{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T04:16:43Z","timestamp":1790741803078,"version":"4.1.0"},"reference-count":121,"publisher":"Public Library of Science (PLoS)","issue":"1","license":[{"start":{"date-parts":[[2025,1,14]],"date-time":"2025-01-14T00:00:00Z","timestamp":1736812800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000025","name":"National Institute of Mental Health","doi-asserted-by":"publisher","award":["R01-MH080318"],"award-info":[{"award-number":["R01-MH080318"]}],"id":[{"id":"10.13039\/100000025","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000025","name":"National Institute of Mental Health","doi-asserted-by":"publisher","award":["R01-MH112688"],"award-info":[{"award-number":["R01-MH112688"]}],"id":[{"id":"10.13039\/100000025","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000026","name":"National Institute on Drug Abuse","doi-asserted-by":"publisher","award":["T32-DA037183"],"award-info":[{"award-number":["T32-DA037183"]}],"id":[{"id":"10.13039\/100000026","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000026","name":"National Institute on Drug Abuse","doi-asserted-by":"publisher","award":["T32-DA007234"],"award-info":[{"award-number":["T32-DA007234"]}],"id":[{"id":"10.13039\/100000026","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100013078","name":"St. Olaf College","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100013078","id-type":"DOI","asserted-by":"publisher"}]},{"name":"University of Minnesota Medical School"}],"content-domain":{"domain":["www.plosbiology.org"],"crossmark-restriction":false},"short-container-title":["PLoS Biol"],"abstract":"<jats:p>Worrying about perceived threats is a hallmark of multiple psychological disorders including anxiety. This concern about future events is particularly important when an individual is faced with an approach-avoidance conflict. Potential goals to approach are known to be represented in the dorsal hippocampus during theta cycles. Similarly, important information that is distant from the animal\u2019s position is represented during hippocampal high-synchrony events (HSEs), which coincide with sharp-wave ripples (SWRs). It is likely that potential future threats may be similarly represented. We examined how threats and rewards were represented within the hippocampus during approach-avoidance conflicts in rats faced with a predator-like robot guarding a food reward. We found decoding of the pseudo-predator\u2019s location during HSEs when hesitating in the nest and during theta prior to retreating as the rats approached the pseudo-predator. After the first attack, we observed new place fields appearing at the location of the robot (not the location the rat was when attacked). The anxiolytic diazepam reduced anxiety-like behavior and altered hippocampal local field potentials (LFPs), including reducing SWRs, suggesting that one potential mechanism of diazepam\u2019s actions may be through altered representations of imagined threat. These results suggest that hippocampal representation of potential threats could be an important mechanism that underlies worry and a potential target for anxiolytics.<\/jats:p>","DOI":"10.1371\/journal.pbio.3002954","type":"journal-article","created":{"date-parts":[[2025,1,14]],"date-time":"2025-01-14T13:24:32Z","timestamp":1736861072000},"page":"e3002954","update-policy":"https:\/\/doi.org\/10.1371\/journal.pbio.corrections_policy","source":"Crossref","is-referenced-by-count":20,"title":["Dorsal hippocampus represents locations to avoid as well as locations to approach during approach-avoidance conflict"],"prefix":"10.1371","volume":"23","author":[{"given":"Olivia L.","family":"Calvin","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matthew T.","family":"Erickson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cody J.","family":"Walters","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3644-9072","authenticated-orcid":true,"given":"A. David","family":"Redish","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2025,1,14]]},"reference":[{"key":"pbio.3002954.ref001","volume":"343","author":"AT Beck","year":"2005","journal-title":"Anxiety disorders and phobias: A cognitive perspective"},{"key":"pbio.3002954.ref002","volume-title":"Neural Computations Underpinning Anxiety in Health and Disease","author":"CJ Walters","year":"2021"},{"key":"pbio.3002954.ref003","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.cobeha.2018.03.013","article-title":"When planning to survive goes wrong: predicting the future and replaying the past in anxiety and PTSD.","volume":"24","author":"C Gagne","year":"2018","journal-title":"Curr Opin Behav Sci"},{"key":"pbio.3002954.ref004","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1016\/j.beth.2011.07.002","article-title":"Concreteness of positive, negative, and neutral repetitive thinking about the future.","volume":"43","author":"E Behar","year":"2012","journal-title":"Behav Ther."},{"key":"pbio.3002954.ref005","article-title":"Episodic foresight and anxiety: Proximate and ultimate perspectives.","author":"B Miloyan","year":"2015","journal-title":"Br J Clin Psychol."},{"key":"pbio.3002954.ref006","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1038\/nrn2213","article-title":"Remembering the past to imagine the future: the prospective brain","volume":"8","author":"DL Schacter","year":"2007","journal-title":"Nat Rev Neurosci"},{"key":"pbio.3002954.ref007","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.tics.2006.11.004","article-title":"Self-projection and the brain","volume":"11","author":"RL Buckner","year":"2007","journal-title":"Trends Cogn Sci"},{"key":"pbio.3002954.ref008","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1017\/S0140525X07001975","article-title":"The evolution of foresight: What is mental time travel, and is it unique to humans?","volume":"30","author":"T Suddendorf","year":"2007","journal-title":"Behav Brain Sci."},{"key":"pbio.3002954.ref009","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1038\/nrn.2015.30","article-title":"Vicarious trial and error.","volume":"17","author":"AD Redish","year":"2016","journal-title":"Nat Rev Neurosci"},{"key":"pbio.3002954.ref010","doi-asserted-by":"crossref","first-page":"1351","DOI":"10.1126\/science.1144161","article-title":"Prospection: Experiencing the future","volume":"317","author":"DT Gilbert","year":"2007","journal-title":"Science"},{"key":"pbio.3002954.ref011","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/j.neubiorev.2021.02.021","article-title":"Motivational competition and the paraventricular thalamus.","author":"GP McNally","year":"2021","journal-title":"Neurosci Biobehav Rev."},{"key":"pbio.3002954.ref012","doi-asserted-by":"crossref","first-page":"1652","DOI":"10.1038\/s41386-022-01332-2","article-title":"A meta-analysis of conditioned fear generalization in anxiety-related disorders","volume":"47","author":"SE Cooper","year":"2022","journal-title":"Neuropsychopharmacology"},{"key":"pbio.3002954.ref013","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/j.cobeha.2015.06.005","article-title":"Neuroethological studies of fear, anxiety, and risky decision-making in rodents and humans.","volume":"5","author":"D Mobbs","year":"2015","journal-title":"Curr Opin Behav Sci"},{"key":"pbio.3002954.ref014","first-page":"185","volume-title":"Evolution and learning","author":"MS Fanselow","year":"1988"},{"key":"pbio.3002954.ref015","first-page":"1","article-title":"Episodic future thinking in generalized anxiety disorder.","author":"JQ Wu","year":"2015","journal-title":"J Anxiety Disord."},{"key":"pbio.3002954.ref016","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1037\/0021-843X.105.2.286","article-title":"Anxiety, depression, and the anticipation of future positive and negative experiences.","volume":"105","author":"AK MacLeod","year":"1996","journal-title":"J Abnorm Psychol"},{"key":"pbio.3002954.ref017","article-title":"Placing prediction into the fear circuit","author":"GP McNally","year":"2011","journal-title":"Trends Neurosci"},{"key":"pbio.3002954.ref018","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1101\/lm.039180.115","article-title":"Neurobehavioral perspectives on the distinction between fear and anxiety.","author":"JN Perusini","year":"2015","journal-title":"Learn Mem."},{"key":"pbio.3002954.ref019","doi-asserted-by":"crossref","first-page":"1394","DOI":"10.1038\/nn.4101","article-title":"Resolving the neural circuits of anxiety","volume":"18","author":"GG Calhoon","year":"2015","journal-title":"Nat Neurosci"},{"key":"pbio.3002954.ref020","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1038\/nrn3945","article-title":"Neuronal circuits for fear and anxiety.","volume":"16","author":"P Tovote","year":"2015","journal-title":"Nat Rev Neurosci"},{"key":"pbio.3002954.ref021","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1016\/S0079-6123(08)61880-4","article-title":"Emotional networks and motor control: a fearful view","volume":"107","author":"J. LeDoux","year":"1996","journal-title":"Prog Brain Res"},{"key":"pbio.3002954.ref022","volume-title":"Anxious: Using the Brain to Understand and Treat Fear and Anxiety","author":"JE LeDoux","year":"2015"},{"key":"pbio.3002954.ref023","volume-title":"The Neuropsychology of Anxiety","author":"J Gray","year":"2000"},{"key":"pbio.3002954.ref024","doi-asserted-by":"crossref","first-page":"12176","DOI":"10.1523\/JNEUROSCI.3761-07.2007","article-title":"Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point","volume":"27","author":"A Johnson","year":"2007","journal-title":"J Neurosci"},{"key":"pbio.3002954.ref025","doi-asserted-by":"crossref","first-page":"552","DOI":"10.1016\/j.cell.2020.01.014","article-title":"Constant Sub-second Cycling between Representations of Possible Futures in the Hippocampus","volume":"180","author":"K Kay","year":"2020","journal-title":"Cell"},{"key":"pbio.3002954.ref026","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1038\/nn.3909","article-title":"Hippocampal theta sequences reflect current goals","volume":"18","author":"AM Wikenheiser","year":"2015","journal-title":"Nat Neurosci"},{"key":"pbio.3002954.ref027","doi-asserted-by":"crossref","first-page":"1981","DOI":"10.1152\/jn.00793.2018","article-title":"Disrupting the medial prefrontal cortex alters hippocampal sequences during deliberative decision making","volume":"121","author":"B Schmidt","year":"2019","journal-title":"J Neurophysiol"},{"key":"pbio.3002954.ref028","doi-asserted-by":"crossref","first-page":"1032","DOI":"10.1038\/nn.3138","article-title":"Segmentation of spatial experience by hippocampal theta sequences","volume":"15","author":"AS Gupta","year":"2012","journal-title":"Nat Neurosci"},{"key":"pbio.3002954.ref029","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1038\/nature12112","article-title":"Hippocampal place-cell sequences depict future paths to remembered goals","volume":"497","author":"BE Pfeiffer","year":"2013","journal-title":"Nature"},{"key":"pbio.3002954.ref030","article-title":"Dynamics of Awake Hippocampal-Prefrontal Replay for Spatial Learning and Memory-Guided Decision Making","author":"JD Shin","year":"2019","journal-title":"Neuron"},{"key":"pbio.3002954.ref031","doi-asserted-by":"crossref","first-page":"R37","DOI":"10.1016\/j.cub.2017.10.073","article-title":"The Role of Hippocampal Replay in Memory and Planning","volume":"28","author":"HF \u00d3lafsd\u00f3ttir","year":"2018","journal-title":"Curr Biol"},{"key":"pbio.3002954.ref032","doi-asserted-by":"crossref","first-page":"3149","DOI":"10.1016\/j.neuron.2021.07.029","article-title":"Hippocampal replay reflects specific past experiences rather than a plan for subsequent choice","volume":"109","author":"AK Gillespie","year":"2021","journal-title":"Neuron"},{"key":"pbio.3002954.ref033","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1016\/j.neuron.2010.01.034","article-title":"Hippocampal replay is not a simple function of experience","volume":"65","author":"AS Gupta","year":"2010","journal-title":"Neuron"},{"key":"pbio.3002954.ref034","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1016\/j.neuron.2009.07.027","article-title":"Hippocampal Replay of Extended Experience.","volume":"63","author":"TJ Davidson","year":"2009","journal-title":"Neuron"},{"key":"pbio.3002954.ref035","doi-asserted-by":"crossref","first-page":"1241","DOI":"10.1038\/nn1961","article-title":"Forward and reverse hippocampal place-cell sequences during ripples","volume":"10","author":"K Diba","year":"2007","journal-title":"Nat Neurosci"},{"key":"pbio.3002954.ref036","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1038\/nn.4507","article-title":"Hippocampal awake replay in fear memory retrieval","volume":"20","author":"C-T Wu","year":"2017","journal-title":"Nat Neurosci"},{"key":"pbio.3002954.ref037","doi-asserted-by":"crossref","first-page":"21773","DOI":"10.1073\/pnas.1010079108","article-title":"Amygdala regulates risk of predation in rats foraging in a dynamic fear environment","volume":"107","author":"J-S Choi","year":"2010","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pbio.3002954.ref038","doi-asserted-by":"crossref","first-page":"12994","DOI":"10.1523\/JNEUROSCI.0407-15.2015","article-title":"Amygdala Signaling during Foraging in a Hazardous Environment","volume":"35","author":"A Amir","year":"2015","journal-title":"J Neurosci"},{"key":"pbio.3002954.ref039","doi-asserted-by":"crossref","first-page":"2513","DOI":"10.1007\/s00213-019-05197-0","article-title":"Avoid-approach conflict behaviors differentially affected by anxiolytics: implications for a computational model of risky decision-making","volume":"236","author":"CJ Walters","year":"2019","journal-title":"Psychopharmacology (Berl)."},{"key":"pbio.3002954.ref040","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1007\/s002130050367","article-title":"Behavioural and pharmacological characterisation of the canopy stretched attend posture test as a model of anxiety in mice and rats","volume":"133","author":"SS Grewal","year":"1997","journal-title":"Psychopharmacology"},{"key":"pbio.3002954.ref041","doi-asserted-by":"crossref","first-page":"31286","DOI":"10.1038\/srep31286","article-title":"MATSAP: An automated analysis of stretch-attend posture in rodent behavioral experiments.","volume":"6","author":"KS Holly","year":"2016","journal-title":"Sci Rep"},{"key":"pbio.3002954.ref042","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1017\/CBO9780511777578.018","volume-title":"Anxiety Disorders: Theory, Research, and Clinical Perspectives.","author":"JA Gordon","year":"2010"},{"key":"pbio.3002954.ref043","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1007\/BF02245594","article-title":"The ambivalent behaviour \u201cstretched approach posture\u201d in the rat as a paradigm to characterize anxiolytic drugs.","volume":"121","author":"HE Molewijk","year":"1995","journal-title":"Psychopharmacology"},{"key":"pbio.3002954.ref044","article-title":"Bed Nucleus of the Stria Terminalis GABA neurons are necessary for changes in foraging behavior following an innate threat","author":"A Ly","year":"2023"},{"key":"pbio.3002954.ref045","article-title":"Periaqueductal gray activates antipredatory neural responses in the amygdala of foraging rats.","author":"EJ Kim","year":"2023","journal-title":"Elife"},{"key":"pbio.3002954.ref046","doi-asserted-by":"crossref","first-page":"1362","DOI":"10.1016\/j.cub.2015.03.048","article-title":"Alterations of Hippocampal Place Cells in Foraging Rats Facing a \u201cPredatory\u201d Threat.","volume":"25","author":"EJ Kim","year":"2015","journal-title":"Curr Biol"},{"key":"pbio.3002954.ref047","volume-title":"The Hippocampus as a Cognitive Map","author":"J O\u2019Keefe","year":"1978"},{"key":"pbio.3002954.ref048","doi-asserted-by":"crossref","DOI":"10.7551\/mitpress\/1571.001.0001","volume-title":"Beyond the Cognitive Map: From Place Cells to Episodic Memory","author":"AD Redish","year":"1999"},{"key":"pbio.3002954.ref049","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/0165-0173(83)90037-1","article-title":"Cellular bases of hippocampal EEG in the behaving rat","volume":"287","author":"G Buzs\u00e1ki","year":"1983","journal-title":"Brain Res"},{"key":"pbio.3002954.ref050","doi-asserted-by":"crossref","first-page":"1073","DOI":"10.1002\/hipo.22488","article-title":"Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning","volume":"25","author":"G. Buzs\u00e1ki","year":"2015","journal-title":"Hippocampus"},{"key":"pbio.3002954.ref051","doi-asserted-by":"crossref","DOI":"10.1093\/acprof:oso\/9780195301069.001.0001","volume-title":"Rhythms of the Brain","author":"G. Buzsaki","year":"2006"},{"key":"pbio.3002954.ref052","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1037\/h0030672","article-title":"Limbic-Diencephalic mechanisms of voluntary movement.","volume":"78","author":"CH Vanderwolf","year":"1971","journal-title":"Psychol Rev"},{"key":"pbio.3002954.ref053","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.neuron.2015.12.005","article-title":"Spatial sequence coding differs during slow and fast gamma rhythms in the hippocampus","volume":"89","author":"C Zheng","year":"2016","journal-title":"Neuron"},{"key":"pbio.3002954.ref054","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1126\/science.abb4151","article-title":"Alternating sequences of future and past behavior encoded within hippocampal theta oscillations","volume":"370","author":"M Wang","year":"2020","journal-title":"Science"},{"key":"pbio.3002954.ref055","doi-asserted-by":"crossref","first-page":"2602","DOI":"10.1152\/jn.2000.83.5.2602","article-title":"Position reconstruction from an ensemble of hippocampal place cells: contribution of theta phase encoding","volume":"83","author":"O Jensen","year":"2000","journal-title":"J Neurophysiol"},{"key":"pbio.3002954.ref056","article-title":"Control of recollection by slow gamma dominating mid-frequency gamma in hippocampus CA1","author":"D Dvorak","year":"2018","journal-title":"PLoS Biol"},{"key":"pbio.3002954.ref057","doi-asserted-by":"crossref","first-page":"1193","DOI":"10.1098\/rstb.2008.0316","article-title":"Prediction, sequences and the hippocampus","volume":"364","author":"J Lisman","year":"2009","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"key":"pbio.3002954.ref058","doi-asserted-by":"crossref","first-page":"975","DOI":"10.1016\/j.neuron.2016.10.028","article-title":"Interplay between Hippocampal Sharp-Wave-Ripple Events and Vicarious Trial and Error Behaviors in Decision Making","volume":"92","author":"AE Papale","year":"2016","journal-title":"Neuron"},{"key":"pbio.3002954.ref059","doi-asserted-by":"crossref","first-page":"913","DOI":"10.1038\/nn.2344","article-title":"Awake replay of remote experiences in the hippocampus","volume":"12","author":"MP Karlsson","year":"2009","journal-title":"Nat Neurosci"},{"key":"pbio.3002954.ref060","doi-asserted-by":"crossref","first-page":"12415","DOI":"10.1523\/JNEUROSCI.4118-06.2006","article-title":"Hippocampal sharp waves and reactivation during awake states depend on repeated sequential experience","volume":"26","author":"JC Jackson","year":"2006","journal-title":"J Neurosci"},{"key":"pbio.3002954.ref061","doi-asserted-by":"crossref","first-page":"1609","DOI":"10.1038\/s41593-018-0232-z","article-title":"Prioritized memory access explains planning and hippocampal replay","volume":"21","author":"MG Mattar","year":"2018","journal-title":"Nat Neurosci"},{"key":"pbio.3002954.ref062","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1101\/lm.85205","article-title":"A simple neural network model of the hippocampus suggesting its pathfinding role in episodic memory retrieval.","volume":"12","author":"AV Samsonovich","year":"2005","journal-title":"Learn Mem"},{"key":"pbio.3002954.ref063","doi-asserted-by":"crossref","first-page":"1163","DOI":"10.1016\/j.neunet.2005.08.009","article-title":"Hippocampal replay contributes to within session learning in a temporal difference reinforcement learning model","volume":"18","author":"A Johnson","year":"2005","journal-title":"Neural Netw"},{"key":"pbio.3002954.ref064","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/hipo.20707","article-title":"Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat.","volume":"20","author":"V Ego-Stengel","year":"2010","journal-title":"Hippocampus"},{"key":"pbio.3002954.ref065","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1038\/nn.3970","article-title":"Explicit memory creation during sleep demonstrates a causal role of place cells in navigation","volume":"18","author":"G de Lavill\u00e9on","year":"2015","journal-title":"Nat Neurosci"},{"key":"pbio.3002954.ref066","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/j.neuron.2007.11.035","article-title":"New experiences enhance coordinated neural activity in the hippocampus","volume":"57","author":"S Cheng","year":"2008","journal-title":"Neuron"},{"key":"pbio.3002954.ref067","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/j.neuron.2005.10.037","article-title":"Place-Selective Firing of CA1 Pyramidal Cells during Sharp Wave\/Ripple Network Patterns in Exploratory Behavior","volume":"49","author":"J O\u2019Neill","year":"2006","journal-title":"Neuron"},{"key":"pbio.3002954.ref068","doi-asserted-by":"crossref","first-page":"582","DOI":"10.1016\/j.neuron.2010.02.022","article-title":"A dual role for hippocampal replay","volume":"65","author":"D Derdikman","year":"2010","journal-title":"Neuron"},{"key":"pbio.3002954.ref069","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1001\/jamapsychiatry.2019.4788","article-title":"Is Hippocampal Replay a Mechanism for Anxiety and Depression?","volume":"77","author":"AS Heller","year":"2020","journal-title":"JAMA Psychiatry"},{"key":"pbio.3002954.ref070","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.cobeha.2018.02.007","article-title":"Fear paradigms: The times they are a-changin\u2019.","volume":"24","author":"JJ Kim","year":"2018","journal-title":"Curr Opin Behav Sci"},{"key":"pbio.3002954.ref071","author":"NJ Cohen","year":"1993"},{"key":"pbio.3002954.ref072","doi-asserted-by":"crossref","first-page":"7015","DOI":"10.1523\/JNEUROSCI.5492-03.2004","article-title":"Putting fear in its place: Remapping of hippocampal place cells during fear conditioning","volume":"24","author":"MA Moita","year":"2004","journal-title":"J Neurosci"},{"key":"pbio.3002954.ref073","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1016\/S0896-6273(03)00033-3","article-title":"Hippocampal place cells acquire location-specific responses to the conditioned stimulus during auditory fear conditioning","volume":"37","author":"MA Moita","year":"2003","journal-title":"Neuron"},{"key":"pbio.3002954.ref074","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1038\/nn.3687","article-title":"Attentive scanning behavior drives one-trial potentiation of hippocampal place fields","volume":"17","author":"JD Monaco","year":"2014","journal-title":"Nat Neurosci"},{"key":"pbio.3002954.ref075","article-title":"Identifying structure in the noise --- covert variables and cognition","author":"A Johnson","year":"2008","journal-title":"Abstr Soc Neurosci"},{"key":"pbio.3002954.ref076","first-page":"40","article-title":"Replay Comes of Age","author":"DJ Foster","year":"2017","journal-title":"Annu Rev Neurosci"},{"key":"pbio.3002954.ref077","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1016\/j.tins.2007.05.002","article-title":"Network and intrinsic cellular mechanisms underlying theta phase precession of hippocampal neurons","volume":"30","author":"AP Maurer","year":"2007","journal-title":"Trends Neurosci"},{"key":"pbio.3002954.ref078","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/B978-0-12-812098-9.00006-1","volume-title":"Goal-Directed Decision Making.","author":"B Schmidt","year":"2018"},{"key":"pbio.3002954.ref079","doi-asserted-by":"crossref","DOI":"10.1002\/hipo.20345","article-title":"Hippocampal Theta Sequences.","volume":"17","author":"DJ Foster","year":"2007","journal-title":"Hippocampus"},{"key":"pbio.3002954.ref080","doi-asserted-by":"crossref","first-page":"1002","DOI":"10.1016\/j.neuron.2013.03.007","article-title":"The Theta-Gamma Neural Code.","volume":"77","author":"JE Lisman","year":"2013","journal-title":"Neuron"},{"key":"pbio.3002954.ref081","doi-asserted-by":"crossref","first-page":"1655","DOI":"10.1038\/s41593-020-00744-x","article-title":"Parameterizing neural power spectra into periodic and aperiodic components","volume":"23","author":"T Donoghue","year":"2020","journal-title":"Nat Neurosci"},{"key":"pbio.3002954.ref082","doi-asserted-by":"crossref","first-page":"3894","DOI":"10.1016\/j.celrep.2018.12.057","article-title":"Hippocampal Theta-Gamma Coupling Reflects State-Dependent Information Processing in Decision Making","volume":"25","author":"S Amemiya","year":"2018","journal-title":"Cell Rep"},{"key":"pbio.3002954.ref083","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1007\/BF00180822","article-title":"The pharmacokinetics of diazepam and desmethyldiazepam in rat brain and plasma","volume":"88","author":"H Friedman","year":"1986","journal-title":"Psychopharmacology (Berl)."},{"key":"pbio.3002954.ref084","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.jneumeth.2004.03.014","article-title":"Measuring fundamental frequencies in local field potentials","volume":"138","author":"B Masimore","year":"2004","journal-title":"J Neurosci Methods"},{"key":"pbio.3002954.ref085","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1038\/nature08573","article-title":"Frequency of gamma oscillations routes flow of information in the hippocampus","volume":"462","author":"LL Colgin","year":"2009","journal-title":"Nature"},{"key":"pbio.3002954.ref086","doi-asserted-by":"crossref","first-page":"1213","DOI":"10.1016\/j.neuron.2017.02.017","article-title":"Entorhinal-CA3 Dual-Input Control of Spike Timing in the Hippocampus by Theta-Gamma Coupling","volume":"93","author":"A Fern\u00e1ndez-Ruiz","year":"2017","journal-title":"Neuron"},{"key":"pbio.3002954.ref087","doi-asserted-by":"crossref","first-page":"6769","DOI":"10.1523\/JNEUROSCI.17-17-06769.1997","article-title":"The effect of aging on experience-dependent plasticity of hippocampal place cells","volume":"17","author":"J Shen","year":"1997","journal-title":"J Neurosci"},{"key":"pbio.3002954.ref088","doi-asserted-by":"crossref","first-page":"6","DOI":"10.3389\/fncir.2012.00006","article-title":"Experience-dependent firing rate remapping generates directional selectivity in hippocampal place cells.","volume":"6","author":"Z Navratilova","year":"2012","journal-title":"Front Neural Circuits"},{"key":"pbio.3002954.ref089","doi-asserted-by":"crossref","first-page":"4541","DOI":"10.1523\/JNEUROSCI.4896-03.2004","article-title":"Local sensory cues and place cell directionality: additional evidence of prospective coding in the hippocampus","volume":"24","author":"FP Battaglia","year":"2004","journal-title":"J Neurosci"},{"key":"pbio.3002954.ref090","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.73046","article-title":"Bidirectional synaptic plasticity rapidly modifies hippocampal representations.","volume":"10","author":"AD Milstein","year":"2021","journal-title":"Elife"},{"key":"pbio.3002954.ref091","doi-asserted-by":"crossref","first-page":"1033","DOI":"10.1126\/science.aan3846","article-title":"Behavioral time scale synaptic plasticity underlies CA1 place fields","volume":"357","author":"KC Bittner","year":"2017","journal-title":"Science"},{"key":"pbio.3002954.ref092","doi-asserted-by":"crossref","first-page":"15022","DOI":"10.1523\/JNEUROSCI.1129-14.2014","article-title":"Back to the future: preserved hippocampal network activity during reverse ambulation","volume":"34","author":"AP Maurer","year":"2014","journal-title":"J Neurosci"},{"key":"pbio.3002954.ref093","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1038\/nn.3698","article-title":"Reversed theta sequences of hippocampal cell assemblies during backward travel","volume":"17","author":"A Cei","year":"2014","journal-title":"Nat Neurosci"},{"key":"pbio.3002954.ref094","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.11352","article-title":"Sexually divergent expression of active and passive conditioned fear responses in rats.","volume":"4","author":"TM Gruene","year":"2015","journal-title":"Elife"},{"key":"pbio.3002954.ref095","first-page":"237","article-title":"Individual differences in bodily freezing predict emotional biases in decision making.","volume":"8","author":"V Ly","year":"2014","journal-title":"Front Behav Neurosci"},{"key":"pbio.3002954.ref096","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1038\/sj.mp.4001939","article-title":"Mechanisms of fear extinction","volume":"12","author":"K Myers","year":"2007","journal-title":"Mol Psychiatry"},{"key":"pbio.3002954.ref097","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1016\/j.tics.2019.12.016","article-title":"Space, Time, and Fear: Survival Computations along Defensive Circuits.","volume":"24","author":"D Mobbs","year":"2020","journal-title":"Trends Cogn Sci"},{"key":"pbio.3002954.ref098","doi-asserted-by":"crossref","first-page":"12030","DOI":"10.1038\/s41598-021-90968-z","article-title":"Defensive freezing and its relation to approach-avoidance decision-making under threat.","volume":"11","author":"FH Klaassen","year":"2021","journal-title":"Sci Rep"},{"key":"pbio.3002954.ref099","doi-asserted-by":"crossref","DOI":"10.1098\/rstb.2016.0206","article-title":"Freeze for action: neurobiological mechanisms in animal and human freezing","volume":"372","author":"K. Roelofs","year":"2017","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"key":"pbio.3002954.ref100","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1097\/HRP.0000000000000065","article-title":"Fear and the Defense Cascade: Clinical Implications and Management.","volume":"23","author":"K Kozlowska","year":"2015","journal-title":"Harv Rev Psychiatry."},{"key":"pbio.3002954.ref101","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1016\/0006-8993(87)91602-7","article-title":"The effect of diazepam on hippocampal EEG in relation to behavior","volume":"435","author":"M Caudarella","year":"1987","journal-title":"Brain Res"},{"key":"pbio.3002954.ref102","doi-asserted-by":"crossref","first-page":"8650","DOI":"10.1523\/JNEUROSCI.5040-12.2013","article-title":"Novelty and anxiolytic drugs dissociate two components of hippocampal theta in behaving rats","volume":"33","author":"CE Wells","year":"2013","journal-title":"J Neurosci"},{"key":"pbio.3002954.ref103","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.neuroscience.2017.08.056","article-title":"Systemic administration of two different anxiolytic drugs decreases local field potential theta frequency in the medial entorhinal cortex without affecting grid cell firing fields","volume":"364","author":"CK Monaghan","year":"2017","journal-title":"Neuroscience"},{"key":"pbio.3002954.ref104","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/S0166-4328(02)00327-3","article-title":"High frequency (200 Hz) oscillations and firing patterns in the basolateral amygdala and dorsal endopiriform nucleus of the behaving rat.","volume":"141","author":"AA Ponomarenko","year":"2003","journal-title":"Behav Brain Res"},{"key":"pbio.3002954.ref105","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1016\/j.neuroscience.2010.11.027","article-title":"Different effects of zolpidem and diazepam on hippocampal sharp wave\u2014ripple activity in vitro","volume":"175","author":"E Koniaris","year":"2011","journal-title":"Neuroscience"},{"key":"pbio.3002954.ref106","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1002\/hipo.22104","article-title":"Effects of the GABA-uptake blocker NNC-711 on spontaneous sharp wave-ripple complexes in mouse hippocampal slices.","volume":"23","author":"T Viereckel","year":"2013","journal-title":"Hippocampus"},{"key":"pbio.3002954.ref107","doi-asserted-by":"crossref","first-page":"604","DOI":"10.1038\/37601","article-title":"Fear conditioning induces associative long-term potentiation in the amygdala","author":"MT Rogan","year":"1997","journal-title":"Nature"},{"key":"pbio.3002954.ref108","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1016\/j.bbr.2016.07.039","article-title":"The role of the hippocampus in approach-avoidance conflict decision-making: Evidence from rodent and human studies","volume":"313","author":"R Ito","year":"2016","journal-title":"Behav Brain Res"},{"key":"pbio.3002954.ref109","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1016\/j.neuron.2016.01.011","article-title":"Direct Ventral Hippocampal-Prefrontal Input Is Required for Anxiety-Related Neural Activity and Behavior","volume":"89","author":"N Padilla-Coreano","year":"2016","journal-title":"Neuron"},{"key":"pbio.3002954.ref110","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1037\/0735-7044.118.1.97","article-title":"Hippocampus and Pavlovian fear conditioning in rats: muscimol infusions into the ventral, but not dorsal hippocampus impair the acquisition of conditional freezing to an auditory conditional stimulus.","volume":"118","author":"S Maren","year":"2004","journal-title":"Behav Neurosci."},{"key":"pbio.3002954.ref111","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.1037\/0735-7044.107.6.1093","article-title":"Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear.","volume":"107","author":"JJ Kim","year":"1993","journal-title":"Behav Neurosci."},{"key":"pbio.3002954.ref112","doi-asserted-by":"crossref","first-page":"1777","DOI":"10.1523\/JNEUROSCI.4681-09.2010","article-title":"Distinct Representations and Theta Dynamics in Dorsal and Ventral Hippocampus","volume":"30","author":"S Royer","year":"2010","journal-title":"J Neurosci"},{"key":"pbio.3002954.ref113","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1016\/j.neuron.2019.11.022","article-title":"Dorsal and Ventral Hippocampal Sharp-Wave Ripples Activate Distinct Nucleus Accumbens Networks","volume":"105","author":"M Sosa","year":"2020","journal-title":"Neuron"},{"key":"pbio.3002954.ref114","doi-asserted-by":"crossref","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":"DM Bannerman","year":"1999","journal-title":"Behav Neurosci"},{"key":"pbio.3002954.ref115","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/j.neubiorev.2004.03.004","article-title":"Regional dissociations within the hippocampus --- memory and anxiety.","volume":"28","author":"DM Bannerman","year":"2004","journal-title":"Neurosci Biobehav Rev"},{"key":"pbio.3002954.ref116","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1016\/j.pbb.2004.04.017","article-title":"Anxiolytic effects of diazepam and ethanol in two behavioral models: comparison of males and females","volume":"78","author":"MA Wilson","year":"2004","journal-title":"Pharmacol Biochem Behav"},{"key":"pbio.3002954.ref117","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.neuron.2021.10.030","article-title":"Beyond t test and ANOVA: applications of mixed-effects models for more rigorous statistical analysis in neuroscience research","volume":"110","author":"Z Yu","year":"2022","journal-title":"Neuron"},{"key":"pbio.3002954.ref118","first-page":"061481","volume-title":"Kilosort: realtime spike-sorting for extracellular electrophysiology with hundreds of channels","author":"M Pachitariu","year":"2016"},{"key":"pbio.3002954.ref119","article-title":"phy: interactive visualization and manual spike sorting of large-scale ephys data","author":"A Buccino","journal-title":"Github"},{"key":"pbio.3002954.ref120","doi-asserted-by":"crossref","first-page":"849","DOI":"10.1152\/jn.00273.2019","article-title":"Cycle-by-cycle analysis of neural oscillations","volume":"122","author":"S Cole","year":"2019","journal-title":"J Neurophysiol"},{"key":"pbio.3002954.ref121","doi-asserted-by":"crossref","first-page":"1017","DOI":"10.1152\/jn.1998.79.2.1017","article-title":"Interpreting Neuronal Population Activity by Reconstruction: Unified Framework With Application to Hippocampal Place Cells","volume":"79","author":"K Zhang","year":"1998","journal-title":"J Neurophysiol"}],"container-title":["PLOS Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pbio.3002954","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,1,14]],"date-time":"2025-01-14T13:25:10Z","timestamp":1736861110000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pbio.3002954"}},"subtitle":[],"editor":[{"given":"Thomas","family":"Klausberger","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2025,1,14]]},"references-count":121,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,1,14]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pbio.3002954","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2024.03.10.584295","asserted-by":"object"}]},"ISSN":["1545-7885"],"issn-type":[{"value":"1545-7885","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,1,14]]}}}