Replay and Time Compression of Recurring Spike Sequences in the Hippocampus
Open accessAbstract
Information in neuronal networks may be represented by the spatiotemporal patterns of spikes. Here we examined the temporal coordination of pyramidal cell spikes in the rat hippocampus during slow-wave sleep. In addition, rats were trained to run in a defined position in space (running wheel) to activate a selected group of pyramidal cells. A template-matching method and a joint probability map method were used for sequence search. Repeating spike sequences in excess of chance occurrence were examined by comparing the number of repeating sequences in the original spike trains and in surrogate trains after Monte Carlo shuffling of the spikes. Four different shuffling procedures were used to control for the population dynamics of hippocampal neurons. Repeating spike sequences in the recorded cell assemblies were present in both the awake and sleeping animal in excess of what might be predicted by random variations. Spike sequences observed during wheel running were “replayed” at a faster timescale during single sharp-wave bursts of slow-wave sleep. We hypothesize that the endogenously expressed spike sequences during sleep reflect reactivation of the circuitry modified by previous experience. Reactivation of acquired sequences may serve to consolidate information.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Entire spike trains observed during a task performed during prior waking reemerged in the same temporal order during succeeding sleep, with replay running at a faster speed (time-compressed).
“In fact, entire spike trains observed during a task performed during prior waking reemerged in the same temporal order during succeeding sleep, with this “replay” running at a faster speed, i.e., in a time-compressed form (715, 716, 843).”
From About Sleep's Role in Memory (2013) · cites this paper as [843]
The Abstract and ‘Externally controlled and internally generated recurring spike sequences’ report that sequences seen during wheel running recurred in subsequent slow-wave sleep at a faster timescale, mainly during sharp-wave bursts. But ‘Behavioral modification of spike sequences’ describes shared short sequences, including spike triplets—not entire spike trains reemerging in full. (LLM, conf=0.88)
Experimental — accuracy not yet measuredDuring SWS, firing patterns observed during waking are replayed at a much faster (10-20 times) rate.
“1) during SWS, firing patterns observed during waking are replayed at a much faster (10 -20 times) rate, suggesting a time-compressed form of memory reactivation (160, 551, 606, 715, 843, 1090);”
From About Sleep's Role in Memory (2013) · cites this paper as [843]
The Abstract and the section on externally controlled and internally generated recurring spike sequences report that waking spike sequences were replayed on a faster timescale during sharp-wave bursts of slow-wave sleep. The passages do not establish the claimed 10–20-fold rate; the 10–20 msec figure elsewhere describes a spike-search window, not replay speed. Page numbers are unavailable in our copy. (LLM, conf=0.87)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010 · see citing works
McClelland, J. L., McNaughton, B. L., & O'Reilly, R. C. (1995) · Psychological Review · doi:10.1037/0033-295x.102.3.419 · Cited by 5,256 · see citing works
The Integrative Action of the Nervous System.
Sherrington, C. (1907) · The Journal of Nervous and Mental Disease · doi:10.1097/00005053-190734120-00021 · Cited by 4,136 · see citing works
Reactivation of hippocampal ensemble memories during sleep
Wilson, M. A., & McNaughton, B. L. (1994) · Science · doi:10.1126/science.8036517 · Cited by 3,118 · see citing works
Phase relationship between hippocampal place units and the EEG theta rhythm
O'Keefe, J. M., & Recce, M. L. (1993) · Hippocampus · doi:10.1002/hipo.450030307 · Cited by 2,561 · see citing works
Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex
Gray, C. M., & Singer, W. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.5.1698 · Cited by 2,463 · see citing works
Coherent oscillations: A mechanism of feature linking in the visual cortex?
Eckhorn, R., Bauer, R., Jordan, W., Brosch, M., Kruse, W., Munk, M., & Reitboeck, H. J. (1988) · Biological Cybernetics · doi:10.1007/bf00202899 · Cited by 2,329 · see citing works
Llinás, R. R. (1988) · Science · doi:10.1126/science.3059497 · Cited by 2,285 · see citing works
Shadlen, M. N., & Newsome, W. T. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-10-03870.1998 · Cited by 2,178 · see citing works
Georgopoulos, A. P., Kalaska, J. F., Caminiti, R., & Massey, J. (1982) · Journal of Neuroscience · doi:10.1523/jneurosci.02-11-01527.1982 · Cited by 2,133 · see citing works
Single Units and Sensation: A Neuron Doctrine for Perceptual Psychology?
Barlow, H. B. (1972) · Perception · doi:10.1068/p010371 · Cited by 1,714 · see citing works
Two-stage model of memory trace formation: A role for “noisy” brain states
Buzsáki, G. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90423-5 · Cited by 1,709 · see citing works
Self-citationSynchronization of cortical activity and its putative role in information processing and learning
Singer, W. (1993) · Annual Review of Physiology · doi:10.1146/annurev.ph.55.030193.002025 · Cited by 1,685 · see citing works
Whittington, M. A., Traub, R. D., & Jefferys, J. G. R. (1995) · Nature · doi:10.1038/373612a0 · Cited by 1,613 · see citing works
Storage of 7 +/- 2 short-term memories in oscillatory subcycles
Lisman, J. E., & Idiart, M. A. P. (1995) · Science · doi:10.1126/science.7878473 · Cited by 1,471 · see citing works
Abeles, M. (1991) · Cambridge University Press eBooks · doi:10.1017/cbo9780511574566 · Cited by 1,380 · see citing works
Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats
Ranck, J. B. (1973) · Experimental Neurology · doi:10.1016/0014-4886(73)90290-2 · Cited by 1,322 · see citing works
Principles of rhythmic motor pattern generation
Marder, E. E., & Calabrese, R. (1996) · Physiological Reviews · doi:10.1152/physrev.1996.76.3.687 · Cited by 1,287 · see citing works
High-frequency network oscillation in the hippocampus
Buzsáki, G., Horváth, Z., Urioste, R., Hetke, J. F., & Wise, K. D. (1992) · Science · doi:10.1126/science.1589772 · Cited by 1,223 · see citing works
Self-citationReplay of neuronal firing sequences in rat hippocampus during sleep following spatial experience
Skaggs, W. E., & McNaughton, B. L. (1996) · Science · doi:10.1126/science.271.5257.1870 · Cited by 1,173 · see citing works
Pattern recognition computation using action potential timing for stimulus representation
Hopfield, J. J. (1995) · Nature · doi:10.1038/376033a0 · Cited by 1,163 · see citing works
Dynamics of neuronal firing correlation: modulation of "effective connectivity"
Aertsen, A. M. H. J., Gerstein, G. L., Habib, M., & Palm, G. (1989) · Journal of Neurophysiology · doi:10.1152/jn.1989.61.5.900 · Cited by 1,073 · see citing works
The "Wake-Sleep" Algorithm for Unsupervised Neural Networks
Hinton, G. E., Dayan, P., Frey, B. J., & Neal, R. M. (1995) · Science · doi:10.1126/science.7761831 · Cited by 1,070 · see citing works
Coordinated interactions between hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep
Siapas, A. G., & Wilson, M. A. (1998) · Neuron · doi:10.1016/s0896-6273(00)80629-7 · Cited by 1,052 · see citing works
Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat
Csicsvari, J., Hirase, H., Czurkó, A., Mamiya, A., & Buzsáki, G. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-01-00274.1999 · Cited by 966 · see citing works
Self-citationDendritic spines as basic functional units of neuronal integration
Yuste, R., & Denk, W. (1995) · Nature · doi:10.1038/375682a0 · Cited by 950 · see citing works
Deciphering The Hippocampal Polyglot: the Hippocampus as a Path Integration System
McNaughton, B. L., Barnes, C. A., Gerrard, J. L., Gothard, K. M., Jung, M. W., Knierim, J. J., Kudrimoti, H. S., Qin, Y., Skaggs, W. E., Suster, M. S., et al. (1996) · Journal of Experimental Biology · doi:10.1242/jeb.199.1.173 · Cited by 900 · see citing works
Spike Synchronization and Rate Modulation Differentially Involved in Motor Cortical Function
Riehle, A., Grün, S., Diesmann, M., & Aertsen, A. (1997) · Science · doi:10.1126/science.278.5345.1950 · Cited by 895 · see citing works
Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks
Buzsáki, G., & Chrobak, J. J. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80012-3 · Cited by 878 · see citing works
Self-citationTs'o, D., Gilbert, C., & Wiesel, T. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-04-01160.1986 · Cited by 843 · see citing works
Kudrimoti, H. S., Barnes, C. A., & McNaughton, B. L. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-10-04090.1999 · Cited by 753 · see citing works
Zhang, K., Ginzburg, I., McNaughton, B. L., & Sejnowski, T. J. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.2.1017 · Cited by 741 · see citing works
Pavlides, C., & Winson, J. (1989) · The Journal of Neuroscience · doi:10.1523/jneurosci.09-08-02907.1989 · Cited by 684 · see citing works
Spatiotemporal firing patterns in the frontal cortex of behaving monkeys
Abeles, M., Bergman, H., Margalit, E., & Vaadia, E. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.70.4.1629 · Cited by 600 · see citing works
Chrobak, J. J., & Buzsáki, G. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-09-03056.1996 · Cited by 587 · see citing works
Self-citationBrown, E. N., Frank, L. M., Tang, D., Quirk, M. C., & Wilson, M. A. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-18-07411.1998 · Cited by 575 · see citing works
Experience-dependent, asymmetric expansion of hippocampal place fields
Mehta, M. R., Barnes, C. A., & McNaughton, B. L. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.16.8918 · Cited by 528 · see citing works
Paul, D. H. (1975) · Cited by 396 · see citing works
Temporal Representations of Odors in an Olfactory Network
Laurent, G., Wehr, M., & Davidowitz, H. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-12-03837.1996 · Cited by 373 · see citing works
Temporal Precision of Spike Trains in Extrastriate Cortex of the Behaving Macaque Monkey
Bair, W., & Christof Koch, A. (1996) · Neural Computation · doi:10.1162/neco.1996.8.6.1185 · Cited by 368 · see citing works
Chrobak, J. J., & Buzsáki, G. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-10-06160.1994 · Cited by 360 · see citing works
Self-citationDetecting spatiotemporal firing patterns among simultaneously recorded single neurons
Abeles, M., & Gerstein, G. L. (1988) · Journal of Neurophysiology · doi:10.1152/jn.1988.60.3.909 · Cited by 326 · see citing works
Sustained activation of hippocampal pyramidal cells by ‘space clamping’ in a running wheel
Czurkó, A., Hirase, H., Csicsvari, J. L., & Buzsáki, G. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00446.x · Cited by 326 · see citing works
Self-citationWallenstein, G. V., & Hasselmo, M. E. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.1.393 · Cited by 295 · see citing works
Bragin, A., Jandó, G., Nádasdy, Z., van Landeghem, M., & Buzsáki, G. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.73.4.1691 · Cited by 237 · see citing works
Self-citationIntrinsic membrane potential oscillations in hippocampal neurons in vitro
Leung, L.-W. S., & Yim, C. Y. (1991) · Brain Research · doi:10.1016/0006-8993(91)90834-i · Cited by 172 · see citing works
Buhl, E. H., Szil�gyi, T., Halasy, K., & Somogyi, P. (1996) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:3 · Cited by 138 · see citing works
Changes in neuronal transmission in the rat hippocampus during behavior
Buzsáki, G., Grastyán, E., Czopf, J., Kelle`nyi, L., & Prohaska, O. J. (1981) · Brain Research · doi:10.1016/0006-8993(81)90833-7 · Cited by 132 · see citing works
Self-citationHippocampal excitability phase-locked to the theta rhythm in walking rats
Rudell, A. P., Fox, S. E., & Ranck, J. B. (1980) · Experimental Neurology · doi:10.1016/0014-4886(80)90068-0 · Cited by 122 · see citing works
Favored patterns in spike trains. I. Detection
Dayhoff, J. E., & Gerstein, G. L. (1983) · Journal of Neurophysiology · doi:10.1152/jn.1983.49.6.1334 · Cited by 116 · see citing works
Strehler, B. L., & Lestienne, R. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.24.9812 · Cited by 92 · see citing works
Neuromodulatory control of hippocampal function: towards a model of Alzheimer’s disease
Menschik, E. D., & Finkel, L. H. (1998) · Artificial Intelligence in Medicine · doi:10.1016/s0933-3657(98)00006-2 · Cited by 84 · see citing works
A Neural Network for the Retrieval of Superimposed Connection Patterns
von der Malsburg, C., & Bienenstock, E. (1987) · Europhysics Letters (EPL) · doi:10.1209/0295-5075/3/11/015 · Cited by 76 · see citing works
Temporal Sequence Compression by an Integrate-and-Fire Model of Hippocampal Area CA3
August, D. A., & Levy, W. B. (1999) · Journal of Computational Neuroscience · doi:10.1023/a:1008861001091 · Cited by 59 · see citing works
Aertsen, A., Vaadia, E., Abeles, M., Ahissar, E., Bergman, H., Karmon, B., Lavner, Y., Margalit, E., Nelken, I., & Rotter, S. (1991) · PubMed · Cited by 45 · see citing works
"Replay" of Hippocampal "Memories"
Moore, G., Rosenberg, J. R., Hary, D., Breeze, P., Skaggs, W. E., & McNaughton, B. L. (1996) · Science · doi:10.1126/science.274.5290.1216 · Cited by 38 · see citing works
Recurring discharge patterns in multiple spike trains
Frostig, R. D., Frostig, Z., & Harper, R. M. (1990) · Biological Cybernetics · doi:10.1007/bf00205110 · Cited by 35 · see citing works
A neural network model of the cortico-hippocampal interplay and the representation of contexts
Bibbig, A., Wennekers, T., & Palm, G. (1995) · Behavioural Brain Research · doi:10.1016/0166-4328(94)00137-5 · Cited by 32 · see citing works
What makes the brain's tickers tock
Lisman, J. E. (1998) · Nature · doi:10.1038/28061 · Cited by 31 · see citing works
Recurring discharge patterns in multiple spike trains
Frostig, R. D., Frysinger, R. C., & Harper, R. M. (1990) · Biological Cybernetics · doi:10.1007/bf00205111 · Cited by 17 · see citing works
Temporal firing patterns of single units, pairs and triplets of units in the auditory cortex.
Vaadia, E., & Abeles, M. (1987) · PubMed · Cited by 10 · see citing works
"Replay" of Hippocampal "Memories"
Moore, G., Rosenberg, J. R., Hary, D., et al. (1996) · Science · doi:10.1126/science.274.5290.1216-a · Cited by 2 · see citing works
Episodic memory, semantic memory, and amnesia
Squire, L. R., & Zola, S. M. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1998)8:3
Self-citation
Flagged first, then by citations
1 of the 65 references couldn’t be matched to a known paper.
Research works printed but not linked: 2
- Abeles M (1991) Corticonics: neural circuits of the cerebral cortex. Cambridge, U.K.: Cambridge UP.
- Na ´dasdy Z, Csicsvari J, Penttonen M, Hetke J, Wise K , Buzsa ´ki G (1998) Extracellular recording and analysis of neuronal activity: from single cells to ensembles. In: Neuronal ensembles: strategies for recording and encoding (Eichenbaum H, Davis J, eds), pp 17-55. New York: Wiley.
Cited by
Sorted by citations
Diekelmann, S., & Born, J. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2762 · Cited by 3,760 · see citing works
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
Tononi, G., & Cirelli, C. (2014) · Neuron · doi:10.1016/j.neuron.2013.12.025 · Cited by 2,356 · see citing works
Sleep function and synaptic homeostasis
Tononi, G., & Cirelli, C. (2006) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2005.05.002 · Cited by 2,151 · see citing works
The functional role of cross-frequency coupling
Canolty, R. T., & Knight, R. T. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.09.001 · Cited by 2,101 · see citing works
Spike Timing–Dependent Plasticity: A Hebbian Learning Rule
Caporale, N., & Dan, Y. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.31.060407.125639 · Cited by 1,997 · see citing works
Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning
Buzsáki, G. (2015) · Hippocampus · doi:10.1002/hipo.22488 · Cited by 1,759 · see citing works
Self-citationLarge-scale recording of neuronal ensembles
Buzsáki, G. (2004) · Nature Neuroscience · doi:10.1038/nn1233 · Cited by 1,875 · see citing works
Self-citationCoordinated memory replay in the visual cortex and hippocampus during sleep
Ji, D., & Wilson, M. A. (2007) · Nature Neuroscience · doi:10.1038/nn1825 · Cited by 1,669 · see citing works
Eichenbaum (2004) · doi:10.1016/j.neuron.2004.08.028 · Cited by 1,464 · see citing works
Memory of sequential experience in the hippocampus during slow wave sleep
Lee, A. K., & Wilson, M. A. (2002) · Neuron · doi:10.1016/s0896-6273(02)01096-6 · Cited by 1,296 · see citing works
Neural syntax: cell assemblies, synapsembles, and readers
Buzsáki, G. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.023 · Cited by 1,289 · see citing works
Self-citationThe role of sleep in learning and memory
Maquet, P. (2001) · Science · doi:10.1126/science.1062856 · Cited by 1,177 · see citing works
Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep
Louie, K., & Wilson, M. A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00186-6 · Cited by 1,148 · see citing works
Harris, K. D., Henze, D. A., Csicsvari, J. L., Hirase, H., & Buzsáki, G. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.84.1.401 · Cited by 1,153 · see citing works
Self-citationNeural ensembles in CA3 transiently encode paths forward of the animal at a decision point
Johnson, A., & Redish, A. D. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3761-07.2007 · Cited by 1,003 · see citing works
Disruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the rat
Ego‐Stengel, V., & Wilson, M. A. (2010) · Hippocampus · doi:10.1002/hipo.20707 · Cited by 842 · see citing works
Hippocampal replay of extended experience
Davidson, T. J., Kloosterman, F., & Wilson, M. A. (2009) · Neuron · doi:10.1016/j.neuron.2009.07.027 · Cited by 806 · see citing works
“Replay events have consistently been found to co-occur with ripple oscillations in the hippocampal local field potential (Diba and Buzsáki, 2007; Foster and Wilson, 2006; Ji and Wilson, 2007; Lee and Wilson, 2002; Nádasdy et al., 1999).”
InfluentialLearning-dependent increases in sleep spindle density
Gais, S., Mölle, M., Helms, K., & Born, J. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06830.2002 · Cited by 859 · see citing works
Buzsáki, G. (2005) · Hippocampus · doi:10.1002/hipo.20113 · Cited by 872 · see citing works
Self-citationAwake replay of remote experiences in the hippocampus
Karlsson, M. P., & Frank, L. M. (2009) · Nature Neuroscience · doi:10.1038/nn.2344 · Cited by 769 · see citing works
“Complementary studies have shown that entire sequences can be replayed at high speeds14–16, 19.”
The cognitive neuroscience of sleep: neuronal systems, consciousness and learning
Hobson, J. A., & Pace-Schott, E. F. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn915 · Cited by 835 · see citing works
Replay of rule-learning related neural patterns in the prefrontal cortex during sleep
Peyrache, A., Khamassi, M., Benchenane, K., Wiener, S. I., & Battaglia, F. P. (2009) · Nature Neuroscience · doi:10.1038/nn.2337 · Cited by 767 · see citing works
Synfire Chains and Cortical Songs: Temporal Modules of Cortical Activity
Ikegaya, Y., Aaron, G., Cossart, R., Aronov, D., Lampl, I., Ferster, D., & Yuste, R. (2004) · Science · doi:10.1126/science.1093173 · Cited by 838 · see citing works
Hippocampal replay is not a simple function of experience
Gupta, A. S., van der Meer, M. A. A., Touretzky, D. S., & Redish, A. D. (2010) · Neuron · doi:10.1016/j.neuron.2010.01.034 · Cited by 733 · see citing works
Preplay of future place cell sequences by hippocampal cellular assemblies
Dragoi, G., & Tonegawa, S. (2011) · Nature · doi:10.1038/nature09633 · Cited by 716 · see citing works
Are spatial memories strengthened in the human hippocampus during slow wave sleep?
Peigneux, P., Laureys, S., Fuchs, S., Collette, F., Perrin, F., Reggers, J., Phillips, C., Degueldre, C., Del Fiore, G., Aerts, J., et al. (2004) · Neuron · doi:10.1016/j.neuron.2004.10.007 · Cited by 766 · see citing works
From the neuron doctrine to neural networks
Yuste, R. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn3962 · Cited by 748 · see citing works
Temporal Encoding of Place Sequences by Hippocampal Cell Assemblies
Dragoi, G., & Buzsáki, G. (2006) · Neuron · doi:10.1016/j.neuron.2006.02.023 · Cited by 727 · see citing works
Self-citationJosselyn, S. A., Köhler, S., & Frankland, P. W. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn4000 · Cited by 687 · see citing works
Neuromodulation of Brain States
Lee, S., & Dan, Y. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.012 · Cited by 666 · see citing works
The Restless Engram: Consolidations Never End
Dudai, Y. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150500 · Cited by 644 · see citing works
Rhythms of the hippocampal network
Colgin, L. L. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.21 · Cited by 654 · see citing works
Cirelli, C., & Tononi, G. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060216 · Cited by 646 · see citing works
Spontaneous Events Outline the Realm of Possible Sensory Responses in Neocortical Populations
Luczak, A., Barthó, P., & Harris, K. D. (2009) · Neuron · doi:10.1016/j.neuron.2009.03.014 · Cited by 593 · see citing works
NMDA receptors, place cells and hippocampal spatial memory
Nakazawa, K., McHugh, T. J., Wilson, M. A., & Tonegawa, S. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1385 · Cited by 619 · see citing works
Fogel, S. M., & Smith, C. T. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.12.003 · Cited by 628 · see citing works
Fast-Forward Playback of Recent Memory Sequences in Prefrontal Cortex During Sleep
Euston, D. R., Tatsuno, M., & McNaughton, B. L. (2007) · Science · doi:10.1126/science.1148979 · Cited by 586 · see citing works
Compartmentalized dendritic plasticity and input feature storage in neurons
Losonczy, A., Makara, J. K., & Magee, J. C. (2008) · Nature · doi:10.1038/nature06725 · Cited by 598 · see citing works
Beggs, J. M., & Plenz, D. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0540-04.2004 · Cited by 575 · see citing works
Enhanced Brain Correlations during Rest Are Related to Memory for Recent Experiences
Tambini, A., Ketz, N., & Davachi, L. (2010) · Neuron · doi:10.1016/j.neuron.2010.01.001 · Cited by 570 · see citing works
Buzsáki, G., & Watson, B. O. (2012) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2012.14.4/gbuzsaki · Cited by 579 · see citing works
Self-citationThe whats and whens of sleep-dependent memory consolidation
Diekelmann, S., Wilhelm, I., & Born, J. (2009) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2008.08.002 · Cited by 566 · see citing works
Takashima, A., Petersson, K. M., Rutters, F., Tendolkar, I., Jensen, O., Zwarts, M. J., McNaughton, B. L., & Fernández, G. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507774103 · Cited by 557 · see citing works
Transcranial direct current stimulation during sleep improves declarative memory
Marshall, L., Mölle, M., Hallschmid, M., & Born, J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.2725-04.2004 · Cited by 548 · see citing works
Space in the brain: How the hippocampal formation supports spatial cognition
Hartley, T., Lever, C., Burgess, N., & O'Keefe, J. (2014) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2012.0510 · Cited by 495 · see citing works
Space and Time: The Hippocampus as a Sequence Generator
Buzsáki, G., & Tingley, D. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.07.006 · Cited by 461 · see citing works
Self-citationEnsemble Patterns of Hippocampal CA3-CA1 Neurons during Sharp Wave–Associated Population Events
Csicsvari, J. L., Hirase, H., Mamiya, A., & Buzsáki, G. (2000) · Neuron · doi:10.1016/s0896-6273(00)00135-5 · Cited by 503 · see citing works
Self-citationMemory formation by neuronal synchronization
Axmacher, N., Mormann, F., Fernández, G., Elger, C. E., & Fell, J. (2006) · Brain Research Reviews · doi:10.1016/j.brainresrev.2006.01.007 · Cited by 480 · see citing works
Hippocampal-cortical interaction during periods of subcortical silence
Logothetis, N. K., Eschenko, O., Murayama, Y., Augath, M., Steudel, T., Evrard, H. C., Besserve, M., & Oeltermann, A. (2012) · Nature · doi:10.1038/nature11618 · Cited by 420 · see citing works
Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer
Jensen, O. B., & Lisman, J. E. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.12.001 · Cited by 467 · see citing works
(2013) · Elsevier eBooks · doi:10.1016/c2010-0-65035-8 · Cited by 465 · see citing works
Song replay during sleep and computational rules for sensorimotor vocal learning
Dave, A. S., & Margoliash, D. (2000) · Science · doi:10.1126/science.290.5492.812 · Cited by 458 · see citing works
Neural signatures of cell assembly organization
Harris, K. D. (2005) · Nature reviews. Neuroscience · doi:10.1038/nrn1669 · Cited by 443 · see citing works
Lisman, J. (2005) · Hippocampus · doi:10.1002/hipo.20121 · Cited by 435 · see citing works
The slow (<1 Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators
Crunelli, V., & Hughes, S. W. (2010) · Nature Neuroscience · doi:10.1038/nn.2445 · Cited by 435 · see citing works
A Neural Coding Scheme Formed by the Combined Function of Gamma and Theta Oscillations
Lisman, J. E., & Buzsáki, G. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn060 · Cited by 433 · see citing works
Self-citationFoster, D. J. (2017) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031538 · Cited by 375 · see citing works
Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans
Clemens, Z., Molle, M., Eross, L., Barsi, P., Halasz, P., & Born, J. (2007) · Brain · doi:10.1093/brain/awm146 · Cited by 398 · see citing works
Memory trace reactivation in hippocampal and neocortical neuronal ensembles
Sutherland, G. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00079-9 · Cited by 384 · see citing works
Beenhakker, M. P., & Huguenard, J. R. (2009) · Neuron · doi:10.1016/j.neuron.2009.05.015 · Cited by 374 · see citing works
Ellenbogen, J. M., Hulbert, J. C., Stickgold, R., Dinges, D. F., & Thompson-Schill, S. L. (2006) · Current Biology · doi:10.1016/j.cub.2006.05.024 · Cited by 377 · see citing works
Are corticothalamic ‘up’ states fragments of wakefulness?
Destexhe, A., Hughes, S. W., Rudolph, M., & Crunelli, V. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.04.006 · Cited by 355 · see citing works
Coordinated Reactivation of Distributed Memory Traces in Primate Neocortex
Hoffman, K. L., & McNaughton, B. L. (2002) · Science · doi:10.1126/science.1073538 · Cited by 420 · see citing works
Buzsáki, G. (2019) · doi:10.1093/oso/9780190905385.001.0001 · Cited by 358 · see citing works
Self-citationRecurrent network models of sequence generation and memory
Rajan, K., Harvey, C. D., & Tank, D. W. (2016) · Neuron · doi:10.1016/j.neuron.2016.02.009 · Cited by 351 · see citing works
Hippocampal ripples and memory consolidation
Girardeau, G., & Zugaro, M. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.02.005 · Cited by 330 · see citing works
Reactivation of experience-dependent cell assembly patterns in the hippocampus
O'Neill, J., Senior, T. J., Allen, K., Huxter, J. R., & Csicsvari, J. (2008) · Nature Neuroscience · doi:10.1038/nn2037 · Cited by 318 · see citing works
Self-citationLisman, J., Cooper, K., Sehgal, M., & Silva, A. J. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0076-6 · Cited by 351 · see citing works
Upgrading the sleeping brain with targeted memory reactivation
Oudiette, D., & Paller, K. A. (2013) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2013.01.006 · Cited by 350 · see citing works
Natural patterns of activity and long-term synaptic plasticity
Paulsen, O. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00076-3 · Cited by 347 · see citing works
Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation
Gais, S., & Born, J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0305404101 · Cited by 412 · see citing works
Maier, N., Nimmrich, V., & Draguhn, A. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.044602 · Cited by 340 · see citing works
The role of sleep in declarative memory consolidation: passive, permissive, active or none?
Ellenbogen, J. M., Payne, J. D., & Stickgold, R. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.10.006 · Cited by 326 · see citing works
Interictal epileptiform discharges induce hippocampal–cortical coupling in temporal lobe epilepsy
Gelinas, J. N., Khodagholy, D., Thesen, T., Devinsky, O., & Buzsáki, G. (2016) · Nature Medicine · doi:10.1038/nm.4084 · Cited by 329 · see citing works
Self-citationMölle, M., Eschenko, O., Gais, S., Sara, S. J., & Born, J. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06654.x · Cited by 322 · see citing works
Peigneux, P., Laureys, S., Fuchs, S., Destrebecqz, A., Collette, F., Delbeuck, X., Phillips, C. L. M., Aerts, J. J., Fiore, G. D., Degueldre, C., et al. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00278-7 · Cited by 309 · see citing works
Sequential replay of nonspatial task states in the human hippocampus
Schuck, N. W., & Niv, Y. (2019) · Science · doi:10.1126/science.aaw5181 · Cited by 304 · see citing works
State-Dependent Dendritic Computation in Hippocampal CA1 Pyramidal Neurons
Gasparini, S., & Magee, J. C. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4428-05.2006 · Cited by 298 · see citing works
Reverberation of recent visual experience in spontaneous cortical waves
Han, F., Caporale, N., & Dan, Y. (2008) · Neuron · doi:10.1016/j.neuron.2008.08.026 · Cited by 268 · see citing works
Schmidt, M. H. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.08.001 · Cited by 291 · see citing works
Sullivan, D. W., Csicsvari, J. L., Mizuseki, K., Montgomery, S. M., Diba, K., & Buzsáki, G. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0294-11.2011 · Cited by 292 · see citing works
Self-citationSustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning
Eschenko, O., Ramadan, W., Mölle, M., Born, J., & Sara, S. J. (2008) · Learning & Memory · doi:10.1101/lm.726008 · Cited by 277 · see citing works
Internally organized mechanisms of the head direction sense
Peyrache, A., Lacroix, M. M., Petersen, P. C., & Buzsáki, G. (2015) · Nature Neuroscience · doi:10.1038/nn.3968 · Cited by 274 · see citing works
Self-citationNew Experiences Enhance Coordinated Neural Activity in the Hippocampus
Cheng, S., & Frank, L. M. (2008) · Neuron · doi:10.1016/j.neuron.2007.11.035 · Cited by 286 · see citing works
Interaction between neocortical and hippocampal networks via slow oscillations
Sirota, A., & Buzsáki, G. (2005) · Thalamus and Related Systems · doi:10.1017/s1472928807000258 · Cited by 270 · see citing works
Self-citationO'Neill, J., Senior, T., & Csicsvari, J. (2006) · Neuron · doi:10.1016/j.neuron.2005.10.037 · Cited by 281 · see citing works
Self-citationWhat is the mammalian dentate gyrus good for?
Treves, A., Tashiro, A., Witter, M. P., & Moser, E. I. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.04.073 · Cited by 282 · see citing works
The relationships between memory systems and sleep stages
Rauchs, G., Desgranges, B., Foret, J., & Eustache, F. (2005) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2005.00450.x · Cited by 279 · see citing works
Mechanisms of Sharp Wave Initiation and Ripple Generation
Schlingloff, D., Káli, S., Freund, T. F., Hájos, N., & Gulyás, A. I. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0867-14.2014 · Cited by 281 · see citing works
Competing Roles of Slow Oscillations and Delta Waves in Memory Consolidation versus Forgetting
Kim, J., Gulati, T., & Ganguly, K. (2019) · Cell · doi:10.1016/j.cell.2019.08.040 · Cited by 254 · see citing works
Albouy, G., King, B. R., Maquet, P., & Doyon, J. (2013) · Hippocampus · doi:10.1002/hipo.22183 · Cited by 270 · see citing works
Ben-Yakov, A., & Dudai, Y. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0702-11.2011 · Cited by 238 · see citing works
Fiete, I., Senn, W., Wang, C. Z.-H., & Hahnloser, R. H. R. (2010) · Neuron · doi:10.1016/j.neuron.2010.02.003 · Cited by 269 · see citing works
Sleep for Preserving and Transforming Episodic Memory
Inostroza, M., & Jan Born, A. (2013) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062012-170429 · Cited by 265 · see citing works
Focal Synchronization of Ripples (80–200 Hz) in Neocortex and Their Neuronal Correlates
Grenier, F., Timofeev, I., & Steriade, M. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.4.1884 · Cited by 264 · see citing works
Offline Persistence of Memory-Related Cerebral Activity during Active Wakefulness
Peigneux, P., Orban, P., Balteau, E., Degueldre, C., Luxen, A., Laureys, S., & Maquet, P. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040100 · Cited by 263 · see citing works
Sharp wave ripples during learning stabilize the hippocampal spatial map
Roux, L., Hu, B., Eichler, R., Stark, E., & Buzsáki, G. (2017) · Nature Neuroscience · doi:10.1038/nn.4543 · Cited by 229 · see citing works
Self-citationComplementary learning systems
O’Reilly, R. C., Bhattacharyya, R., Howard, M. D., & Ketz, N. (2014) · Cognitive Science · doi:10.1111/j.1551-6709.2011.01214.x · Cited by 259 · see citing works
Dreaming of a learning task is associated with enhanced sleep-dependent memory consolidation
Wamsley, E. J., Tucker, M., Payne, J. D., Benavides, J. A., & Stickgold, R. (2010) · Current Biology · doi:10.1016/j.cub.2010.03.027 · Cited by 255 · see citing works
- Authors
- Nádasdy, Z., Hirase, H., Czurkó, A., Csicsvari, J., & Buzsáki, G.
- Affiliations
- Rutgers, The State University of New Jersey (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1999-11-01
- Volume
- 19
- Issue
- 21
- Pages
- 9497-9507
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6782894
- OpenAlex
- W1580901834
- Cited by
- 932
- References
- 65
- Citations by year
- 2026: 25 · 2025: 46 · 2024: 46 · 2023: 44 · 2022: 36 · 2021: 34 · 2020: 43 · 2019: 53 · 2018: 36 · 2017: 46 · 2016: 38 · 2015: 40 · 2014: 51 · 2013: 39 · 2012: 29
- FWCI
- 7.04
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (R01MH054671, MH54671)
- National Institute of Neurological Disorders and Stroke (R01NS034994, NS-34994)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Keywords
- replay, slow-wave sleep, pyramidal neurons, template matching, memory consolidation, spatial navigation
- MeSH terms
- Animals, Brain Mapping, Evoked Potentials, Hippocampus, Models, Neurological, Monte Carlo Method, Motor Activity, Nerve Net, Neurons, Probability, Sleep, Time Factors, Wakefulness, Rats, Sprague-Dawley, Pyramidal Cells, 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