Cited by 1,709Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeural dynamics and brain function

The DOI matches its Crossref record; 156 of the 160 references it cites were found in a registry or an index.

Two-stage model of memory trace formation: A role for “noisy” brain states

Buzsáki, G.·1989·Neuroscience

Open this paper in CoChat — free account

Abstract

Review of the normally occurring neuronal patterns of the hippocampus suggests that the two principal cell types of the hippocampus, the pyramidal neurons and granule cells, are maximally active during different behaviors. Granule cells reach their highest discharge rates during theta-concurrent exploratory activities, while population synchrony of pyramidal cells is maximum during immobility, consummatory behaviors, and slow wave sleep associated with field sharp waves. Sharp waves reflect the summed postsynaptic depolarization of large numbers of pyramidal cells in the CA1 and subiculum as a consequence of synchronous discharge of bursting CA3 pyramidal neurons. The trigger for the population burst in the CA3 region is the temporary release from subcortical tonic inhibition. An overview of the experimentally explored criteria of synaptic enhancement (intensity, frequency, and pattern of postsynaptic depolarization, calcium influx, cooperativity, threshold) suggests that these requirements may be present during sharp wave-concurrent population bursts of pyramidal cells. Experimental evidence is cited showing that (a) population bursts in CA3 may lead to long-term potentiation in their postsynaptic CA1 targets, (b) tetanizing stimuli are capable of increasing the synchrony of the sharp wave-burst, and (c) activity patterns of the neocortical input to the hippocampus determine which subgroup of CA3 neurons will trigger subsequently occurring population bursts (initiator cells). Based on the experimental evidence reviewed a formal model of memory trace formation is outlined. During exploratory (theta) behaviors the neocortical information is transmitted to the hippocampus via the fast-firing granule cells which may induce a weak and transient heterosynaptic potentiation in a subgroup of CA3 pyramidal cells. The weakly potentiated CA3 neurons will then initiate population bursts upon the termination of exploratory activity (sharp wave state). It is assumed that recurrent excitation during the population burst is strongest on those cells which initiated the population event. It is suggested that the strong excitatory drive brought about by the sharp wave-concurrent population bursts during consummatory behaviors, immobility, and slow wave sleep may be sufficient for the induction of long-term synaptic modification in the initiator neurons of the CA3 region and in their targets in CA1. In this two-stage model both exploratory (theta) and sharp wave states of the hippocampus are essential and any interference that might modify the structure of the population bursts (e.g. epileptic spikes) is detrimental to memory trace formation.

Integrity signals

Registry

Crossref · 10.1016/0306-4522(89)90423-5

Cites

156 of 156 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

The Organization of Behavior
Hebb, D. O. (2005) · doi:10.4324/9781410612403 · Cited by 9,825
Untitled work
(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010
Long‐lasting potentiation of synaptic transmission in the dentate area of the unanaesthetized rabbit following stimulation of the perforant path
Bliss, T. V. P., & Gardner-Medwin, A. R. (1973) · The Journal of Physiology · doi:10.1113/jphysiol.1973.sp010274 · Cited by 7,424
Modification of seizure activity by electrical stimulation: II. Motor seizure
Racine, R. J. (1972) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(72)90177-0 · Cited by 7,141
The organization of behavior.
indicated, N. A. (1950) · Journal of Consulting Psychology · doi:10.1037/h0049612 · Cited by 6,984
The hippocampus as a cognitive map
Passingham, R. E. (1979) · Neuroscience · doi:10.1016/0306-4522(79)90015-0 · Cited by 5,128
Brain stem reticular formation and activation of the EEG
Moruzzi, G., & Magoun, H. W. (1949) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(49)90219-9 · Cited by 4,307
Principles of Behavior
Skinner, B. F., & Hull, C. L. (1944) · The American Journal of Psychology · doi:10.2307/1416955 · Cited by 4,061
Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5
Morris, R. G. M., Anderson, E., Lynch, G. S., & Baudry, M. (1986) · Nature · doi:10.1038/319774a0 · Cited by 3,640
Behavior of Organisms
Skinner, B. F. (1938) · Cited by 3,571

Show all 160 references

Research works printed but not linked: 8

Auerbach, 1988, Nervenendigungen in den Centralorganen, Neurol. Zentralbl., 17, 445
Ben-Ari Y., Represa A., Robain O., Tremblay E. and Le Gal La Salle G. Sprouting of mossy fibers in the hippocampus of epileptic patients and kindled and kainate treated rats. InNeurotransmitters, Seizures and Epilepsy (eds Avanzini G., Fariello R., Heinemann U. and Engel J. Jr). Demos Press, New York (in press).
Buzsáki, 1986, Generation of hippocampal EEG patterns, Vol. 3, 137
Buzsáki G. and Gage F. H. Fetal brain tissue grafts modulate neuronal excitability in a chronic model of epilepsy. InNeurotransmitters, Seizures and Epilepsy (eds Avanzini G., Fariello R., Heinemann U. and Engel J. Jr). Demos Press, New York (in press).
Crowne, 1975, Some characteristics of functional relations of the electrical activity of the primate hippocampus and hypotheses of hippocampal function, Vol. 2, 185
Ellman, 1978, REM deprivation: a review, 419
Jouvet, 1959, L'activite electrique du rhinencephale au cours du sommeil chez le chat, C.r. Séanc. Soc. Biol., 153, 101
McNaughton, 1982, Directional specificity of rat hippocampal “pace cells” on a radical 8-arm maze, Soc. Neurosci. Abstr., 12, 86.10

Sorted by citations

Items 601–700 of 1,004

Reconstruction of hippocampal granule cell electrophysiology by computer simulation
Yuen, G., & Durand, D. M. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90337-n · Cited by 53
A critical appraisal of the what-where-when episodic-like memory test in rodents: Achievements, caveats and future directions
Binder, S., Dere, E., & Zlomuzica, A. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.04.002 · Cited by 56
Causal Contribution of Awake Post-encoding Processes to Episodic Memory Consolidation
Tambini, A., & D’Esposito, M. (2020) · Current Biology · doi:10.1016/j.cub.2020.06.063 · Cited by 54
In Vivo Whole-Cell Patch-Clamp Methods: Recent Technical Progress and Future Perspectives
Noguchi, A., Ikegaya, Y., & Matsumoto, N. (2021) · Sensors · doi:10.3390/s21041448 · Cited by 58
Looking for the neural basis of memory
Kragel, J. E., & Voss, J. L. (2021) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2021.10.010 · Cited by 52
Alterations of sleep oscillations in Alzheimer's disease: A potential role for GABAergic neurons in the cortex, hippocampus, and thalamus
Katsuki, F., Gerashchenko, D., & Brown, R. E. (2022) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2022.07.002 · Cited by 50
Cell assemblies, sequences and temporal coding in the hippocampus
Dragoi, G. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.03.003 · Cited by 56
Recruitment of an inhibitory hippocampal network after bursting in a single granule cell
Mori, M., Gähwiler, B. H., & Gerber, U. R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702164104 · Cited by 55
Consolidation of sensorimotor learning during sleepPreprint
Brawn, T. P., Fenn, K. M., Nusbaum, H. C., & Margoliash, D. (2008) · Learning & Memory · doi:10.1101/lm.1180908 · Cited by 52
Not only…but also: REM sleep creates and NREM Stage 2 instantiates landmark junctions in cortical memory networks
Llewellyn, S., & Hobson, J. A. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.04.005 · Cited by 54
The role of experience in prioritizing hippocampal replay
Gorriz, M. H., Takigawa, M., & Bendor, D. (2023) · Nature Communications · doi:10.1038/s41467-023-43939-z · Cited by 59
Altered hippocampal information coding and network synchrony in APP-PS1 mice
Cayzac, S., Mons, N. E., Ginguay, A., Allinquant, B., Jeantet, Y., & Cho, Y. H. (2015) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2015.08.023 · Cited by 54
Sharp wave/ripple network oscillations and learning-associated hippocampal maps
Csicsvari, J., & Dupret, D. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0528 · Cited by 55
Hippocampal CA1 replay becomes less prominent but more rigid without inputs from medial entorhinal cortex
Chenani, A., Sabariego, M., Schlesiger, M. I., Leutgeb, J. K., Leutgeb, S., & Leibold, C. (2019) · Nature Communications · doi:10.1038/s41467-019-09280-0 · Cited by 52
Sleep and Epilepsy Link by Plasticity
Halász, P., & Szűcs, A. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00911 · Cited by 51
Circadian rhythms, aging and memory
Antoniadis, E. A., Ko, C. H., Ralph, M. R., & McDonald, R. J. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00145-5 · Cited by 54
Behavior‐dependent activity patterns of GABAergic long‐range projecting neurons in the rat hippocampus
Katona, L., Micklem, B., Borhegyi, Z., Swiejkowski, D. A., Valenti, O., Viney, T. J., Kotzadimitriou, D., Klausberger, T., & Somogyi, P. (2017) · Hippocampus · doi:10.1002/hipo.22696 · Cited by 50
Preferential consolidation of emotionally salient information during a nap is preserved in middle age
Alger, S. E., Kensinger, E. A., & Payne, J. D. (2018) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2018.03.030 · Cited by 50
Interictal spikes with and without high-frequency oscillation have different single-neuron correlates
Guth, T. A., Kunz, L., Brandt, A., Dümpelmann, M., Klotz, K. A., Reinacher, P. C., Schulze‐Bonhage, A., Jacobs, J., & Schönberger, J. (2021) · Brain · doi:10.1093/brain/awab288 · Cited by 51
Temporal context and latent state inference in the hippocampal splitter signal
Duvelle, É., Grieves, R. M., & van der Meer, M. A. A. (2022) · eLife · doi:10.7554/elife.82357 · Cited by 56
Cell Type-Specific Synaptic Dynamics of Synchronized Bursting in the Juvenile CA3 Rat Hippocampus
Aradi, I., & Maccaferri, G. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2800-04.2004 · Cited by 50
Sleep selectively enhances hippocampus-dependent memory in mice.
Cai, D. J., Shuman, T., Gorman, M. R., Sage, J. R., & Anagnostaras, S. (2009) · Behavioral Neuroscience · doi:10.1037/a0016415 · Cited by 53
Theta burst stimulation‐induced LTP: Differences and similarities between the dorsal and ventral CA1 hippocampal synapses
Kouvaros, S., & Papatheodoropoulos, C. (2016) · Hippocampus · doi:10.1002/hipo.22655 · Cited by 54
The differential effects of emotional salience on direct associative and relational memory during a nap
Alger, S. E., & Payne, J. D. (2016) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-016-0460-1 · Cited by 54
Task-dependent mixed selectivity in the subiculum
Ledergerber, D., Battistin, C., Blackstad, J. S., Gardner, R. J., Witter, M. P., Moser, M., Roudi, Y., & Moser, E. I. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109175 · Cited by 53
Different effects of anxiolytic agents, diazepam and 5-HT1A agonist tandospirone, on hippocampal long-term potentiation in vivo
Mori, K., Togashi, H., Kojima, T., Matsumoto, M., Ohashi, S., Ueno, K.-I., & Yoshioka, M. (2001) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00546-9 · Cited by 49
Slow-γ Rhythms Coordinate Cingulate Cortical Responses to Hippocampal Sharp-Wave Ripples during Wakefulness
Remondes, M., & Wilson, M. A. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.10.005 · Cited by 46
The entorhinal cortex and neurotrophin signaling in Alzheimer’s disease and other disorders
Scharfman, H. E., & Chao, M. V. (2013) · Cognitive Neuroscience · doi:10.1080/17588928.2013.826184 · Cited by 52
The Role of Sleep in Human Declarative Memory Consolidation
Alger, S. E., Chambers, A. M., Cunningham, T. J., & Payne, J. D. (2014) · Current topics in behavioral neurosciences · doi:10.1007/7854_2014_341 · Cited by 55
Local Sleep Oscillations: Implications for Memory Consolidation
Geva‐Sagiv, M., & Nir, Y. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00813 · Cited by 56
Changes in the sensory processing of olfactory signals induced by birth in sleep
Kendrick, K. M., Lévy, F., & Keverne, E. B. (1992) · Science · doi:10.1126/science.256.5058.833 · Cited by 46
Delayed Onset of a Daytime Nap Facilitates Retention of Declarative Memory
Alger, S. E., Lau, H., & Fishbein, W. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012131 · Cited by 48
Progressive Functional Impairments of Hippocampal Neurons in a Tauopathy Mouse Model
Ciupek, S. M., Cheng, J., Ali, Y., Lu, H., & Ji, D. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3130-14.2015 · Cited by 49
Making Waves in the Brain: What Are Oscillations, and Why Modulating Them Makes Sense for Brain Injury
Pevzner, A., Izadi, A., Lee, D. J., Shahlaie, K., & Gurkoff, G. G. (2016) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2016.00030 · Cited by 51
Sex differences in hippocampal area CA3 pyramidal cells
Scharfman, H. E., & MacLusky, N. J. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23927 · Cited by 49
The Role of Sleep in Declarative Memory Consolidation—Direct Evidence by Intracranial EEG
Axmacher, N., Haupt, S., Fernández, G., Elger, C. E., & Fell, J. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm084 · Cited by 49
Spatial working memory over long retention intervals: Dependence on sustained cholinergic activation in the septohippocampal or nucleus basalis magnocellularis-cortical pathways?
Durkin, T. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90469-3 · Cited by 48
Structured cognition and neural systems: From rats to language
Battaglia, F. P., Borensztajn, G., & Bod, R. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.04.004 · Cited by 47
The axon as a unique computational unit in neurons
Sasaki, T. (2013) · Neuroscience Research · doi:10.1016/j.neures.2012.12.004 · Cited by 47
Effects of M 1 and M 4 activation on excitatory synaptic transmission in CA 1
Thorn, C. A., Popiolek, M., Stark, E., & Edgerton, J. R. (2017) · Hippocampus · doi:10.1002/hipo.22732 · Cited by 47
Brain Rhythms During Sleep and Memory Consolidation: Neurobiological Insights
Marshall, L., Cross, N. E., Binder, S., & Dang‐Vu, T. T. (2019) · Physiology · doi:10.1152/physiol.00004.2019 · Cited by 52
Impaired Hippocampal-Cortical Interactions during Sleep in a Mouse Model of Alzheimer’s Disease
Cushing, S. D., Skelin, I., Moseley, S. C., Stimmell, A. C., Dixon, J. R., Melilli, A. S., Molina, L. A., McNaughton, B. L., & Wilber, A. A. (2020) · Current Biology · doi:10.1016/j.cub.2020.04.087 · Cited by 51
Replay in minds and machines
Wittkuhn, L., Chien, S., Hall-McMaster, S., & Schuck, N. W. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.08.002 · Cited by 49
Neuronal activity of the septal pacemaker of theta rhythm under the influence of stimulation and blockade of the median raphe nucleus in the awake rabbit
Kitchigina, V. F., Kudina, T. A., Kutyreva, E. V., & Vinogradova, O. S. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00258-4 · Cited by 47
Cell Assemblies in the Cortico-Hippocampal-Reuniens Network during Slow Oscillations
Angulo‐García, D., Ferraris, M., Ghestem, A., Nallet-Khosrofian, L., Bernard, C., & Quilichini, P. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0571-20.2020 · Cited by 49
Advances in the Application of Technology to Epilepsy: The CIMIT/NIO Epilepsy Innovation Summit
Schachter, S. C., Guttag, J. V., Schiff, S. J., & Schomer, D. L. (2009) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2009.06.028 · Cited by 46
Characterization of Inhibitory Circuits in the Malformed Hippocampus ofLis1Mutant Mice
Jones, D., & Baraban, S. C. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00938.2007 · Cited by 46
A bird-brain view of episodic memory
Rattenborg, N. C., & Martinez-Gonzalez, D. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.03.030 · Cited by 45
Intra- and interregional cortical interactions related to sharp-wave ripples and dentate spikes
Headley, D. B., Kanta, V., & Paré, D. (2016) · Journal of Neurophysiology · doi:10.1152/jn.00644.2016 · Cited by 45
On the methods for reactivation and replay analysis
Tingley, D., & Peyrache, A. (2020) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0231 · Cited by 52
Synaptic plasticity and self-organization in the hippocampus
Buzsáki, G., & Chrobak, J. J. (2005) · Nature Neuroscience · doi:10.1038/nn1105-1418 · Cited by 45
Self-citation
Simultaneous activation of gamma and theta network oscillations in rat hippocampal slice cultures
Fischer, Y., Wittner, L., Freund, T. F., & Gähwiler, B. H. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2001.013050 · Cited by 47
Functional neural anatomy of talent
Kalbfleisch, M. L. (2004) · The Anatomical Record Part B The New Anatomist · doi:10.1002/ar.b.20010 · Cited by 47
Relationships between testing-induced alterations of hippocampal cholinergic activity and memory performance on two spatial tasks in mice
Marighetto, A. (1993) · Behavioural Brain Research · doi:10.1016/0166-4328(93)90031-k · Cited by 48
Prenatal Stress Produces Persistence of Remote Memory and Disrupts Functional Connectivity in the Hippocampal–Prefrontal Cortex Axis
Negrón-Oyarzo, I., Neira, D., Espinosa, N., Fuentealba, P., & Aboitiz, F. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhu108 · Cited by 50
Slow oscillatory transcranial direct current stimulation (so-tDCS) during slow wave sleep has no effects on declarative memory in healthy young subjects
Bueno‐Lopez, A., Eggert, T., Dorn, H., & Danker‐Hopfe, H. (2019) · Brain stimulation · doi:10.1016/j.brs.2019.02.012 · Cited by 50
The spatiotemporal organization of experience dictates hippocampal involvement in primary visual cortical plasticity
Finnie, P. S. B., Komorowski, R. W., & Bear, M. F. (2021) · Current Biology · doi:10.1016/j.cub.2021.06.079 · Cited by 44
In Vivo Multi-Day Calcium Imaging of CA1 Hippocampus in Freely Moving Rats Reveals a High Preponderance of Place Cells with Consistent Place Fields
Wirtshafter, H. S., & Disterhoft, J. F. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1750-21.2022 · Cited by 45
Threshold-linear formal neurons in auto-associative nets
Treves, A. (1990) · Journal of Physics A Mathematical and General · doi:10.1088/0305-4470/23/12/037 · Cited by 44
Chapter 1 Neuromodulation and the hippocampus: memory function and dysfunction in a network simulation
Hasselmo, M. E. (1999) · Progress in brain research · doi:10.1016/s0079-6123(08)63064-2 · Cited by 44
Hippocampal Ripple Oscillations and Inhibition-First Network Models: Frequency Dynamics and Response to GABA Modulators
Donoso, J. R., Schmitz, D., Maier, N., & Kempter, R. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0188-17.2018 · Cited by 43
Stimulating the sleeping brain: Current approaches to modulating memory-related sleep physiology
Cellini, N., & Mednick, S. C. (2018) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2018.11.011 · Cited by 45
Sleep-dependent directional coupling between human neocortex and hippocampus
Wagner, T., Axmacher, N., Lehnertz, K., Elger, C. E., & Fell, J. (2009) · Cortex · doi:10.1016/j.cortex.2009.05.012 · Cited by 47
Neurophysiological correlates of eye movement desensitization and reprocessing sessions: preliminary evidence for traumatic memories integration
Farina, B., Imperatori, C., Quintiliani, M. I., Gattinara, P. C., Onofri, A., Lepore, M., Brunetti, R., Losurdo, A., Testani, E., & Marca, G. D. (2014) · Clinical Physiology and Functional Imaging · doi:10.1111/cpf.12184 · Cited by 43
Cannabinoids attenuate hippocampal gamma oscillations by suppressing excitatory synaptic input onto CA3 pyramidal neurons and fast spiking basket cells
Holderith, N. B., Németh, B., Papp, O. I., Veres, J. M., Nagy, G. A., & Hájos, N. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.216259 · Cited by 42
Neuronal Activity and Amyloid Plaque Pathology: An Update
Ovsepian, S. V., & O’Leary, V. B. (2015) · Journal of Alzheimer s Disease · doi:10.3233/jad-150544 · Cited by 42
Rhythmic Constraints on Hippocampal Processing: State and Phase-Related Fluctuations of Synaptic Excitability During Theta and the Slow Oscillation
Schall, K. P., Kerber, J., & Dickson, C. T. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00915.2007 · Cited by 42
The prominent role of stimulus processing
Furey, M. L. (2011) · Current Opinion in Neurology · doi:10.1097/wco.0b013e328348bda5 · Cited by 42
Hippocampal Sleep Features: Relations to Human Memory Function
Ferrara, M., Moroni, F., Gennaro, L. D., & Nobili, L. (2012) · Frontiers in Neurology · doi:10.3389/fneur.2012.00057 · Cited by 43
Contribution of transcranial oscillatory stimulation to research on neural networks: an emphasis on hippocampo-neocortical rhythms
Marshall, L., & Binder, S. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00614 · Cited by 42
Reward Cues in Space: Commonalities and Differences in Neural Coding by Hippocampal and Ventral Striatal Ensembles
Lansink, C. S., Jackson, J. C., Lankelma, J. V., Ito, R., Robbins, T. W., Everitt, B. J., & Pennartz, C. M. A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0593-12.2012 · Cited by 45
Routes to, from and within the subiculum
Böhm, C., Peng, Y., Geiger, J. R. P., & Schmitz, D. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2848-4 · Cited by 44
Processing of Hippocampal Network Activity in the Receiver Network of the Medial Entorhinal Cortex Layer V
Rozov, A. V., Rannap, M., Lorenz, F., Nasretdinov, A., Draguhn, A., & Egorov, A. V. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0586-20.2020 · Cited by 45
Reactivation of behavioral activity during sharp waves: A computational model for two stage hippocampal dynamics
Molter, C., Sato, N., & Yamaguchi, Y. (2007) · Hippocampus · doi:10.1002/hipo.20258 · Cited by 42
Slow wave sleep in naps supports episodic memories in early childhood
Lokhandwala, S., & Spencer, R. M. C. (2021) · Developmental Science · doi:10.1111/desc.13035 · Cited by 41
Contributions of extracellular-signal regulated kinase 1/2 activity to the memory trace
Ramos, S. O., Feld, M., & Fustiñana, M. S. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.988790 · Cited by 43
Consistent sequential activity across diverse forms of UP states under ketamine anesthesia
Luczak, A., & Barthó, P. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08201.x · Cited by 41
Variability in State-Dependent Plasticity of Intrinsic Properties during Cell-Autonomous Self-Regulation of Calcium Homeostasis in Hippocampal Model Neurons
Srikanth, S., & Narayanan, R. (2015) · eNeuro · doi:10.1523/eneuro.0053-15.2015 · Cited by 41
Modulation of Adult Hippocampal Neurogenesis by Sleep: Impact on Mental Health
Navarro-Sanchis, C., Brock, O., Winsky‐Sommerer, R., & Thuret, S. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00074 · Cited by 43
The transformation of multi-sensory experiences into memories during sleep
Rothschild, G. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.03.019 · Cited by 45
Dissociating medial temporal and basal ganglia memory systems with a latent learning task
Myers, C. E., Daphna Shohamy, A., Gluck, M. A., Grossman, S., Onla-or, S., & Kapur, N. (2003) · Neuropsychologia · doi:10.1016/s0028-3932(03)00127-1 · Cited by 41
Frequency-Dependent Gating of Hippocampal–Neocortical Interactions
Moreno, A., Morris, R., & Canals, S. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv033 · Cited by 42
New evidence for the necessity of a silent plastic period during sleep for a memory benefit of targeted memory reactivation
Farthouat, J., Gilson, M., & Peigneux, P. (2017) · Sleep Spindles & Cortical Up States · doi:10.1556/2053.1.2016.002 · Cited by 42
Septal Lesions Impair the Acquisition of a Cued Place Navigation Task: Attentional or Memory Deficit?
Brandner, C., & Schenk, F. (1998) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1997.3814 · Cited by 41
Rewinding the memory record
Colgin, L. L., & Moser, E. I. (2006) · Nature · doi:10.1038/440615a · Cited by 42
Brain State Dependence of Hippocampal Subthreshold Activity in Awake Mice
Hulse, B. K., Lubenov, E. V., & Siapas, A. G. (2017) · Cell Reports · doi:10.1016/j.celrep.2016.11.084 · Cited by 40
A stable hippocampal representation of a space requires its direct experience
Rowland, D. C., Yanovich, Y., & Kentros, C. G. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105445108 · Cited by 40
Cognitive impairment in temporal lobe epilepsy: Role of online and offline processing of single cell information
Titiz, A. S., Mahoney, J. M., Testorf, M. E., Holmes, G. L., & Scott, R. C. (2014) · Hippocampus · doi:10.1002/hipo.22297 · Cited by 40
Novel object presentation affects sleep–wake behavior in rats
Schiffelholz, T., & Aldenhoff, J. B. (2002) · Neuroscience Letters · doi:10.1016/s0304-3940(02)00452-4 · Cited by 40
Frequency of network synchronization in the hippocampus marks learning
Ponomarenko, A. A., Li, J., Korotkova, T. M., Huston, J. P., & Haas, H. L. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06232.x · Cited by 40
Behavioral Transitions Modulate Hippocampal Electroencephalogram Correlates of Open Field Behavior in the Rat: Support for a Sensorimotor Function of Hippocampal Rhythmical Synchronous Activity
van Lier, H., Coenen, A. M. L., & Drinkenburg, W. H. I. M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-06-02459.2003 · Cited by 40
Homeostatic regulation of memory systems and adaptive decisions
Mizumori, S. J. Y., & Jo, Y. S. (2013) · Hippocampus · doi:10.1002/hipo.22176 · Cited by 43
Neural Activity Patterns Underlying Spatial Coding in the Hippocampus
Sosa, M., Gillespie, A. K., & Frank, L. M. (2016) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_462 · Cited by 43
A Novel Approach to Dream Content Analysis Reveals Links Between Learning-Related Dream Incorporation and Cognitive Abilities
Fogel, S. M., Ray, L. B., Sergeeva, V., Koninck, J. D., & Owen, A. M. (2018) · Frontiers in Psychology · doi:10.3389/fpsyg.2018.01398 · Cited by 42
Neuromodulation and a Reconceptualization of Autism Spectrum Disorders: Using the Locus Coeruleus Functioning as an Exemplar
London, E. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.01120 · Cited by 40
De novo inter-regional coactivations of preconfigured local ensembles support memory
Miyawaki, H., & Mizuseki, K. (2022) · Nature Communications · doi:10.1038/s41467-022-28929-x · Cited by 42
Mixed-mode oscillations in a three time-scale system of ODEs motivated by a neuronal model
Jalics, J. Z., Крупа, М. М., & Rotstein, H. G. (2010) · Dynamical Systems · doi:10.1080/14689360903535760 · Cited by 40
The Timing of Learning before Night-Time Sleep Differentially Affects Declarative and Procedural Long-Term Memory Consolidation in Adolescents
Holz, J., Piosczyk, H., Landmann, N., Feige, B., Spiegelhalder, K., Riemann, D. W., Nissen, C., & Voderholzer, U. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040963 · Cited by 43
Cholinergic enhancement reduces functional connectivity and BOLD variability in visual extrastriate cortex during selective attention
Ricciardi, E., Handjaras, G., Bernardi, G., Pietrini, P., & Furey, M. L. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.07.003 · Cited by 39
Breathing Coordinates Limbic Network Dynamics Underlying Memory ConsolidationPreprint
Karalis, N., & Sirota, A. (2018) · SSRN Electronic Journal · doi:10.2139/ssrn.3283711 · Cited by 43

Authors: Buzsáki, G.
Affiliations: University of California System (US)
Corresponding author: Buzsáki, G.
ORCID: Buzsáki, G.
Venue: Neuroscience
Publisher: Elsevier BV
Published: 1989-01
Volume: 31
Issue: 3
Pages: 551-570
ISSN: 0306-4522 (ISSN-L)
DOI: 10.1016/0306-4522(89)90423-5
OpenAlex: W2020272049
Cited by: 1,709
References: 160
Citations by year: 2026: 43 · 2025: 63 · 2024: 74 · 2023: 86 · 2022: 64 · 2021: 67 · 2020: 65 · 2019: 86 · 2018: 73 · 2017: 70 · 2016: 56 · 2015: 64 · 2014: 80 · 2013: 66 · 2012: 53
FWCI: 2.53
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords: memory trace formation, hippocampus, sharp-wave ripples, CA3 pyramidal cells, CA1, granule cells, theta oscillations, population bursts, long-term potentiation, synaptic plasticity, slow-wave sleep, recurrent excitation, two-stage model
MeSH terms: Animals, Hippocampus, Memory, Models, Neurological, Neuronal Plasticity, Rats

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Two-stage model of memory trace formation: A role for “noisy” brain states

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks