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E. Moser, E. Kropff, M. Moser (2008)
Place cells, grid cells, and the brain's spatial representation system.Annual review of neuroscience, 31
W. Skaggs, B. McNaughton, M. Wilson, C. Barnes (1996)
Theta phase precession in hippocampal neuronal populations and the compression of temporal sequencesHippocampus, 6
Z. Nadasdy, H. Hirase, András Czurkó, J. Csicsvari, G. Buzsáki (1999)
Replay and Time Compression of Recurring Spike Sequences in the HippocampusThe Journal of Neuroscience, 19
Alessio Attardo, James Fitzgerald, M. Schnitzer (2015)
Impermanence of dendritic spines in live adult CA1 hippocampusNature, 523
T. Bliss, T. Lømo (1973)
Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant pathThe Journal of Physiology, 232
Alon Rubin, Nitzan Geva, L. Sheintuch, Yaniv Ziv (2015)
Hippocampal ensemble dynamics timestamp events in long-term memoryeLife, 4
Matthijs Meer, A. Redish (2011)
Theta Phase Precession in Rat Ventral Striatum Links Place and Reward InformationThe Journal of Neuroscience, 31
Margaret Carr, Shantanu Jadhav, L. Frank (2011)
Hippocampal replay in the awake state: a potential physiological substrate of memory consolidation and retrieval
Agnès Villers, E. Godaux, L. Ris (2012)
Long-Lasting LTP Requires Neither Repeated Trains for Its Induction Nor Protein Synthesis for Its DevelopmentPLoS ONE, 7
T. Nakashiba, D. Buhl, T. McHugh, S. Tonegawa (2009)
Hippocampal CA3 Output Is Crucial for Ripple-Associated Reactivation and Consolidation of MemoryNeuron, 62
S. Gunawardena, W. Rivera, Epstein, C Heathcock, B. Finkelstein, T. Aoki, C. Poulter, D. Jarstfer, C. Zhang, J. Poulter, Am, Chem, B Blagg, M. Jarstfer, D. Rogers, B Bierl-Leonhardt, D. Moreno, M. Schwarz, J. Fargerlund, J. Plimmer, L Tarshis, M. Yan, J. Sacchettini, A Hemmerlin, S. Rivera, H. Erickson, H Erickson, L Altman, R. Kowerski, D. Laungani, J. Am, D. Tse, R. Langston, M. Kakeyama, I. Bethus, P. Spooner, E. Wood, M. Witter, R. Morris
References and Notes Supporting Online Material Materials and Methods Figs. S1 to S5 Tables S1 to S3 Electron Impact (ei) Mass Spectra Chemical Ionization (ci) Mass Spectra References Schemas and Memory Consolidation Research Articles Research Articles Research Articles Research Articles
Zev Rosen, Stephanie Cheung, S. Siegelbaum (2015)
Midbrain dopamine neurons bidirectionally regulate CA3-CA1 synaptic driveNature Neuroscience, 18
Aleena Garner, David Rowland, Sang Hwang, K. Baumgaertel, Bryan Roth, C. Kentros, M. Mayford (2012)
Generation of a Synthetic Memory TraceScience, 335
Mark Brandon, A. Bogaard, Chris Andrews, Michael Hasselmo (2012)
Head direction cells in the postsubiculum do not show replay of prior waking sequences during sleepHippocampus, 22
G. Buzsáki (2015)
Hippocampal sharp wave‐ripple: A cognitive biomarker for episodic memory and planningHippocampus, 25
B. McNaughton, C. Barnes, J. O’Keefe (1983)
The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving ratsExperimental Brain Research, 52
T. Dugladze, D. Schmitz, M. Whittington, I. Vida, T. Gloveli (2012)
Awake Hippocampal Sharp-Wave Ripples Support Spatial MemoryScience, 336
(2012)
Disrupting neural activity related to awake-state sharp wave-ripple complexes prevents hippocampal learning
John Trimper, Sean Trettel, Ernie Hwaun, L. Colgin (2017)
Methodological Caveats in the Detection of Coordinated Replay between Place Cells and Grid CellsFrontiers in Systems Neuroscience, 11
J. Sjöström, W. Gerstner (2010)
Spike-timing dependent plasticityScholarpedia, 5
G. Buzsáki, J. Czopf, I. Kondákor, A. Björklund, F. Gage (1987)
Cellular activity of intracerebrally transplanted fetal hippocampus during behaviorNeuroscience, 22
Katie Bittner, Aaron Milstein, Christine Grienberger, S. Romani, J. Magee (2017)
Behavioral time scale synaptic plasticity underlies CA1 place fieldsScience, 357
D. Bendor, M. Wilson (2012)
Biasing the content of hippocampal replay during sleepNature Neuroscience, 15
A. Grosmark, G. Buzsáki (2016)
Diversity in neural firing dynamics supports both rigid and learned hippocampal sequencesScience, 351
Fabian Roth, Katinka Beyer, M. Both, A. Draguhn, A. Egorov (2016)
Downstream effects of hippocampal sharp wave ripple oscillations on medial entorhinal cortex layer V neurons in vitroHippocampus, 26
J. O’Keefe, J. Dostrovsky (1971)
The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat.Brain research, 34 1
Joseph O’Neill, Timothy Senior, K. Allen, J. Huxter, J. Csicsvari (2008)
Reactivation of experience-dependent cell assembly patterns in the hippocampusNature Neuroscience, 11
Y. Dan, M. Poo (2004)
Spike Timing-Dependent Plasticity of Neural CircuitsNeuron, 44
L. Colgin (2013)
Mechanisms and functions of theta rhythms.Annual review of neuroscience, 36
J. Csicsvari, Joseph O’Neill, K. Allen, Timothy Senior (2007)
Place-selective firing contributes to the reverse-order reactivation of CA1 pyramidal cells during sharp waves in open-field explorationThe European Journal of Neuroscience, 26
David Foster (2017)
Replay Comes of Age.Annual review of neuroscience, 40
R. Ambrose, Brad Pfeiffer, David Foster, Solomon Snyder (2016)
Reverse Replay of Hippocampal Place Cells Is Uniquely Modulated by Changing RewardNeuron, 91
G. Dragoi, S. Tonegawa (2013)
Development of schemas revealed by prior experience and NMDA receptor knock-outeLife, 2
R. Redondo, H. Okuno, P. Spooner, B. Frenguelli, H. Bito, R. Morris (2010)
Synaptic Tagging and Capture: Differential Role of Distinct Calcium/Calmodulin Kinases in Protein Synthesis-Dependent Long-Term PotentiationThe Journal of Neuroscience, 30
J. Knott (1951)
The organization of behavior: A neuropsychological theoryElectroencephalography and Clinical Neurophysiology, 3
Susumu Takahashi (2015)
Episodic-like memory trace in awake replay of hippocampal place cell activity sequenceseLife, 4
V. Douchamps, Ali Jeewajee, Pam Blundell, N. Burgess, C. Lever (2013)
Evidence for Encoding versus Retrieval Scheduling in the Hippocampus by Theta Phase and AcetylcholineThe Journal of Neuroscience, 33
R. Mishra, Sooyun Kim, S. Guzman, P. Jonas (2016)
Symmetric spike timing-dependent plasticity at CA3–CA3 synapses optimizes storage and recall in autoassociative networksNature Communications, 7
Adam Johnson, A. Redish (2007)
Neural Ensembles in CA3 Transiently Encode Paths Forward of the Animal at a Decision PointThe Journal of Neuroscience, 27
David Foster, M. Wilson (2006)
Reverse replay of behavioural sequences in hippocampal place cells during the awake stateNature, 440
Brad Pfeiffer, David Foster (2015)
Autoassociative dynamics in the generation of sequences of hippocampal place cellsScience, 349
Delia Silva, Ting Feng, David Foster (2015)
Trajectory events across hippocampal place-cells require previous experienceNature neuroscience, 18
G. Buzsáki, Leung S., C. Vanderwolf (1983)
Cellular bases of hippocampal EEG in the behaving ratBrain Research Reviews, 6
Jiemin Shen, H. Kudrimoti, B. McNaughton, C. Barnes (1998)
Reactivation of neuronal ensembles in hippocampal dentate gyrus during sleep after spatial experienceJournal of Sleep Research, 7
Gabrielle Girardeau, Ingrid Inema, G. Buzsáki (2017)
Reactivations of emotional memory in the hippocampus–amygdala system during sleepNature Neuroscience, 20
Thomas Davidson, F. Kloosterman, M. Wilson (2009)
Hippocampal Replay of Extended ExperienceNeuron, 63
C. Pavlides, J. Winson (1989)
Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes, 9
R. Buckner (2010)
The role of the hippocampus in prediction and imagination.Annual review of psychology, 61
Chun-Ting Wu, D. Haggerty, C. Kemere, D. Ji (2017)
Hippocampal awake replay in fear memory retrievalNature neuroscience, 20
Xiaojing Wu, David Foster (2014)
Hippocampal Replay Captures the Unique Topological Structure of a Novel EnvironmentThe Journal of Neuroscience, 34
Joseph O’Neill, Charlotte Boccara, Federico Stella, Philipp Schoenenberger, J. Csicsvari (2017)
Superficial layers of the medial entorhinal cortex replay independently of the hippocampusScience, 355
K. Diba, G. Buzsáki (2007)
Forward and reverse hippocampal place-cell sequences during ripplesNature Neuroscience, 10
M. Nokia, J. Mikkonen, M. Penttonen, J. Wikgren, J. Nokia, M. Nokia, J. Mikkonen, M. Penttonen, Susan Sara
This Reprint May Differ from the Original in Pagination and Typographic Detail. Disrupting Neural Activity Related to Awake-state Sharp Wave-ripple Complexes Prevents Hippocampal Learning Disrupting Neural Activity Related to Awake-state Sharp Wave-ripple Complexes Prevents Hippocampal Learning
D. Feldman (2012)
The Spike-Timing Dependence of PlasticityNeuron, 75
E. Tolman (1948)
Cognitive maps in rats and men.Psychological review, 55 4
Dong Wang, Hau-Jie Yau, Carl Broker, Jen-Hui Tsou, A. Bonci, S. Ikemoto (2015)
Mesopontine median raphe regulates hippocampal ripple oscillation and memory consolidationNature neuroscience, 18
H. Kudrimoti, C. Barnes, B. McNaughton (1999)
Reactivation of Hippocampal Cell Assemblies: Effects of Behavioral State, Experience, and EEG DynamicsThe Journal of Neuroscience, 19
(1976)
Concluding Summary
Joseph O’Neill, Timothy Senior, J. Csicsvari (2006)
Place-Selective Firing of CA1 Pyramidal Cells during Sharp Wave/Ripple Network Patterns in Exploratory BehaviorNeuron, 49
Yingxue Wang, S. Romani, Brian Lustig, A. Leonardo, E. Pastalkova (2014)
Theta sequences are essential for internally generated hippocampal firing fieldsNature Neuroscience, 18
K. Kovács, Joseph O’Neill, Philipp Schoenenberger, M. Penttonen, Damaris Guerrero, J. Csicsvari (2016)
Optogenetically Blocking Sharp Wave Ripple Events in Sleep Does Not Interfere with the Formation of Stable Spatial Representation in the CA1 Area of the HippocampusPLoS ONE, 11
J. O’Keefe, M. Recce (1993)
Phase relationship between hippocampal place units and the EEG theta rhythmHippocampus, 3
Mattias Karlsson, L. Frank (2009)
Awake replay of remote experiences in the hippocampusNature neuroscience, 12
W. Skaggs, B. McNaughton (1996)
Replay of Neuronal Firing Sequences in Rat Hippocampus During Sleep Following Spatial ExperienceScience, 271
G. Buzsáki (1986)
Hippocampal sharp waves: Their origin and significanceBrain Research, 398
G. Seol, J. Ziburkus, Shiyong Huang, Lihua Song, In Kim, K. Takamiya, R. Huganir, Hey-Kyoung Lee, A. Kirkwood (2007)
Neuromodulators Control the Polarity of Spike-Timing-Dependent Synaptic PlasticityNeuron, 55
Sreedharan Sajikumar, Sheeja Navakkode, J. Frey (2008)
Distinct single but not necessarily repeated tetanization is required to induce hippocampal late-LTP in the rat CA1.Learning & memory, 15 2
GyÖrgy BuzsÁk (1998)
Memory consolidation during sleep: a neurophysiological perspective.Journal of sleep research, 7 Suppl 1
S. Ramirez, Xu Liu, Pei-Ann Lin, Junghyup Suh, Michele Pignatelli, R. Redondo, T. Ryan, S. Tonegawa (2013)
Creating a False Memory in the HippocampusScience, 341
G. Dragoi, S. Tonegawa (2011)
Preplay of future place cell sequences by hippocampal cellular assembliesNature, 469
G. Buzsáki (1989)
Two-stage model of memory trace formation: A role for “noisy” brain statesNeuroscience, 31
D. Dupret, Joseph O’Neill, Barty Pleydell-Bouverie, J. Csicsvari (2010)
The reorganization and reactivation of hippocampal maps predict spatial memory performanceNature neuroscience, 13
J. Isaac, K. Buchanan, R. Muller, J. Mellor (2009)
Hippocampal Place Cell Firing Patterns Can Induce Long-Term Synaptic Plasticity In VitroThe Journal of Neuroscience, 29
Takeyuki Miyawaki, H. Norimoto, Tomoe Ishikawa, Yusuke Watanabe, N. Matsuki, Y. Ikegaya (2014)
Dopamine Receptor Activation Reorganizes Neuronal Ensembles during Hippocampal Sharp Waves In VitroPLoS ONE, 9
Joseph O’Neill, Barty Pleydell-Bouverie, D. Dupret, J. Csicsvari (2010)
Play it again: reactivation of waking experience and memoryTrends in Neurosciences, 33
A. Singer, Margaret Carr, Mattias Karlsson, L. Frank (2013)
Hippocampal SWR Activity Predicts Correct Decisions during the Initial Learning of an Alternation TaskNeuron, 77
Li Zhang, Hui-zhong Tao, C. Holt, W. Harris, M. Poo (1998)
A critical window for cooperation and competition among developing retinotectal synapsesNature, 395
L. Squire, C. Stark, R. Clark (2004)
The medial temporal lobe.Annual review of neuroscience, 27
Shantanu Jadhav, Gideon Rothschild, Demetris Roumis, L. Frank (2016)
Coordinated Excitation and Inhibition of Prefrontal Ensembles during Awake Hippocampal Sharp-Wave Ripple EventsNeuron, 90
S. Diekelmann, C. Büchel, J. Born, B. Rasch (2011)
Labile or stable: opposing consequences for memory when reactivated during waking and sleepNature Neuroscience, 14
G. Dragoi, G. Buzsáki (2006)
Temporal Encoding of Place Sequences by Hippocampal Cell AssembliesNeuron, 50
H. Hirase, X. Leinekugel, András Czurkó, J. Csicsvari, G. Buzsáki (2001)
Firing rates of hippocampal neurons are preserved during subsequent sleep episodes and modified by novel awake experienceProceedings of the National Academy of Sciences of the United States of America, 98
Ting Feng, Delia Silva, David Foster (2015)
Dissociation between the Experience-Dependent Development of Hippocampal Theta Sequences and Single-Trial Phase PrecessionThe Journal of Neuroscience, 35
A. K. Lee, M. A. Wilson (2002)
Memory of sequential experience in the hippocampus during slow wave sleep, 36
H. Ólafsdóttir, C. Barry, A. Saleem, D. Hassabis, H. Spiers (2015)
Hippocampal place cells construct reward related sequences through unexplored spaceeLife, 4
Colin McNamara, Álvaro Tejero-Cantero, S. Trouche, Natalia Campo-Urriza, D. Dupret (2014)
Dopaminergic neurons promote hippocampal reactivation and spatial memory persistenceNature neuroscience, 17
Brendan Gaesser, R. Spreng, Victoria McLelland, D. Addis, D. Schacter (2013)
Imagining the future: Evidence for a hippocampal contribution to constructive processingHippocampus, 23
J. Knierim (2009)
Faculty Opinions recommendation of Selective suppression of hippocampal ripples impairs spatial memory.
V. Ego-Stengel, M. Wilson (2009)
Disruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the ratHippocampus, 20
M. Witter, F. Wouterlood, P. Naber, T. Haeften (2000)
Anatomical Organization of the Parahippocampal‐Hippocampal NetworkAnnals of the New York Academy of Sciences, 911
H. Ólafsdóttir, Francis Carpenter, C. Barry (2016)
Coordinated grid and place cell replay during restNature Neuroscience, 19
Margaret Carr, Shantanu Jadhav, L. Frank (2011)
Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrievalNature Neuroscience, 14
W. Schultz, P. Dayan, P. Montague (1997)
A Neural Substrate of Prediction and RewardScience, 275
Paweł Cichosz (1999)
An Analysis of Experience Replay in Temporal Difference LearningCybern. Syst., 30
Andrew Wikenheiser, A. Redish (2013)
The balance of forward and backward hippocampal sequences shifts across behavioral statesHippocampus, 23
A. Redish, D. Touretzky (1998)
The Role of the Hippocampus in Solving the Morris Water MazeNeural Computation, 10
M. Moser, David Rowland, E. Moser (2015)
Place cells, grid cells, and memory.Cold Spring Harbor perspectives in biology, 7 2
Jadin Jackson, Adam Johnson, A. Redish (2006)
Hippocampal Sharp Waves and Reactivation during Awake States Depend on Repeated Sequential ExperienceThe Journal of Neuroscience, 26
G. Dragoi, S. Tonegawa (2013)
Distinct preplay of multiple novel spatial experiences in the ratProceedings of the National Academy of Sciences, 110
Yaniv Ziv, Laurie Burns, E. Cocker, E. Hamel, Kunal Ghosh, L. Kitch, Abbas Gamal, M. Schnitzer (2013)
Long-term dynamics of CA1 hippocampal place codesNature neuroscience, 16
G. Buzsáki (1996)
The hippocampo-neocortical dialogue.Cerebral cortex, 6 2
Mathew Wilson, B. McNaughton (1994)
Reactivation of hippocampal ensemble memories during sleep.Science, 265 5172
(2009)
Selective suppression of hippocampal ripples impairs spatial memory, 12
Jun Yamamoto, S. Tonegawa (2017)
Direct Medial Entorhinal Cortex Input to Hippocampal CA1 Is Crucial for Extended Quiet Awake ReplayNeuron, 96
P. Lewis, S. Durrant (2011)
Overlapping memory replay during sleep builds cognitive schemataTrends in Cognitive Sciences, 15
Yan-You Huang, E. Kandel (2005)
Theta frequency stimulation induces a local form of late phase LTP in the CA1 region of the hippocampus.Learning & memory, 12 6
A. Singer, L. Frank (2009)
Rewarded Outcomes Enhance Reactivation of Experience in the HippocampusNeuron, 64
(2018)
How to cite this article: Pfeiffer BE. The content of hippocampal "replay
Wei Xu, T. Südhof (2013)
A Neural Circuit for Memory Specificity and GeneralizationScience, 339
David Foster, M. Wilson (2007)
Hippocampal theta sequencesHippocampus, 17
D. Marr (1971)
Simple memory: a theory for archicortex.Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 262 841
Brad Pfeiffer, David Foster (2013)
Hippocampal place cell sequences depict future paths to remembered goalsNature, 497
Anoopum Gupta, Matthijs Meer, D. Touretzky, A. Redish (2010)
Hippocampal Replay Is Not a Simple Function of ExperienceNeuron, 65
W. Scoville, B. Milner (1957)
LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONSJournal of Neurology, Neurosurgery & Psychiatry, 20
Ayelet Sarel, Arseny Finkelstein, Liora Las, N. Ulanovsky (2017)
Vectorial representation of spatial goals in the hippocampus of batsScience, 355
S. Josselyn, S. Köhler, P. Frankland (2015)
Finding the engramNature Reviews Neuroscience, 16
R. Muller, E. Bostock, J. Taube, J. Kubie (1994)
On the directional firing properties of hippocampal place cells, 14
R. Morris, P. Garrud, J. Rawlins, J. O’Keefe (1982)
Place navigation impaired in rats with hippocampal lesionsNature, 297
D. Tse, R. F. Langston, M. Kakeyama, I. Bethus, P. A. Spooner, E. R. Wood, R. G. M. Morris (2007)
Schemas and memory consolidation, 316
D. Ji, M. Wilson (2007)
Coordinated memory replay in the visual cortex and hippocampus during sleepNature Neuroscience, 10
L. Roux, Bo Hu, Ronny Eichler, E. Stark, G. Buzsáki (2017)
Sharp wave ripples during learning stabilize hippocampal spatial mapNature neuroscience, 20
One of the most striking features of the hippocampal network is its ability to self‐generate neuronal sequences representing temporally compressed, spatially coherent paths. These brief events, often termed “replay” in the scientific literature, are largely confined to non‐exploratory states such as sleep or quiet rest. Early studies examining the content of replay noted a strong correlation between the encoded spatial information and the animal's prior behavior; thus, replay was initially hypothesized to play a role in memory formation and/or systems‐level consolidation via “off‐line” reactivation of previous experiences. However, recent findings indicate that replay may also serve as a memory retrieval mechanism to guide future behavior or may be an incidental reflection of pre‐existing network assemblies. Here, I will review what is known regarding the content of replay events and their correlation with past and future actions, and I will discuss how this knowledge might inform or constrain models which seek to explain the circuit‐level mechanisms underlying these events and their role in mnemonic processes.
Hippocampus – Wiley
Published: Jan 1, 2020
Keywords: ; ; ; ;
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