A review of neurocognitive studies and an exploration of how they build their cognitive map of London.","volume":"32","author":"Griesbauer","year":"2022","journal-title":"Hippocampus"},{"key":"B25","doi-asserted-by":"publisher","first-page":"61","DOI":"10.3389\/fncir.2016.00061","article-title":"How does the sparse memory \u201cEngram\u201d neurons encode the memory of a spatial\u2013temporal event?","volume":"10","author":"Guan","year":"2016","journal-title":"Front. Neural Circuits"},{"key":"B26","doi-asserted-by":"publisher","first-page":"256","DOI":"10.1016\/j.neurobiolaging.2021.01.019","article-title":"Engram reactivation during memory retrieval predicts long-term memory performance in aged mice.","volume":"101","author":"Gulmez Karaca","year":"2021","journal-title":"Neurobiol. Aging"},{"key":"B27","doi-asserted-by":"publisher","first-page":"1120","DOI":"10.1038\/16046","article-title":"Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles.","volume":"2","author":"Guzowski","year":"1999","journal-title":"Nat. Neurosci."},{"key":"B28","doi-asserted-by":"publisher","first-page":"20230229","DOI":"10.1098\/rstb.2023.0229","article-title":"Interplay of hippocampal long-term potentiation and long-term depression in enabling memory representations.","volume":"379","author":"Hagena","year":"2024","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"B29","doi-asserted-by":"publisher","first-page":"e2402356122","DOI":"10.1073\/pnas.2402356122","article-title":"Oppositional and competitive instigation of hippocampal synaptic plasticity by the VTA and locus coeruleus.","volume":"122","author":"Hagena","year":"2025","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B30","doi-asserted-by":"publisher","first-page":"315","DOI":"10.1002\/hipo.22833","article-title":"Novel encoding and updating of positional, or directional, spatial cues are processed by distinct hippocampal subfields: Evidence for parallel information processing and the \u201cwhat\u201d stream.","volume":"28","author":"Hoang","year":"2018","journal-title":"Hippocampus"},{"key":"B31","doi-asserted-by":"publisher","first-page":"897","DOI":"10.1002\/hipo.23333","article-title":"Hippocampal subfield-specific Homer1a expression is triggered by learning-facilitated long-term potentiation and long-term depression at medial perforant path synapses.","volume":"31","author":"Hoang","year":"2021","journal-title":"Hippocampus"},{"key":"B32","doi-asserted-by":"publisher","first-page":"639","DOI":"10.1007\/s00429-023-02694-z","article-title":"Differentiated somatic gene expression is triggered in the dorsal hippocampus and the anterior retrosplenial cortex by hippocampal synaptic plasticity prompted by spatial content learning.","volume":"229","author":"Hoang","year":"2024","journal-title":"Brain Struct. Funct."},{"key":"B33","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1016\/j.physbeh.2016.11.015","article-title":"Changes in acoustic startle reflex in rats induced by playback of 22-kHz calls.","volume":"169","author":"Inagaki","year":"2017","journal-title":"Physiol. Behav."},{"key":"B34","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/j.bbr.2012.09.011","article-title":"Sleep-dependency of episodic-like memory consolidation in rats.","volume":"237","author":"Inostroza","year":"2013","journal-title":"Behav. Brain Res."},{"key":"B35","doi-asserted-by":"publisher","first-page":"8192","DOI":"10.1073\/pnas.0402650101","article-title":"Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition.","volume":"101","author":"Kemp","year":"2004","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B36","doi-asserted-by":"publisher","first-page":"1326","DOI":"10.1093\/cercor\/bhm164","article-title":"Beta-adrenoreceptors comprise a critical element in learning-facilitated long-term plasticity.","volume":"18","author":"Kemp","year":"","journal-title":"Cereb. Cortex"},{"key":"B37","doi-asserted-by":"publisher","first-page":"968","DOI":"10.1093\/cercor\/bhm136","article-title":"The hippocampal CA1 region and dentate gyrus differentiate between environmental and spatial feature encoding through long-term depression.","volume":"18","author":"Kemp","year":"","journal-title":"Cereb. Cortex"},{"key":"B38","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1016\/j.bbr.2013.04.036","article-title":"Learning-facilitated long-term depression requires activation of the immediate early gene, c-fos, and is transcription dependent.","volume":"254","author":"Kemp","year":"2013","journal-title":"Behav. Brain Res."},{"key":"B39","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1016\/j.beproc.2012.09.018","article-title":"Role of the hippocampus in mediating interference as measured by pattern separation processes.","volume":"93","author":"Kesner","year":"2013","journal-title":"Behav. Processes"},{"key":"B40","doi-asserted-by":"publisher","first-page":"735","DOI":"10.1038\/s41586-025-08993-1","article-title":"Systems consolidation reorganizes hippocampal engram circuitry.","volume":"643","author":"Ko","year":"2025","journal-title":"Nature"},{"key":"B41","doi-asserted-by":"publisher","first-page":"108057","DOI":"10.1016\/j.nlm.2025.108057","article-title":"The molecular and cellular basis of memory engrams: Mechanisms of synaptic and systems consolidation.","volume":"219","author":"Kupke","year":"2025","journal-title":"Neurobiol. Learn. Mem."},{"key":"B42","doi-asserted-by":"publisher","first-page":"4999","DOI":"10.1523\/JNEUROSCI.2799-18.2019","article-title":"HDAC3-Mediated repression of the Nr4a family contributes to age-related impairments in long-term memory.","volume":"39","author":"Kwapis","year":"2019","journal-title":"J. Neurosci."},{"key":"B43","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1016\/j.conb.2020.03.004","article-title":"Parallel processing streams in the hippocampus.","volume":"64","author":"Lee","year":"2020","journal-title":"Curr. Opin. Neurobiol."},{"key":"B44","doi-asserted-by":"publisher","first-page":"162","DOI":"10.1038\/nn790","article-title":"Differential contribution of NMDA receptors in hippocampal subregions to spatial working memory.","volume":"5","author":"Lee","year":"2002","journal-title":"Nat. Neurosci."},{"key":"B45","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1016\/0896-6273(95)90299-6","article-title":"Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites.","volume":"14","author":"Lyford","year":"1995","journal-title":"Neuron"},{"key":"B46","article-title":"Learning-Related hippocampal long-term potentiation and long-term depression","volume-title":"Learning and memory: A comprehensive reference (second edition). reference module in neuroscience and biobehavioral psychology","author":"Manahan-Vaughan","year":"2017"},{"key":"B47","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/B978-0-12-812012-5.00019-7","article-title":"Item-place encoding through hippocampal long-term depression","volume-title":"Handbook of object novelty recognition","author":"Manahan-Vaughan","year":"2018"},{"key":"B48","doi-asserted-by":"publisher","first-page":"8739","DOI":"10.1073\/pnas.96.15.8739","article-title":"Novelty acquisition is associated with induction of hippocampal long-term depression.","volume":"96","author":"Manahan-Vaughan","year":"1999","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B49","doi-asserted-by":"publisher","first-page":"10445","DOI":"10.1523\/jneurosci.2883-07.2007","article-title":"Sustained Arc\/Arg3.1 synthesis controls long-term potentiation consolidation through regulation of local actin polymerization in the dentate gyrusin vivo.","volume":"27","author":"Messaoudi","year":"2007","journal-title":"J. Neurosci."},{"key":"B50","doi-asserted-by":"publisher","first-page":"1024","DOI":"10.1016\/j.neuron.2013.04.036","article-title":"Arc\/Arg3.1 is a postsynaptic mediator of activity-dependent synapse elimination in the developing cerebellum.","volume":"78","author":"Mikuni","year":"2013","journal-title":"Neuron"},{"key":"B51","doi-asserted-by":"publisher","first-page":"78","DOI":"10.3389\/fnmol.2015.00078","article-title":"Role of immediate-early genes in synaptic plasticity and neuronal ensembles underlying the memory trace.","volume":"8","author":"Minatohara","year":"2015","journal-title":"Front. Mol. Neurosci."},{"key":"B52","doi-asserted-by":"publisher","first-page":"12931","DOI":"10.1073\/pnas.1104495108","article-title":"Identification of transmitter systems and learning tag molecules involved in behavioral tagging during memory formation.","volume":"108","author":"Moncada","year":"2011","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B53","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1002\/hipo.1028","article-title":"Reciprocal connections between the entorhinal cortex and hippocampal fields CA1 and the subiculum are in register with the projections from CA1 to the subiculum.","volume":"11","author":"Naber","year":"2001","journal-title":"Hippocampus"},{"key":"B54","doi-asserted-by":"publisher","first-page":"394","DOI":"10.1016\/j.neuron.2021.12.012","article-title":"Spatial goal coding in the hippocampal formation.","volume":"110","author":"Nyberg","year":"2022","journal-title":"Neuron"},{"key":"B55","doi-asserted-by":"publisher","first-page":"886","DOI":"10.1016\/j.cell.2012.02.062","article-title":"Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc\/Arg3.1 with CaMKIIbeta.","volume":"149","author":"Okuno","year":"2012","journal-title":"Cell"},{"key":"B56","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1016\/j.semcdb.2017.09.025","article-title":"Inverse synaptic tagging: An inactive synapse-specific mechanism to capture activity-induced Arc\/arg3.1 and to locally regulate spatial distribution of synaptic weights.","volume":"77","author":"Okuno","year":"2018","journal-title":"Semin. Cell Dev. Biol."},{"key":"B57","doi-asserted-by":"publisher","first-page":"1017","DOI":"10.14670\/HH-25.1017","article-title":"Sudan Black B treatment reduces autofluorescence and improves resolution of in situ hybridization specific fluorescent signals of brain sections.","volume":"25","author":"Oliveira","year":"2010","journal-title":"Histol. Histopathol."},{"key":"B58","doi-asserted-by":"publisher","first-page":"70","DOI":"10.1016\/j.neuron.2008.05.023","article-title":"Elongation Factor 2 and Fragile X Mental Retardation Protein Control the Dynamic Translation of Arc\/Arg3.1 Essential for mGluR-LTD.","volume":"59","author":"Park","year":"2008","journal-title":"Neuron"},{"key":"B59","volume-title":"Paxinos and Watson\u2019s the rat brain instereotaxic coordinates","author":"Paxinos","year":"2014"},{"key":"B60","doi-asserted-by":"publisher","first-page":"18173","DOI":"10.1073\/pnas.1006546107","article-title":"Arc regulates spine morphology and maintains network stability in vivo.","volume":"107","author":"Peebles","year":"2010","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B61","doi-asserted-by":"publisher","first-page":"575915","DOI":"10.3389\/fncel.2020.575915","article-title":"Engrams of fast learning.","volume":"14","author":"Piette","year":"2020","journal-title":"Front. Cell. Neurosci."},{"key":"B62","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1016\/j.neuron.2006.08.024","article-title":"Arc\/Arg3.1 is essential for the consolidation of synaptic plasticity and memories.","volume":"52","author":"Plath","year":"2006","journal-title":"Neuron"},{"key":"B63","doi-asserted-by":"publisher","first-page":"501","DOI":"10.1093\/cercor\/bhq093","article-title":"Involvement of the metabotropic glutamate receptor mGluR5 in NMDA receptor-dependent, learning-facilitated long-term depression in CA1 synapses.","volume":"21","author":"Popkirov","year":"2011","journal-title":"Cereb. Cortex"},{"key":"B64","doi-asserted-by":"publisher","first-page":"994","DOI":"10.1016\/j.tics.2020.09.012","article-title":"No pattern separation in the human hippocampus.","volume":"24","author":"Quian Quiroga","year":"2020","journal-title":"Trends Cogn. Sci."},{"key":"B65","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1016\/j.conb.2020.03.015","article-title":"Finding order in slow axonal transport.","volume":"63","author":"Roy","year":"2020","journal-title":"Curr. Opin. Neurobiol."},{"key":"B66","doi-asserted-by":"publisher","first-page":"65","DOI":"10.21926\/obm.genet.1901065","article-title":"New tools in cognitive neurobiology: Biotin-digoxigenin detection of overlapping active neuronal populations by two-color c-fos compartment analysis of temporal activity by fluorescent in situ hybridization (catFISH).","volume":"3","author":"Saidov","year":"2018","journal-title":"OBM Genet."},{"key":"B67","doi-asserted-by":"publisher","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: An open-source platform for biological-image analysis.","volume":"9","author":"Schindelin","year":"2012","journal-title":"Nat. Methods"},{"key":"B68","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1097\/00001756-199101000-00004","article-title":"Activation of immediate early genes after acute stress.","volume":"2","author":"Schreiber","year":"1991","journal-title":"Neuroreport"},{"key":"B69","doi-asserted-by":"publisher","first-page":"279","DOI":"10.1038\/nn.2708","article-title":"New views of Arc, a master regulator of synaptic plasticity.","volume":"14","author":"Shepherd","year":"2011","journal-title":"Nat. Neurosci."},{"key":"B70","doi-asserted-by":"publisher","first-page":"284","DOI":"10.1016\/j.tins.2022.01.007","article-title":"Mechanistic flexibility of the retrosplenial cortex enables its contribution to spatial cognition.","volume":"45","author":"Stacho","year":"2022","journal-title":"Trends Neurosci."},{"key":"B71","doi-asserted-by":"publisher","first-page":"423","DOI":"10.1016\/j.tics.2021.02.005","article-title":"Pattern separation in the human hippocampus: Response to quiroga.","volume":"25","author":"Suthana","year":"2021","journal-title":"Trends Cogn. Sci."},{"key":"B72","doi-asserted-by":"publisher","first-page":"485","DOI":"10.1038\/s41583-018-0031-2","article-title":"The role of engram cells in the systems consolidation of memory.","volume":"19","author":"Tonegawa","year":"2018","journal-title":"Nat. Rev. Neurosci."},{"key":"B73","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2307275120","article-title":"Cell-type-specific optogenetic stimulation of the locus coeruleus induces slow-onset potentiation and enhances everyday memory in rats.","volume":"120","author":"Tse","year":"2023","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B74","doi-asserted-by":"publisher","first-page":"881","DOI":"10.1002\/hipo.23331","article-title":"Object and object-memory representations across the proximodistal axis of CA1.","volume":"31","author":"Vandrey","year":"2021","journal-title":"Hippocampus"},{"key":"B75","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1007\/978-3-031-62983-9_4","article-title":"Hippocampal engrams and contextual memory.","volume":"38","author":"Vasudevan","year":"2024","journal-title":"Adv. Neurobiol."},{"key":"B76","doi-asserted-by":"publisher","first-page":"6489","DOI":"10.1523\/jneurosci.0350-04.2004","article-title":"Differences in hippocampal neuronal population responses to modifications of an environmental context: Evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles.","volume":"24","author":"Vazdarjanova","year":"2004","journal-title":"J. Neurosci."},{"key":"B77","doi-asserted-by":"publisher","first-page":"10067","DOI":"10.1523\/JNEUROSCI.22-23-10067.2002","article-title":"Experience-dependent coincident expression of the effector immediate-early genes arc and Homer 1a in hippocampal and neocortical neuronal networks.","volume":"22","author":"Vazdarjanova","year":"2002","journal-title":"J. Neurosci."},{"key":"B78","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1016\/j.semcdb.2017.09.035","article-title":"Roles for Arc in metabotropic glutamate receptor-dependent LTD and synapse elimination: Implications in health and disease.","volume":"77","author":"Wilkerson","year":"2018","journal-title":"Sem. Cell Dev. Biol."},{"key":"B79","doi-asserted-by":"publisher","first-page":"515","DOI":"10.1016\/j.tins.2011.06.006","article-title":"Pattern separation in the hippocampus.","volume":"34","author":"Yassa","year":"2011","journal-title":"Trends Neurosci."},{"key":"B80","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1007\/978-3-031-62983-9_6","article-title":"All IEGs are not created equal-molecular sorting within the memory engram.","volume":"38","author":"Yelhekar","year":"2024","journal-title":"Adv. Neurobiol."},{"key":"B81","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.neuroscience.2004.07.030","article-title":"Hippocampal N-methyl-D-aspartate receptor-mediated encoding and retrieval processes in spatial working memory: Delay-interposed radial maze performance in rats.","volume":"129","author":"Yoshihara","year":"2004","journal-title":"Neuroscience"}],"container-title":["Frontiers in Integrative Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnint.2025.1660536\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,12,3]],"date-time":"2025-12-03T06:33:28Z","timestamp":1764743608000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnint.2025.1660536\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,12,3]]},"references-count":81,"alternative-id":["10.3389\/fnint.2025.1660536"],"URL":"https:\/\/doi.org\/10.3389\/fnint.2025.1660536","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2025.07.06.663345","asserted-by":"object"}]},"ISSN":["1662-5145"],"issn-type":[{"value":"1662-5145","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,12,3]]},"article-number":"1660536"}}