{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,14]],"date-time":"2026-09-14T10:46:16Z","timestamp":1789382776928,"version":"build-2803163510"},"reference-count":95,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,7,7]],"date-time":"2022-07-07T00:00:00Z","timestamp":1657152000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000071","name":"National Institute of Child Health and Human Development","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000071","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000025","name":"National Institute of Mental Health","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000025","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000049","name":"National Institute on Aging","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000049","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000065","name":"National Institute of Neurological Disorders and Stroke","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000065","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Behav. Neurosci."],"abstract":"<jats:p>Altered fear learning is a strong behavioral component of anxiety disorders such as post-traumatic stress disorder (PTSD). Recent efforts have attempted to combine exposure therapies with drugs that target fear memory retrieval and memory reconsolidation, in order to improve treatment efficacy. The noradrenergic (NA) signaling system is of particular interest, due to its role in regulating the stress response and its involvement in fear and learning processes. Importantly, propranolol (P), a non-selective \u03b2-adrenergic antagonist, has shown the potential in decreasing exaggerated fear in both humans and animal models. In a previous study, we utilized an activity-dependent tagging murine model to determine the neural mechanisms by which propranolol attenuates learned fear. We found that propranolol acutely decreased memory trace reactivation specifically in the dorsal dentate gyrus (dDG), but not in CA3 or CA1. Here, we extended our previous study by investigating whether propranolol additionally altered activity in the hilus, a polymorphic layer that consists of neurons, mossy cells, and GABAergic interneurons. We found that propranolol acutely reduced overall hilar activity in both the dorsal and ventral hilus. Moreover, we report that propranolol significantly altered the activity of parvalbumin (PV)<jats:sup>+<\/jats:sup> cells in the ventral (vDG), but not dorsal DG (dDG). Together, these results suggest that a \u03b2-adrenergic blockade may affect the activity of excitatory and inhibitory cell types in the hilar layer of the DG, and that these alterations may contribute to manipulating fear memory traces.<\/jats:p>","DOI":"10.3389\/fnbeh.2022.919831","type":"journal-article","created":{"date-parts":[[2022,7,7]],"date-time":"2022-07-07T08:40:22Z","timestamp":1657183222000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":7,"title":["Propranolol Administration Modulates Neural Activity in the Hippocampal Hilus During Fear Retrieval"],"prefix":"10.3389","volume":"16","author":[{"given":"Sofia","family":"Leal Santos","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Briana K.","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guilherme R.","family":"Pereira","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vananh","family":"Pham","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christine A.","family":"Denny","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,7,7]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/S0079-6123(07)63001-5","article-title":"The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies).","volume":"163","author":"Amaral","year":"2007","journal-title":"Prog. Brain Res."},{"key":"B2","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1038\/s41586-018-0262-4","article-title":"Hippocampal neurogenesis confers stress resilience by inhibiting the ventral dentate gyrus.","volume":"559","author":"Anacker","year":"2018","journal-title":"Nature"},{"key":"B3","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.brainres.2016.03.001","article-title":"Locus coeruleus: From global projection system to adaptive regulation of behavior.","volume":"1645","author":"Aston-Jones","year":"2016","journal-title":"Brain Res."},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.3389\/fncir.2017.00108","article-title":"Neuromodulatory Systems and Their Interactions: A Review of Models, Theories, and Experiments.","volume":"11","author":"Avery","year":"2017","journal-title":"Front. Neural. Circuits"},{"key":"B5","doi-asserted-by":"publisher","first-page":"11406","DOI":"10.1073\/pnas.1936664100","article-title":"Beta-arrestin-mediated activation of MAPK by inverse agonists reveals distinct active conformations for G protein-coupled receptors.","volume":"100","author":"Azzi","year":"2003","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B6","doi-asserted-by":"crossref","first-page":"1312","DOI":"10.1124\/mol.63.6.1312","article-title":"Agonist actions of \u201cbeta-blockers\u201d provide evidence for two agonist activation sites or conformations of the human beta1-adrenoceptor.","volume":"63","author":"Baker","year":"2003","journal-title":"Mol. Pharmacol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1016\/j.neubiorev.2004.03.004","article-title":"Regional dissociations within the hippocampus\u2013memory and anxiety.","volume":"28","author":"Bannerman","year":"2004","journal-title":"Neurosci. Biobehav. Rev."},{"key":"B8","doi-asserted-by":"publisher","first-page":"1170","DOI":"10.1037\/\/0735-7044.113.6.1170","article-title":"Double dissociation of function within the hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions.","volume":"113","author":"Bannerman","year":"1999","journal-title":"Behav. Neurosci."},{"key":"B9","doi-asserted-by":"crossref","DOI":"10.7573\/dic.212286","article-title":"Alpha-2 receptor agonists for the treatment of posttraumatic stress disorder.","volume":"4","author":"Belkin","year":"2015","journal-title":"Drugs Context"},{"key":"B10","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1016\/S0921-0709(05)80025-2","article-title":"Chapter 4.3 The locus coeruleus-noradrenergic system and stress: modulation of arousal state and state-dependent behavioral processes.","volume":"15","author":"Berridge","year":"2005","journal-title":"Tech. Behav. Neural Sci."},{"key":"B11","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1016\/s0165-0173(03)00143-7","article-title":"The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes.","volume":"42","author":"Berridge","year":"2003","journal-title":"Brain Res. Brain Res. Rev."},{"key":"B12","doi-asserted-by":"publisher","first-page":"1628","DOI":"10.1038\/s41593-018-0241-y","article-title":"Integration of gene expression and brain-wide connectivity reveals the multiscale organization of mouse hippocampal networks.","volume":"21","author":"Bienkowski","year":"2018","journal-title":"Nat. Neurosci."},{"key":"B13","doi-asserted-by":"publisher","first-page":"206","DOI":"10.1002\/syn.890130303","article-title":"Beta-adrenergic receptors in the hippocampal and retrohippocampal regions of rats and guinea pigs: autoradiographic and immunohistochemical studies.","volume":"13","author":"Booze","year":"1993","journal-title":"Synapse"},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.1007\/s11920-017-0788-4","article-title":"Recent Progress in Virtual Reality Exposure Therapy for Phobias: A Systematic Review.","volume":"19","author":"Botella","year":"2017","journal-title":"Curr. Psychiatry Rep."},{"key":"B15","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1176\/appi.ajp.2017.17050481","article-title":"Reduction of PTSD Symptoms With Pre-Reactivation Propranolol Therapy: A Randomized Controlled Trial.","volume":"175","author":"Brunet","year":"2018","journal-title":"Am. J. Psychiatry"},{"key":"B16","doi-asserted-by":"crossref","first-page":"752","DOI":"10.1002\/hipo.22556","article-title":"Improved specificity of hippocampal memory trace labeling.","volume":"26","author":"Cazzulino","year":"2016","journal-title":"Hippocampus"},{"key":"B17","doi-asserted-by":"publisher","first-page":"1885.e","DOI":"10.1016\/j.cub.2019.04.065","article-title":"Artificially Enhancing and Suppressing Hippocampus-Mediated Memories.","volume":"29","author":"Chen","year":"2019","journal-title":"Curr. Biol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"1614","DOI":"10.1038\/mp.2017.159","article-title":"Selective activation of parvalbumin interneurons prevents stress-induced synapse loss and perceptual defects.","volume":"23","author":"Chen","year":"2018","journal-title":"Mol. Psychiatry"},{"key":"B19","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1016\/j.neuroscience.2006.09.037","article-title":"Locus coeruleus activation by foot shock or electrical stimulation inhibits amygdala neurons.","volume":"144","author":"Chen","year":"2007","journal-title":"Neuroscience"},{"key":"B20","doi-asserted-by":"publisher","first-page":"551","DOI":"10.1002\/cne.21758","article-title":"Beta-adrenergic receptors are differentially expressed in distinct interneuron subtypes in the rat hippocampus.","volume":"509","author":"Cox","year":"2008","journal-title":"J. Comp. Neurol."},{"key":"B21","author":"De N\u00f3","year":"1934","journal-title":"Studies on the Structure of the Cerebral Cortex: continuation of the Study of the Ammonic System."},{"key":"B22","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1016\/j.neuron.2014.05.018","article-title":"Hippocampal memory traces are differentially modulated by experience, time, and adult neurogenesis.","volume":"83","author":"Denny","year":"2014","journal-title":"Neuron"},{"key":"B23","doi-asserted-by":"publisher","DOI":"10.3389\/fncir.2017.00023","article-title":"From Engrams to Pathologies of the Brain.","volume":"11","author":"Denny","year":"2017","journal-title":"Front. Neural. Circuits"},{"key":"B24","doi-asserted-by":"publisher","first-page":"13296","DOI":"10.1523\/JNEUROSCI.2843-08.2008","article-title":"New perspectives on beta-adrenergic mediation of innate and learned fear responses to predator odor.","volume":"28","author":"Do Monte","year":"2008","journal-title":"J. Neurosci."},{"key":"B25","doi-asserted-by":"publisher","first-page":"318","DOI":"10.1016\/j.nlm.2010.07.004","article-title":"Role of beta-adrenergic receptors in the ventromedial prefrontal cortex during contextual fear extinction in rats.","volume":"94","author":"Do-Monte","year":"2010","journal-title":"Neurobiol. Learn. Mem."},{"key":"B26","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1002\/hipo.22138","article-title":"Expression of c-fos in hilar mossy cells of the dentate gyrus in vivo.","volume":"23","author":"Duffy","year":"2013","journal-title":"Hippocampus"},{"key":"B27","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1016\/j.neuron.2009.05.026","article-title":"Amygdala inhibitory circuits and the control of fear memory.","volume":"62","author":"Ehrlich","year":"2009","journal-title":"Neuron"},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-018-06899-3","article-title":"Parvalbumin(+) interneurons obey unique connectivity rules and establish a powerful lateral-inhibition microcircuit in dentate gyrus.","volume":"9","author":"Espinoza","year":"2018","journal-title":"Nat. Commun."},{"key":"B29","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1159\/000118186","article-title":"Effect of beta-receptor blockade on anxiety with reference to the three-systems model of phobic behavior.","volume":"13","author":"Fagerstr\u00f6m","year":"1985","journal-title":"Neuropsychobiology"},{"key":"B30","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.neuron.2009.11.031","article-title":"Are the dorsal and ventral hippocampus functionally distinct structures?","volume":"65","author":"Fanselow","year":"2010","journal-title":"Neuron"},{"key":"B31","doi-asserted-by":"publisher","first-page":"E3729","DOI":"10.1073\/pnas.1500682112","article-title":"Noradrenergic blockade stabilizes prefrontal activity and enables fear extinction under stress.","volume":"112","author":"Fitzgerald","year":"2015","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B32","doi-asserted-by":"publisher","first-page":"1575","DOI":"10.1124\/mol.106.026716","article-title":"Distinct signaling profiles of beta1 and beta2 adrenergic receptor ligands toward adenylyl cyclase and mitogen-activated protein kinase reveals the pluridimensionality of efficacy.","volume":"70","author":"Galandrin","year":"2006","journal-title":"Mol. Pharmacol."},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.3389\/fnbeh.2018.00043","article-title":"Noradrenergic Modulation of Fear Conditioning and Extinction.","volume":"12","author":"Giustino","year":"2018","journal-title":"Front. Behav. Neurosci."},{"key":"B34","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.nlm.2016.01.009","article-title":"Revisiting propranolol and PTSD: Memory erasure or extinction enhancement?","volume":"130","author":"Giustino","year":"2016","journal-title":"Neurobiol. Learn. Mem."},{"key":"B35","doi-asserted-by":"publisher","first-page":"2537","DOI":"10.1038\/npp.2017.89","article-title":"\u03b2-Adrenoceptor Blockade in the Basolateral Amygdala, But Not the Medial Prefrontal Cortex, Rescues the Immediate Extinction Deficit.","volume":"42","author":"Giustino","year":"2017","journal-title":"Neuropsychopharmacology"},{"key":"B36","doi-asserted-by":"publisher","first-page":"342","DOI":"10.1007\/s00213-004-1819-5","article-title":"Effects of the beta-blocker propranolol on cued and contextual fear conditioning in humans.","volume":"175","author":"Grillon","year":"2004","journal-title":"Psychopharmacology"},{"key":"B37","doi-asserted-by":"publisher","first-page":"298","DOI":"10.1016\/j.neuroscience.2007.01.013","article-title":"Cellular and subcellular distributions of beta1- and beta2-adrenoceptors in the CA1 and CA3 regions of the rat hippocampus.","volume":"146","author":"Guo","year":"2007","journal-title":"Neuroscience"},{"key":"B38","doi-asserted-by":"publisher","first-page":"1349","DOI":"10.1093\/cercor\/bhv330","article-title":"\u03b2-Adrenergic Control of Hippocampal Function: Subserving the Choreography of Synaptic Information Storage and Memory.","volume":"26","author":"Hagena","year":"2016","journal-title":"Cereb Cortex"},{"key":"B39","doi-asserted-by":"publisher","DOI":"10.3389\/fncir.2021.687558","article-title":"Hippocampal Somatostatin Interneurons, Long-Term Synaptic Plasticity and Memory.","volume":"15","author":"Honor\u00e9","year":"2021","journal-title":"Front. Neural. Circ."},{"key":"B40","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1016\/S0079-6123(07)63013-1","article-title":"Interneurons of the dentate gyrus: an overview of cell types, terminal fields and neurochemical identity.","volume":"163","author":"Houser","year":"2007","journal-title":"Prog. Brain Res."},{"key":"B41","doi-asserted-by":"publisher","first-page":"1839","DOI":"10.1017\/S0033291709992376","article-title":"Human amygdala reactivity is diminished by the \u03b2-noradrenergic antagonist propranolol.","volume":"40","author":"Hurlemann","year":"2010","journal-title":"Psychol. Med."},{"key":"B42","doi-asserted-by":"publisher","first-page":"1378","DOI":"10.1037\/0735-7044.117.6.1378","article-title":"Deficient spatial memory induced by blockade of beta-adrenoceptors in the hippocampal CA1 region.","volume":"117","author":"Ji","year":"2003","journal-title":"Behav. Neurosci."},{"key":"B43","doi-asserted-by":"publisher","DOI":"10.3389\/fnmol.2019.00070","article-title":"Reactivation of Recall-Induced Neurons in the Infralimbic Cortex and the Basolateral Amygdala After Remote Fear Memory Attenuation.","volume":"12","author":"Khalaf","year":"2019","journal-title":"Front. Mol. Neurosci."},{"key":"B44","doi-asserted-by":"publisher","first-page":"1239","DOI":"10.1126\/science.aas9875","article-title":"Reactivation of recall-induced neurons contributes to remote fear memory attenuation.","volume":"360","author":"Khalaf","year":"2018","journal-title":"Science"},{"key":"B45","doi-asserted-by":"publisher","first-page":"955","DOI":"10.1016\/j.neuron.2012.12.038","article-title":"Differential control of learning and anxiety along the dorsoventral axis of the dentate gyrus.","volume":"77","author":"Kheirbek","year":"2013","journal-title":"Neuron"},{"key":"B46","doi-asserted-by":"crossref","first-page":"10825","DOI":"10.1073\/pnas.152112399","article-title":"Reduced fear expression after lesions of the ventral hippocampus.","volume":"99","author":"Kjelstrup","year":"2002","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B47","doi-asserted-by":"crossref","first-page":"1569","DOI":"10.1038\/npp.2015.315","article-title":"How Administration of the Beta-Blocker Propranolol Before Extinction can Prevent the Return of Fear.","volume":"41","author":"Kroes","year":"2016","journal-title":"Neuropsychopharmacology"},{"key":"B48","doi-asserted-by":"publisher","first-page":"753","DOI":"10.1038\/s41593-019-0361-z","article-title":"Distinct hippocampal engrams control extinction and relapse of fear memory.","volume":"22","author":"Lacagnina","year":"2019","journal-title":"Nat. Neurosci."},{"key":"B49","doi-asserted-by":"publisher","first-page":"1150","DOI":"10.1016\/j.biopsych.2021.01.005","article-title":"Propranolol Decreases Fear Expression by Modulating Fear Memory Traces.","volume":"89","author":"Leal Santos","year":"2021","journal-title":"Biol. Psychiatry"},{"key":"B50","doi-asserted-by":"crossref","first-page":"5734","DOI":"10.1073\/pnas.92.12.5734","article-title":"Somatodendritic expression of an immediate early gene is regulated by synaptic activity.","volume":"92","author":"Link","year":"1995","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B51","doi-asserted-by":"crossref","first-page":"1306","DOI":"10.1177\/00220345910700091401","article-title":"Effect of a beta-adrenergic blocking agent on dental anxiety.","volume":"70","author":"Liu","year":"1991","journal-title":"J. Dent. Res."},{"key":"B52","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1038\/nature11028","article-title":"Optogenetic stimulation of a hippocampal engram activates fear memory recall.","volume":"484","author":"Liu","year":"2012","journal-title":"Nature"},{"key":"B53","doi-asserted-by":"publisher","first-page":"222","DOI":"10.1503\/jpn.120111","article-title":"Propranolol\u2019s effects on the consolidation and reconsolidation of long-term emotional memory in healthy participants: a meta-analysis.","volume":"38","author":"Lonergan","year":"2013","journal-title":"J. Psychiatry Neurosci."},{"key":"B54","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":"B55","doi-asserted-by":"publisher","first-page":"846","DOI":"10.1016\/j.biopsych.2018.02.011","article-title":"Ventral CA3 Activation Mediates Prophylactic Ketamine Efficacy Against Stress-Induced Depressive-like Behavior.","volume":"84","author":"Mastrodonato","year":"2018","journal-title":"Biol. Psychiatry"},{"key":"B56","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1586\/14737175.2014.934677","article-title":"Enhancing exposure therapy for anxiety disorders, obsessive-compulsive disorder and post-traumatic stress disorder.","volume":"14","author":"McGuire","year":"2014","journal-title":"Expert Rev. Neurother."},{"key":"B57","doi-asserted-by":"publisher","first-page":"178","DOI":"10.1002\/(SICI)1098-2396(20000601)36:3<178::AID-SYN3>3.0.CO;2-6","article-title":"beta-adrenergic receptors primarily are located on the dendrites of granule cells and interneurons but also are found on astrocytes and a few presynaptic profiles in the rat dentate gyrus.","volume":"36","author":"Milner","year":"2000","journal-title":"Synapse"},{"key":"B58","doi-asserted-by":"publisher","first-page":"2405","DOI":"10.1007\/s00429-016-1349-z","article-title":"Acute restraint stress decreases c-fos immunoreactivity in hilar mossy cells of the adult dentate gyrus.","volume":"222","author":"Moretto","year":"2017","journal-title":"Brain Struct. Funct."},{"key":"B59","doi-asserted-by":"crossref","first-page":"608","DOI":"10.1002\/(SICI)1098-1063(1998)8:6<608::AID-HIPO3>3.0.CO;2-7","article-title":"Functional differentiation in the hippocampus.","volume":"8","author":"Moser","year":"1998","journal-title":"Hippocampus"},{"key":"B60","doi-asserted-by":"publisher","first-page":"9697","DOI":"10.1073\/pnas.92.21.9697","article-title":"Spatial learning with a minislab in the dorsal hippocampus.","volume":"92","author":"Moser","year":"1995","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B61","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1101\/lm.1794710","article-title":"Limited efficacy of propranolol on the reconsolidation of fear memories.","volume":"17","author":"Muravieva","year":"2010","journal-title":"Learn. Mem."},{"key":"B62","article-title":"Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation.","volume":"8","author":"Ognjanovski","year":"2017","journal-title":"Nat. Communicat."},{"key":"B63","doi-asserted-by":"crossref","first-page":"275.e","DOI":"10.1016\/j.cell.2017.12.024","article-title":"The Neuronal Gene Arc Encodes a Repurposed Retrotransposon Gag Protein that Mediates Intercellular RNA Transfer.","volume":"172","author":"Pastuzyn","year":"2018","journal-title":"Cell"},{"key":"B64","doi-asserted-by":"publisher","first-page":"523","DOI":"10.1002\/hipo.22951","article-title":"Optimization of immunolabeling and clearing techniques for indelibly labeled memory traces.","volume":"28","author":"Pavlova","year":"2018","journal-title":"Hippocampus"},{"key":"B65","doi-asserted-by":"publisher","DOI":"10.1016\/j.ynstr.2021.100380","article-title":"Parvalbumin interneuron alterations in stress-related mood disorders: A systematic review.","volume":"15","author":"Perlman","year":"2021","journal-title":"Neurobiol. Stress"},{"key":"B66","doi-asserted-by":"publisher","first-page":"1110","DOI":"10.1002\/hipo.22756","article-title":"Optogenetic stimulation of dentate gyrus engrams restores memory in Alzheimer\u2019s disease mice.","volume":"27","author":"Perusini","year":"2017","journal-title":"Hippocampus"},{"key":"B67","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1002\/cne.901550103","article-title":"A radioautographic study of the efferent pathways of the nucleus locus coeruleus.","volume":"155","author":"Pickel","year":"1974","journal-title":"J. Comp. Neurol."},{"key":"B68","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1016\/j.bbrc.2008.01.007","article-title":"Are beta-adrenergic receptors in the hippocampal CA1 region required for retrieval of contextual fear memory?","volume":"368","author":"Qi","year":"2008","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"B69","doi-asserted-by":"publisher","first-page":"335","DOI":"10.1038\/nature14514","article-title":"Activating positive memory engrams suppresses depression-like behaviour.","volume":"522","author":"Ramirez","year":"2015","journal-title":"Nature"},{"key":"B70","doi-asserted-by":"publisher","first-page":"679","DOI":"10.1682\/jrrd.2011.08.0152","article-title":"Review of exposure therapy: a gold standard for PTSD treatment.","volume":"49","author":"Rauch","year":"2012","journal-title":"J. Rehabil. Res. Dev."},{"key":"B71","doi-asserted-by":"publisher","first-page":"426","DOI":"10.1038\/nature13725","article-title":"Bidirectional switch of the valence associated with a hippocampal contextual memory engram.","volume":"513","author":"Redondo","year":"2014","journal-title":"Nature"},{"key":"B72","doi-asserted-by":"crossref","first-page":"1230","DOI":"10.1126\/science.1143839","article-title":"Localization of a stable neural correlate of associative memory.","volume":"317","author":"Reijmers","year":"2007","journal-title":"Science"},{"key":"B73","doi-asserted-by":"publisher","first-page":"1189","DOI":"10.1037\/0735-7044.113.6.1189","article-title":"Dissociating context and space within the hippocampus: effects of complete, dorsal, and ventral excitotoxic hippocampal lesions on conditioned freezing and spatial learning.","volume":"113","author":"Richmond","year":"1999","journal-title":"Behav. Neurosci."},{"key":"B74","doi-asserted-by":"publisher","first-page":"887","DOI":"10.1016\/j.biopsych.2009.01.009","article-title":"Systemic propranolol acts centrally to reduce conditioned fear in rats without impairing extinction.","volume":"65","author":"Rodriguez-Romaguera","year":"2009","journal-title":"Biol. Psychiatry"},{"key":"B75","doi-asserted-by":"publisher","first-page":"508","DOI":"10.1038\/nature17172","article-title":"Memory retrieval by activating engram cells in mouse models of early Alzheimer\u2019s disease.","volume":"531","author":"Roy","year":"2016","journal-title":"Nature"},{"key":"B76","doi-asserted-by":"publisher","first-page":"562","DOI":"10.1038\/nrn.2016.87","article-title":"The enigmatic mossy cell of the dentate gyrus.","volume":"17","author":"Scharfman","year":"2016","journal-title":"Nat. Rev. Neurosci."},{"key":"B77","doi-asserted-by":"publisher","DOI":"10.3389\/fncir.2012.00106","article-title":"Hilar mossy cells of the dentate gyrus: a historical perspective.","volume":"6","author":"Scharfman","year":"2012","journal-title":"Front. Neural. Circuits"},{"key":"B78","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":"B79","doi-asserted-by":"publisher","DOI":"10.3389\/fnbeh.2017.00065","article-title":"In Search for Boundary Conditions of Reconsolidation: A Failure of Fear Memory Interference.","volume":"11","author":"Schroyens","year":"2017","journal-title":"Front. Behav. Neurosci."},{"key":"B80","doi-asserted-by":"publisher","first-page":"380","DOI":"10.1016\/j.biopsych.2011.10.028","article-title":"Neural signature of reconsolidation impairments by propranolol in humans.","volume":"71","author":"Schwabe","year":"2012","journal-title":"Biol. Psychiatry"},{"key":"B81","doi-asserted-by":"crossref","first-page":"R1051","DOI":"10.1016\/j.cub.2015.09.039","article-title":"Organization of the locus coeruleus-norepinephrine system.","volume":"25","author":"Schwarz","year":"2015","journal-title":"Curr. Biol."},{"key":"B82","author":"Semon","year":"1921","journal-title":"The mneme."},{"key":"B83","doi-asserted-by":"publisher","first-page":"2116.e","DOI":"10.1016\/j.neuron.2021.05.006","article-title":"A locus coeruleus to dentate gyrus noradrenergic circuit modulates aversive contextual processing.","volume":"109","author":"Seo","year":"2021","journal-title":"Neuron"},{"key":"B84","doi-asserted-by":"publisher","first-page":"573","DOI":"10.1111\/j.1460-9568.1997.tb01634.x","article-title":"Interneurons in the hippocampal dentate gyrus: an in vivo intracellular study.","volume":"9","author":"Sik","year":"1997","journal-title":"Eur. J. Neurosci."},{"key":"B85","doi-asserted-by":"publisher","first-page":"880","DOI":"10.1016\/j.biopsych.2015.04.006","article-title":"An Abrupt Transformation of Phobic Behavior After a Post-Retrieval Amnesic Agent.","volume":"78","author":"Soeter","year":"2015","journal-title":"Biol. Psychiatry"},{"key":"B86","doi-asserted-by":"publisher","DOI":"10.1186\/1471-213x-1-4","article-title":"Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus.","volume":"1","author":"Srinivas","year":"2001","journal-title":"BMC Dev. Biol."},{"key":"B87","doi-asserted-by":"publisher","first-page":"687","DOI":"10.1016\/s0306-4522(01)00501-2","article-title":"Excitatory and inhibitory neurons express c-Fos in barrel-related columns after exploration of a novel environment.","volume":"109","author":"Staiger","year":"2002","journal-title":"Neuroscience"},{"key":"B88","doi-asserted-by":"publisher","first-page":"467","DOI":"10.1002\/cne.901630406","article-title":"The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-beta-hydroxylase as a marker.","volume":"163","author":"Swanson","year":"1975","journal-title":"J. Comp. Neurol."},{"key":"B89","doi-asserted-by":"crossref","first-page":"716","DOI":"10.2146\/ajhp070124","article-title":"Prazosin for treatment of nightmares related to posttraumatic stress disorder.","volume":"65","author":"Taylor","year":"2008","journal-title":"Am. J. Health Syst. Pharm."},{"key":"B90","doi-asserted-by":"publisher","first-page":"918","DOI":"10.1016\/j.neuron.2015.08.002","article-title":"Memory Engram Cells Have Come of Age.","volume":"87","author":"Tonegawa","year":"2015","journal-title":"Neuron"},{"key":"B91","doi-asserted-by":"publisher","first-page":"1054","DOI":"10.1016\/j.neuron.2013.07.047","article-title":"Fear extinction causes target-specific remodeling of perisomatic inhibitory synapses.","volume":"80","author":"Trouche","year":"2013","journal-title":"Neuron"},{"key":"B92","doi-asserted-by":"publisher","first-page":"773","DOI":"10.2165\/00003495-198836060-00006","article-title":"Current status of beta-blocking drugs in the treatment of anxiety disorders.","volume":"36","author":"Tyrer","year":"1988","journal-title":"Drugs"},{"key":"B93","doi-asserted-by":"crossref","first-page":"530.e","DOI":"10.1016\/j.neuron.2018.04.001","article-title":"Different Neuronal Activity Patterns Induce Different Gene Expression Programs.","volume":"98","author":"Tyssowski","year":"2018","journal-title":"Neuron"},{"key":"B94","doi-asserted-by":"publisher","first-page":"363.e","DOI":"10.1016\/j.neuron.2017.03.037","article-title":"Chemogenetic Interrogation of a Brain-wide Fear Memory Network in Mice.","volume":"94","author":"Vetere","year":"2017","journal-title":"Neuron"},{"key":"B95","doi-asserted-by":"publisher","DOI":"10.3389\/fnbeh.2013.00211","article-title":"Reactivating fear memory under propranolol resets pre-trauma levels of dendritic spines in basolateral amygdala but not dorsal hippocampus neurons.","volume":"7","author":"Vetere","year":"2013","journal-title":"Front. Behav. Neurosci."}],"container-title":["Frontiers in Behavioral Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnbeh.2022.919831\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,7,7]],"date-time":"2022-07-07T08:40:46Z","timestamp":1657183246000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnbeh.2022.919831\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,7]]},"references-count":95,"alternative-id":["10.3389\/fnbeh.2022.919831"],"URL":"https:\/\/doi.org\/10.3389\/fnbeh.2022.919831","relation":{},"ISSN":["1662-5153"],"issn-type":[{"value":"1662-5153","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,7,7]]},"article-number":"919831"}}