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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.
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“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]
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“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]
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Background
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Electrical synapses in mammalian CNS: Past eras, present focus and future directions
Nagy, J. I., Pereda, A. E., & Rash, J. E. (2017) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2017.05.019 · Cited by 112
Laminar organization of encoding and memory reactivation in the parietal cortex
Wilber, A. A., Skelin, I., Wu, W., & McNaughton, B. L. (2017) · Neuron · doi:10.1016/j.neuron.2017.08.033 · Cited by 95
Novitskaya, Y., Sara, S. J., Logothetis, N. K., & Eschenko, O. (2016) · Learning & Memory · doi:10.1101/lm.040923.115 · Cited by 116
“…of increased cellular excitability (Buzsaki 1985), they are indicative of replay of experience-activated neuronal sequences (Kudrimoti et al. 1999; Nadasdy et al. 1999) and their occurrence during slow wave sleep (SWS) is temporally locked to periods of enhanced cortical excitability, or…”
BackgroundInfluentialTrettel, S. G., Trimper, J. B., Hwaun, E., Fiete, I. R., & Colgin, L. L. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0359-6 · Cited by 108
The balance of forward and backward hippocampal sequences shifts across behavioral states
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“Each recording session began by recording 10–15 min of neural data as subjects rested on a platform placed in the center of the track.”
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Replay in Deep Learning: Current Approaches and Missing Biological Elements
Hayes, T. L., Krishnan, G. P., Bazhenov, M., Siegelmann, H. T., Sejnowski, T. J., & Kanan, C. (2021) · Neural Computation · doi:10.1162/neco_a_01433 · Cited by 106
“Furthermore, many existing artificial replay implementations do not purge their memory buffer, which is not consistent with biology (Nádasdy et al., 1999; Karlsson & Frank, 2009) and do not have a notion of waking (streaming/online) learning.”
Consolidation of Long-Term Memory: Evidence and Alternatives.
Meeter, M., & Murre, J. M. J. (2004) · Psychological Bulletin · doi:10.1037/0033-2909.130.6.843 · Cited by 148
“Moreover, several studies have shown that hippocampal neurons active during daytime tasks are reactivated in slow-wave sleep (Nadasdy et al., 1999; Pavlides and Winson, 1989; Skaggs and McNaughton, 1996; Sutherland and McNaughton, 2000; Wilson and McNaughton, 1994).”
BackgroundNeural representations during sleep: From sensory processing to memory traces
Hennevin, E., Huetz, C., & Edeline, J.-M. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.10.006 · Cited by 133
Differential responses of hippocampal subfields to cortical up–down states
Hahn, T. T. G., Sakmann, B. J., & Mehta, M. R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700222104 · Cited by 109
Coordinated Interaction between Hippocampal Sharp-Wave Ripples and Anterior Cingulate Unit Activity
Wang, D. V., & Ikemoto, S. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1042-16.2016 · Cited by 108
“…states have also been reported within the hippocampus: while sleep ripples are associated with memory reactivation (Wilson and McNaughton, 1994; Nádasdy et al., 1999; Lee and Wilson, 2002), awake ripples may support cognitive functions, such as behavioral planning, likely by influencing…”
BackgroundResultModels, structure, function: the transformation of cortical signals in the dentate gyrus
Acsády, L., & Káli, S. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)63031-3 · Cited by 110
Extending the effects of spike-timing-dependent plasticity to behavioral timescales
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Wirt, R. A., & Hyman, J. M. (2017) · Brain Sciences · doi:10.3390/brainsci7040043 · Cited by 109
Hippocampo-cortical circuits for selective memory encoding, routing, and replay
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Michelmann, S., Bowman, H., & Hanslmayr, S. (2016) · PLoS Biology · doi:10.1371/journal.pbio.1002528 · Cited by 104
Cellular and neurochemical basis of sleep stages in the thalamocortical network
Krishnan, G. P., Chauvette, S., Shamie, I., Soltani, S., Timofeev, I., Cash, S. S., Halgren, E., & Bazhenov, M. (2016) · eLife · doi:10.7554/elife.18607 · Cited by 125
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“Hippocampal place cells are reactivated in a compressed time frame during SWRs in a manner that recapitulates spatial experience (Nádasdy et al. 1999; Lee & Wilson, 2002; Davidson et al. 2009; Karlsson & Frank, 2009).”
BackgroundInfluentialDetecting precise firing sequences in experimental data
Abeles, M., & Gat, I. (2001) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(01)00364-8 · Cited by 99
Coordinated emergence of hippocampal replay and theta sequences during post-natal development
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Impaired neural replay of inferred relationships in schizophrenia
Nour, M. M., Liu, Y., Arumuham, A., Kurth-Nelson, Z. L., & Dolan, R. J. (2021) · Cell · doi:10.1016/j.cell.2021.06.012 · Cited by 101
“During subsequent rest periods a rapid sequential place cell reactivation (replay) recapitulates previously navigated trajectories, in addition to exploring novel paths that go beyond previous experience (Diba and Buzsáki, 2007; Foster, 2017; Foster and Wilson, 2006; Ólafsdóttir et al., 2015; Gupta et al., 2010; Lee a…”
What is episodic memory if it is a natural kind?
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“active at an earlier time in the online state (Nádasdy et al. 1999; Lee andWilson 2002).”
BackgroundLearning multiple variable-speed sequences in striatum via cortical tutoring
Murray, J. M., & Escola, G. S. (2017) · eLife · doi:10.7554/elife.26084 · Cited by 102
Decoding cognition from spontaneous neural activity
Liu, Y., Nour, M. M., Schuck, N. W., Behrens, T. E. J., & Dolan, R. J. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00570-z · Cited by 107
Sleep and rest facilitate auditory learning
Gottselig, J. M., Hofer-Tinguely, G., Borbély, A. A., Regel, S. J., Landolt, H., Rétey, J., & Achermann, P. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.05.053 · Cited by 103
Sequence Reactivation in the Hippocampus Is Impaired in Aged Rats
Gerrard, J. L., Burke, S. N., McNaughton, B. L., & Barnes, C. A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1265-08.2008 · Cited by 97
“Among these is the well documented observation that activity pattern reactivation (Kudrimoti et la., 1999; Gerrard et al., 2001) and sequence reactivation (Nadasdy et al., 1999; Lee and Wilson, 2002) in the hippocampus are concentrated during sharp wave/ripple events.”
BackgroundMethodSleep-Dependent Plasticity Requires Cortical Activity
Jha, S. K., Jones, B. E., Coleman, T., Steinmetz, N., Law, C.-T., Griffin, G., Hawk, J., Dabbish, N., Kalatsky, V. A., & Frank, M. G. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2722-05.2005 · Cited by 96
“Similar reactivation on the level of single neurons and neuronal ensembles has been observed during sleep in nonhuman vertebrates, suggesting that information acquired during wake is reprocessed in subsequent sleep (Wilson and McNaughton, 1994; Nadasky et al., 1999; Louie and Wilson, 2001; Hoffman and McNaughton, 2002…”
BackgroundSelection of preconfigured cell assemblies for representation of novel spatial experiences
Dragoi, G., & Tonegawa, S. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0522 · Cited by 95
Rigid firing sequences undermine spatial memory codes in a neurodegenerative mouse model
Cheng, J., & Ji, D. (2013) · eLife · doi:10.7554/elife.00647 · Cited by 95
“consolidation with or without partial external input (Buzsaki, 1989; Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Nadasdy et al., 1999; Lee and Wilson, 2002; Foster and Wilson, 2006; Diba and Buzsaki, 2007; Ji and Wilson, 2007; Gelbard-Sagiv et al., 2008; Davidson et al., 2009; Karlsson and Frank, 2009; C…”
BackgroundReplay and compositional computation
Kurth-Nelson, Z. L., Behrens, T. E. J., Wayne, G., Miller, K. J., Luettgau, L., Dolan, R. J., Liu, Y., & Schwartenbeck, P. (2023) · Neuron · doi:10.1016/j.neuron.2022.12.028 · Cited by 100
Episodic memory retrieval success is associated with rapid replay of episode content
Wimmer, G. E., Liu, Y., Vehar, N., Behrens, T. E. J., & Dolan, R. J. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0649-z · Cited by 100
Learning-Induced Plasticity Regulates Hippocampal Sharp Wave-Ripple Drive
Girardeau, G., Cei, A., & Zugaro, M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4288-13.2014 · Cited by 97
“These sequences are later replayed at accelerated rates during SPW-Rs (Skaggs et al., 1996; Nádasdy et al., 1999; Lee and Wilson, 2002; Davidson et al., 2009).”
BackgroundSchapiro, A. C., Reid, A. G., Morgan, A., Manoach, D. S., Verfaellie, M., & Stickgold, R. (2019) · Hippocampus · doi:10.1002/hipo.23101 · Cited by 94
Reyes‐Puerta, V., Sun, J., Kim, S., Kilb, W., & Luhmann, H. J. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhu007 · Cited by 95
“In brief, repetitive spike sequences were detected in spike datasets by the use of a template-matching algorithm (Abeles and Gerstein 1988; Nadasdy et al. 1999; Rolston et al. 2007).”
BackgroundMethodHippocampal replay of experience at real-world speeds
Denovellis, E. L., Gillespie, A. K., Coulter, M. E., Sosa, M., Chung, J. E., Eden, U. T., & Frank, L. M. (2021) · eLife · doi:10.7554/elife.64505 · Cited by 89
“Importantly, previous work has reported that these sequential firing events proceed at an average speed of ~10 meters per second, about 20x faster than the animal’s usual movement speed (10, 25, 30, 36).”
BackgroundResultA Unified Dynamic Model for Learning, Replay, and Sharp-Wave/Ripples
Jahnke, S., Timme, M., & Memmesheimer, R.-M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3977-14.2015 · Cited by 90
“The sequences of activity are replayed in a further compressed manner, while the animal rests and sleeps (Wilson and McNaughton, 1994; Nadasdy et al., 1999; Lee and Wilson, 2002; Pastalkova et al., 2008; Davidson et al., 2009).”
BackgroundResultInfluentialJohnson, A. C., & Redish, A. D. (2005) · Neural Networks · doi:10.1016/j.neunet.2005.08.009 · Cited by 92
“Hippocampal replay has been examined on simple runway tasks (Lee & Wilson, 2002; Louie & Wilson, 2001; Nádasdy et al., 1999; Skaggs et al., 1996; Wilson & McNaughton, 1994).”
InfluentialWatson, B. O., & Buzsáki, G. (2015) · Daedalus · doi:10.1162/daed_a_00318 · Cited by 99
Self-citationSpontaneous cognitive processes and the behavioral validation of time-varying brain connectivity
Kucyi, A., Tambini, A., Sadaghiani, S., Keilholz, S. D., & Cohen, J. R. (2018) · Network Neuroscience · doi:10.1162/netn_a_00037 · Cited by 95
Circadian rhythms and memory: not so simple as cogs and gears
Eckel‐Mahan, K. L., & Storm, D. R. (2009) · EMBO Reports · doi:10.1038/embor.2009.123 · Cited by 99
Wamsley, E. J., Tucker, M. A., Payne, J. D., & Stickgold, R. (2010) · Learning & Memory · doi:10.1101/lm.1828310 · Cited by 89
“…largely from electrophysiological studies in rodents, demonstrating that patterns of hippocampal place cell activity first seen during waking exploration are later reexpressed during post-learning sleep (Wilson and McNaughton 1994; Kudrimoti et al. 1999; Nadasdy et al. 1999; Ji and Wilson 2007).”
BackgroundLearning and sleep: the sequential hypothesis
Ambrosini, M. V., & Giuditta, A. (2001) · Sleep Medicine Reviews · doi:10.1053/smrv.2001.0180 · Cited by 108
Cross-species neuroscience: closing the explanatory gap
Barron, H. C., Mars, R. B., Dupret, D., Lerch, J. P., & Sampaio‐Baptista, C. (2020) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0633 · Cited by 89
Comparison of Sleep Spindles and Theta Oscillations in the Hippocampus
Sullivan, D. W., Mizuseki, K., Sorgi, A., & Buzsáki, G. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0552-13.2014 · Cited by 99
“The lack of orderly firing during spindles is in contrast with the striking sequential firing of neurons during sharp wave ripples (Wilson and McNaughton, 1994; Nadasdy et al., 1999).”
ResultSelf-citationThe hippocampal debate: are we asking the right questions?
Redish, A. D. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00356-4 · Cited by 87
“There is now strong evidence that hippocampal representations active during awake states are replayed during subsequent sleep states [94,139,161,206,241].”
BackgroundCaccavano, A., Bozzelli, P. L., Forcelli, P. A., Pak, D. T. S., Wu, J., Conant, K. E., & Vicini, S. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0425-20.2020 · Cited by 94
Self‐organization of repetitive spike patterns in developing neuronal networks in vitro
Sun, J., Kilb, W., & Luhmann, H. J. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07383.x · Cited by 88
“Repetitive spike patterns were detected in spike datasets by the use of a template-matching algorithm (Abeles &Gerstein, 1988; Nadasdy et al., 1999; Rolston et al., 2007; Schrader et al., 2008) implemented in a matlab environment.”
BackgroundMethodUsing Matrix and Tensor Factorizations for the Single-Trial Analysis of Population Spike Trains
Onken, A., Liu, J. K., Karunasekara, P. P. C. R., Delis, I., Gollisch, T., & Panzeri, S. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1005189 · Cited by 84
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The Challenge of Understanding the Brain: Where We Stand in 2015
Lisman, J. E. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.032 · Cited by 92
Hippocampal coupling with cortical and subcortical structures in the context of memory consolidation
Skelin, I., Kilianski, S., & McNaughton, B. L. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.04.004 · Cited by 83
“, 2015), as well as time-compressed (4–10×) reactivations of neuronal activity patterns present during behavior (Wilson & McNaughton, 1994; Skaggs & McNaughton, 1996; Nádasdy et al., 1999; Euston, Tatsuno, & McNaughton, 2007).”
BackgroundSleep-Related Neural Activity in a Premotor and a Basal-Ganglia Pathway of the Songbird
Hahnloser, R. H. R., Kozhevnikov, A. A., & Fee, M. S. (2006) · Journal of Neurophysiology · doi:10.1152/jn.01064.2005 · Cited by 83
“It is currently unclear how this finding fits into theories of memory consolidation during slow-wave sleep, where usually a dramatic difference between circuit dynamics during behavior and sleep is observed (Nadasdy et al. 1999).”
Ferraris, M., Cassel, J., de Vasconcelos, A. P., Stéphan, A., & Quilichini, P. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.02.025 · Cited by 92
“More importantly, neuronal patterns activated during learning are replayed during sleep SPW-Rs (Buzsáki, 2015; Lee and Wilson, 2002; Nadasdy et al., 1999).”
BackgroundOrder-Based Representation in Random Networks of Cortical Neurons
Shahaf, G., Eytan, D., Gal, A., Kermany, E., Lyakhov, V., Zrenner, C., & Marom, S. (2008) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000228 · Cited by 82
“, [8,11,26,31,39–42]), the general applicability of”
Age-related changes in sleep and memory: commonalities and interrelationships
Hornung, O. P., Danker‐Hopfe, H., & Heuser, I. (2005) · Experimental Gerontology · doi:10.1016/j.exger.2005.02.001 · Cited by 86
Temporally Precise Cortical Firing Patterns Are Associated With Distinct Action Segments
Shmiel, T., Drori, R., Shmiel, O., Ben‐Shaul, Y., Nádasdy, Z., Shemesh, M., Teicher, M., & Abeles, M. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00798.2005 · Cited by 81
“…Landolt et al. 1985; Legendy and Salcman 1985; Lestienne et al. 1987, 1996, 1999; Nadasdy et al. 1999; Prut et al. 1998; Riehle et al. 1997; Tetko and Villa 2001; Villa and Fuster 1992; Villa et al. 1990, 1999), the statistical validity of these findings has been challenged (Oram et al. 1999).”
Self-citationRipples Make Waves: Binding Structured Activity and Plasticity in Hippocampal Networks
Sadowski, J. H. L. P., Jones, M. W., & Mellor, J. R. (2011) · Neural Plasticity · doi:10.1155/2011/960389 · Cited by 84
“[61] Place cell replay SWS Low SWRs Wheel running”
BackgroundImagination as a fundamental function of the hippocampus
Comrie, A. E., Frank, L. M., & Kay, K. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0336 · Cited by 91
“These replays occur on the order of tens to hundreds of milliseconds, far faster than the seconds-long timescale over which the actual behavioural traversal of those locations unfolds (figure 1b) [71].”
BackgroundThe impact of overnight consolidation upon memory for emotional and neutral encoding contexts
Lewis, P. A., Cairney, S., Manning, L., & Critchley, H. D. (2011) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2011.05.009 · Cited by 79
The Neural Representation of Prospective Choice during Spatial Planning and Decisions
Kaplan, R., King, J. A., Koster, R., Penny, W. D., Burgess, N., & Friston, K. J. (2017) · PLoS Biology · doi:10.1371/journal.pbio.1002588 · Cited by 81
All My Circuits: Using Multiple Electrodes to Understand Functioning Neural Networks
Miller, E. K., & Wilson, M. A. (2008) · Neuron · doi:10.1016/j.neuron.2008.10.033 · Cited by 76
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Zheng, C., Bieri, K. W., Trettel, S. G., & Colgin, L. L. (2015) · Hippocampus · doi:10.1002/hipo.22415 · Cited by 79
“…slow gamma power is heightened during sharp wave-ripples (Carr et al., 2012; Bieri et al., 2014), a state during which the hippocampal network reactivates representations of previously experienced locations rather than representing current position (Kudrimoti et al., 1999; Nadasdy et al., 1999).”
BackgroundHeading direction with respect to a reference point modulates place-cell activity
Jercog, P. E., Ahmadian, Y., Woodruff, C. M., Deb-Sen, R., Abbott, L. F., & Kandel, E. R. (2019) · Nature Communications · doi:10.1038/s41467-019-10139-7 · Cited by 72
Tatsuno, M., Lipa, P., & McNaughton, B. L. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3317-06.2006 · Cited by 86
“…role in the consolidation process of certain types of memory (Pavlides and Winson, 1989; Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Nadasdy et al., 1999; Dave and Margoliash, 2000; Louie and Wilson, 2001; Hoffman and McNaughton, 2002; Lee and Wilson, 2002; Ribeiro et al., 2004).”
BackgroundSensorimotor Cognition and Natural Language Syntax
Knott, A. (2012) · The MIT Press eBooks · doi:10.7551/mitpress/8938.001.0001 · Cited by 76
Electrophysiological signatures of memory reactivation in humans
Schreiner, T., & Staudigl, T. (2020) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0293 · Cited by 87
Emergence of Cognition from ActionPreprint
Buzsáki, G., Peyrache, A., & Kubie, J. L. (2014) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2014.79.024679 · Cited by 86
“…sleep “replay” experiments in both rodents and humans show that sleep patterns are far from random but, instead, are reminiscent of waking when the neuronal trajectories evolve under the influence of sensory inputs (Wilson and McNaughton 1994; Nádasdy et al. 1999; cf. Diekelmann and Born 2010).”
BackgroundSelf-citationContribution of hippocampal region CA3 to consciousness and schizophrenic hallucinations
Behrendt, R. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.12.009 · Cited by 75
“wave-ripple complexes (sharp-wave bursts) (Nádasdy et al., 1999; Lee and Wilson, 2002).”
A Rate and History-Preserving Resampling Algorithm for Neural Spike Trains
Harrison, M. T., & Geman, S. (2008) · Neural Computation · doi:10.1162/neco.2008.03-08-730 · Cited by 75
“…such as synchronous spikes or other forms of repeated spike-time patterns in the recorded data (cf. Date et al., 1998; Oram et al., 1999; Nádasdy et al., 1999; Baker & Lemon, 2000; Gerstein, 2004; Ikegaya et al., 2004; Amarasingham, 2004; Harrison, 2005; Shmiel et al., 2005; Shmiel et…”
Identification of Parvalbumin Interneurons as Cellular Substrate of Fear Memory Persistence
Çalışkan, G., Müller, I., Semtner, M., Winkelmann, A., Raza, A. S., Hollnagel, J., Rösler, A., Heinemann, U., Stork, O., & Meier, J. C. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw001 · Cited by 73
“during sharp wave-ripple complexes (SPW-Rs) (Buzsaki et al. 1992; Wilson and McNaughton 1994; Nadasdy et al. 1999).”
BackgroundBRIDGING THE GAP BETWEEN BRAIN AND BEHAVIOR: COGNITIVE AND NEURAL MECHANISMS OF EPISODIC MEMORY
Eichenbaum, H., & Fortin, N. J. (2005) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.2005.80-04 · Cited by 80
Sleep smart—optimizing sleep for declarative learning and memory
Feld, G. B., & Diekelmann, S. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.00622 · Cited by 87
Molecular signatures and mechanisms of long-lasting memory consolidation and storage
Katche, C., Cammarota, M., & Medina, J. H. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.06.018 · Cited by 79
Memory processes during sleep: beyond the standard consolidation theory
Axmacher, N., Draguhn, A., Elger, C. E., & Fell, J. (2009) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-0019-1 · Cited by 80
“Even sequences of three spikes fired by three different place cells during wheel-running are repeated in subsequent slow wave sleep [68], and information about the order in which the cells”
Temporal structure in associative retrieval
Kurth-Nelson, Z. L., Barnes, G. R., Sejdinović, D., Dolan, R. J., & Dayan, P. (2015) · eLife · doi:10.7554/elife.04919 · Cited by 77
“…et al., 2012; Morton et al., 2013), mental time travel (Hopfield, 2010; Schacter et al., 2012), memory maintenance and consolidation (Marr, 1971; Nádasdy et al., 1999; Káli and Dayan, 2004; Kuhl et al., 2012; Deuker et al., 2013) as well as temporal expectation (Sakai and Miyashita, 1991;…”
BackgroundMetastable attractors explain the variable timing of stable behavioral action sequences
Recanatesi, S., Pereira, U., Murakami, M., Mainen, Z. F., & Mazzucato, L. (2021) · Neuron · doi:10.1016/j.neuron.2021.10.011 · Cited by 76
Tao, K., Chung, M., Watarai, A., Huang, Z., Wang, M., & Okuyama, T. (2022) · Molecular Psychiatry · doi:10.1038/s41380-021-01430-5 · Cited by 74
Age-related Changes in the Sleep-dependent Reorganization of Declarative Memories
Baran, B., Mantua, J., & Spencer, R. M. C. (2016) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00938 · Cited by 72
Reward biases spontaneous neural reactivation during sleep
Sterpenich, V., van Schie, M. K. M., Catsiyannis, M., Ramyead, A., Perrig, S., Yang, H.-D., Van De Ville, D., & Schwartz, S. (2021) · Nature Communications · doi:10.1038/s41467-021-24357-5 · Cited by 71
Sleep in the Human Hippocampus: A Stereo-EEG Study
Moroni, F., Nobili, L., Curcio, G., Carli, F. D., Fratello, F., Marzano, C., Gennaro, L. D., Ferrillo, F., Cossu, M., Francione, S., et al. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000867 · Cited by 76
“For example, high order replay of waking activity has been observed in the hippocampus during both SWS and REM sleep [3–5].”
MethodEcker, A., Bagi, B., Vértes, E., Steinbach-Németh, O., Karlócai, M. R., Papp, O. I., Miklós, I., Hájos, N., Freund, T. F., Gulyás, A. I., et al. (2022) · eLife · doi:10.7554/elife.71850 · Cited by 73
Synchronous neural activity in scale-free network models versus random network models
Grinstein, G., & Linsker, R. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504127102 · Cited by 69
Sakurai, Y. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00509-2 · Cited by 73
Looking for cognition in the structure within the noise
Johnson, A. C., Fenton, A. A., Kentros, C. G., & Redish, A. D. (2009) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2008.11.005 · Cited by 67
Hippocampal place cell sequences differ during correct and error trials in a spatial memory task
Zheng, C., Hwaun, E., Loza, C. A., & Colgin, L. L. (2021) · Nature Communications · doi:10.1038/s41467-021-23765-x · Cited by 73
Habibollahi, F., Kagan, B. J., Burkitt, A. N., & French, C. R. (2023) · Nature Communications · doi:10.1038/s41467-023-41020-3 · Cited by 68
“Moreover, while numerous studies have observed critical dynamicsfrom spontaneous activity in vivo 8 – 13 , the neural regions measured are not isolated from external input, including input from other unmeasured neural regions, even when anesthetized.”
Heterosynaptic plasticity in the neocortex
Chistiakova, M., & Volgushev, M. (2009) · Experimental Brain Research · doi:10.1007/s00221-009-1859-5 · Cited by 69
Olfactory Cortex Generates Synchronized Top-Down Inputs to the Olfactory Bulb during Slow-Wave Sleep
Manabe, H., Kusumoto‐Yoshida, I., Ota, M., & Mori, K. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6578-10.2011 · Cited by 72
“During the slow-wave sleep state, a subset of hippocampal CA1 pyramidal cells repeatedly participates in hippocampal SPWs, whereas others rarely participate (Nadasdy et al., 1999).”
BackgroundElectrophysiological recordings from behaving animals—going beyond spikes
Chorev, E., Epsztein, J., Houweling, A. R., Lee, A. K., & Brecht, M. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.08.005 · Cited by 69
“The use of multiple electrodes led to the discovery of offline replay of spatial trajectories firing patterns [5,6].”
Deciphering Neural Codes of Memory during Sleep
Chen, Z. S., & Wilson, M. A. (2017) · Trends in Neurosciences · doi:10.1016/j.tins.2017.03.005 · Cited by 65
“The reactivated patterns during SWRs closely resembled the compressed structure of encoded memory observed within individual cycles of the theta rhythm during awake behavior in the hippocampus [12,50].”
BackgroundInfluentialChao, Z. C., Bakkum, D. J., & Potter, S. M. (2007) · Journal of Neural Engineering · doi:10.1088/1741-2560/4/3/015 · Cited by 65
“Spike sequences, imposed upon the network by behavioral manipulations, recur spontaneously during subsequent sleep episodes (Nádasdy et al 1999, Nádasdy 2000, Lee and Wilson 2002).”
The evolving view of replay and its functions in wake and sleep
Findlay, G., Tononi, G., & Cirelli, C. (2020) · SLEEP Advances · doi:10.1093/sleepadvances/zpab002 · Cited by 66
“Early studies found that the strength of reactivations declined rapidly during the first post-task hour [12, 13], and the same trend has been reported for post-task sequence replay [14, 19, 26].”
BackgroundRibeiro, S. T. G. (2011) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-011-1031-5 · Cited by 65
“Furthermore, several electrophysiological and imaging studies provide comprehensive support and mechanistic basis for the notion that sleep promotes cognitive processing [22, 37, 53, 54, 59, 61, 67, 71, 80, 82, 83, 88, 90, 98, 99, 104, 109, 117, 148].”
BackgroundNeurons of the cerebral cortex exhibit precise interspike timing in correspondence to behavior
Shmiel, T., Drori, R., Shmiel, O., Ben‐Shaul, Y., Nádasdy, Z., Shemesh, M., Teicher, M., & Abeles, M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509346102 · Cited by 64
Self-citationPropagation of specific network patterns through the mouse hippocampus
Both, M., Bähner, F., Halbach, O. V. B. U., & Draguhn, A. (2008) · Hippocampus · doi:10.1002/hipo.20446 · Cited by 64
“spatial/declarative memory by transferring this information to neocortical areas (Buzsaki, 1989, 1998; Nadasdy et al., 1999; Battaglia et al., 2004; Ji and Wilson, 2007).”
BackgroundDynamic modulation of theta–gamma coupling during rapid eye movement sleep
Bandarabadi, M., Boyce, R., Herrera, C. G., Bassetti, C. L., Williams, S., Schindler, K. A., & Adamantidis, A. (2019) · SLEEP · doi:10.1093/sleep/zsz182 · Cited by 75
“Classically, the reactivation of hippocampal place cells during NREM sleep provides one possible mechanism for the long-term encoding of newly acquired spatial [1, 8] but also procedural and emotional information [9–11].”
BackgroundFear conditioning increases NREM sleep.
Hellman, K., & Abel, T. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.2.310 · Cited by 62
“…2002) Exploration of a new context produces significant alterations in gene expression within the hippocampus (Guzowski, McNaugh ton, Barnes, & Worley, 1999) and results in neural activity patterns resembling prior exploration during NREM (Nadasdy et al., 1999) and REM sleep (Louie & Wilson, 2001).”
BackgroundSynaptic plasticity by antidromic firing during hippocampal network oscillations
Bukalo, O., Campanac, E., Hoffman, D. A., & Fields, R. D. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210735110 · Cited by 68
“SPW-Rs coincide with periods of offline replay of neural sequences learned during encoding sensory information (7, 8).”
BackgroundSynaptic Homeostasis and Restructuring across the Sleep-Wake Cycle
Blanco, W., Pereira, C. M., Cota, V. R., Souza, A. C., Rennó‐Costa, C., Santos, S., Dias, G., Guerreiro, A. M. G., Tort, A. B. L., Neto, A. D., et al. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004241 · Cited by 63
Metadata
- 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
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