Hippocampal sharp wave bursts coincide with neocortical “up-state” transitions
Open accessAbstract
The sleeping neocortex shows nested oscillatory activity in different frequency ranges, characterized by fluctuations between “up-states” and “down-states.” High-density neuronal ensemble recordings in rats now reveal the interaction between synchronized activity in the hippocampus and neocortex: Electroencephalographic sharp waves in the hippocampus were more probable during down-states than during up-states, and tended to coincide with transitions from down-states to up-states. The form of cortical activity fluctuations and their interactions with sharp waves depend on sleep depth: In deeper sleep stages, characterized by strong neocortical oscillation in the delta range or slower (∼0.8-4 Hz), sharp-wave-triggered peri-event time histograms (PETH) are consistent with a longer duration for down-states than for up-states. In lighter sleep, the sharp-wave-triggered PETH suggested longer up-states than down-states. These results highlight the interplay in the hippocampal/neocortical loop: Decreased neocortical input during down-states may be a factor in generation of sharp waves. In turn, sharp waves may facilitate down-to-up transitions. This interplay may reflect joint memory trace reactivation in the hippocampus and in the neocortex, possibly contributing to consolidation of long-term memory: Off-line reactivation of recent neural activity patterns in the hippocampus occurs during 50-100-msec electroencephalographic sharp waves, corresponding to pyramidal-cell population bursts. The neocortical up-states starting in correspondence with sharp waves may be influenced by the reactivated information carried by the hippocampal sharp wave.
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?
Generation of spindles in the thalamus and generation of SW-Rs in the hippocampus are distinctly suppressed during the down-phase of the slow oscillation, followed by a rebound in spindle and SW-R activity during the succeeding depolarizing up-state.
“Generation of spindles in the thalamus and generation of SW-Rs in the hippocampus are distinctly suppressed during the down-phase of the slow oscillation, and this is followed by a rebound in spindle and SW-R activity during the succeeding depolarizing up-state (66, 215, 597, 829 -832, 925, 1088).”
From About Sleep's Role in Memory (2013) · cites this paper as [66]
Split into 2 atoms — 0 confirmed, 0 partially supported, 2 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Checked by a reasoning model — may be wrong.
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
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
Destexhe, A., Contreras, D., & Steriade, M. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-11-04595.1999 · Cited by 573 · see citing works
Flagged first, then by citations
Research works printed but not linked: 10
- Marr, D. 1970. A theory for cerebral neocortex. Proc. R Soc. Lond. B Biol. Sci. 176: 161-234.
- McNaughton, B.L. 1983. Comments in hippocampus symposium panel discussion. In Neurobiology of the hippocampus (ed. W. Siefert), p. 610. Academic Press, New York.
- McNaughton, B.L., Barnes, C.A., Battaglia, F.P., Bower, M.R., Cowen, S.L., Ekstrom, A.D., Gerrard, J.L., Hoffman, K.L., Houston, F.P., Karten, Y., et al. 2003. Off-line reprocessing of recent memory and its role in memory consolidation: A progress report. In Sleep and brain plasticity (eds. P. Maquet et al.), pp. 225-246. Oxford University Press, Oxford, UK.
- O'Keefe, J. and Nadel, L. 1978. The hippocampus as a cognitive map. Oxford University Press, Oxford.
- Percival, D.B. and Walden, A.T. 2002. Spectral analysis for physical applications. Cambridge University Press, Cambridge, UK.
- Petersen, C.C., Hahn, T.T., Mehta, M., Grinvald, A., and Sakmann, B. 2003. Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc. Natl. Acad. Sci. 100: 13638-13643.
- Sirota, A., Csicsvari, J., Buhl, D., and Buzsaki, G. 2003. Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl. Acad. Sci. 100: 2065-2069.
- Steriade, M. and Buzsaki, G. 1990. Parallel activation of thalamic and cortical neurons by brainstem and basal forebrain cholinergic systems. In Brain cholinergic systems (eds. M. Steriade and D. Biesold), pp. 3-64. Oxford University Press, Oxford, UK.
- Timofeev, I., Grenier, F., and Steriade, M. 2001. Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: An intracellular study. Proc. Natl. Acad. Sci. 98: 1924-1929.
- Zilles, K. 1985. The cortex of the rat. Springer-Verlag, New York.
Cited by
Sorted by citations
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · 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
Coordinated 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
Selective suppression of hippocampal ripples impairs spatial memory
Girardeau, G., Benchenane, K., Wiener, S. I., Buzsáki, G., & Zugaro, M. B. (2009) · Nature Neuroscience · doi:10.1038/nn.2384 · Cited by 1,560 · see citing works
The role of medial prefrontal cortex in memory and decision making
Euston, D. R., Gruber, A. J., & McNaughton, B. L. (2012) · Neuron · doi:10.1016/j.neuron.2012.12.002 · Cited by 1,541 · see citing works
Self-citationNeural 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
“, 2003), which can bias the spike content of hippocampal sharp wave ripples (Battaglia et al., 2004; Ji and Wilson, 2007).”
Harris, K. D., & Thiele, A. (2011) · Nature reviews. Neuroscience · doi:10.1038/nrn3084 · Cited by 871 · see citing works
Scaling Brain Size, Keeping Timing: Evolutionary Preservation of Brain Rhythms
Buzsáki, G., Logothetis, N., & Singer, W. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.002 · Cited by 886 · see citing works
Hippocampal GABAergic Inhibitory Interneurons
Pelkey, K. A., Chittajallu, R., Craig, M. T., Tricoire, L., Wester, J. C., & McBain, C. J. (2017) · Physiological Reviews · doi:10.1152/physrev.00007.2017 · Cited by 889 · 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
“In support of this hypothesis, sharp waveripple events in the hippocampus have been shown to occur in close temporal proximity to neocortical spindles (Siapas and Wilson, 1998) and neocortical transitions from down to up states (Battaglia et al., 2004).”
BackgroundHippocampal 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
“…are also present during slowwave sleep, where they predominantly occur during periodic increases in neocortical population activity (‘‘up states’’) (Battaglia et al., 2004; Clemens et al., 2007; Mölle et al., 2006; Sirota et al., 2003) associated with slow oscillations in the cortical EEG…”
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
Self-citationWhat Learning Systems do Intelligent Agents Need? Complementary Learning Systems Theory Updated
Kumaran, D., Hassabis, D., & McClelland, J. L. (2016) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2016.05.004 · Cited by 736 · see citing works
Hippocampo-cortical coupling mediates memory consolidation during sleep
Maingret, N., Girardeau, G., Todorova, R., Goutierre, M., & Zugaro, M. (2016) · Nature Neuroscience · doi:10.1038/nn.4304 · Cited by 667 · 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
“Cortical circuits both in vitro and in vivo during resting and sleep spontaneously produce periods of activity known as ‘‘upstates’’ (Battaglia et al., 2004; Luczak et al., 2007; Massimini et al., 2004; Petersen et al., 2003; Sirota et al., 2003; Steriade et al., 1993a).”
BackgroundHippocampal-Neocortical Interactions in Memory Formation, Consolidation, and Reconsolidation
Wang, S., & Morris, R. (2009) · Annual Review of Psychology · doi:10.1146/annurev.psych.093008.100523 · Cited by 536 · 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
Born, J., Rasch, B., & Gais, S. (2006) · The Neuroscientist · doi:10.1177/1073858406292647 · Cited by 557 · see citing works
Play it again: reactivation of waking experience and memory
O’Neill, J., Pleydell-Bouverie, B., Dupret, D., & Csicsvari, J. L. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.01.006 · Cited by 448 · 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
The hippocampal sharp wave-ripple in memory retrieval for immediate use and consolidation
Joo, H. R., & Frank, L. M. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0077-1 · Cited by 430 · see citing works
The Role of Hippocampal Replay in Memory and Planning
Ólafsdóttir, H. F., Bush, D., & Barry, C. (2018) · Current Biology · doi:10.1016/j.cub.2017.10.073 · Cited by 413 · 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
“In rats and mice the grouping effect of the cortical slow oscillation is not limited to activity within neocortical and thalamocortical circuitry but pertains to hippocampal ripple activity as well, such that ripple activity becomes likewise suppressed during the slow oscillation down-state and increases in parallel w…”
BackgroundInfluentialThe hippocampal indexing theory and episodic memory: Updating the index
Teyler, T. J., & Rudy, J. W. (2007) · Hippocampus · doi:10.1002/hipo.20350 · Cited by 373 · see citing works
“, 2007) and bursts of activity during sleep (Battaglia et al., 2004; Behrens et al., 2005).”
BackgroundRipples in the medial temporal lobe are relevant for human memory consolidation
Axmacher, N., Elger, C. E., & Fell, J. (2008) · Brain · doi:10.1093/brain/awn103 · Cited by 372 · see citing works
“In vivo recordings in rats revealed that hippocampal sharp waves were locked to the depolarizing phase of neocortical delta waves/slow rhythm, which is associated with enhanced cortical activity (Sirota et al., 2003; Battaglia et al., 2004; Isomura et al., 2006; Mölle et al., 2006).”
BackgroundLearning-enhanced coupling between ripple oscillations in association cortices and hippocampus
Khodagholy, D., Gelinas, J. N., & Buzsáki, G. (2017) · Science · doi:10.1126/science.aan6203 · Cited by 357 · 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
The hippocampus: hub of brain network communication for memory
Battaglia, F. P., Benchenane, K., Sirota, A., Pennartz, C. M. A., & Wiener, S. I. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.05.008 · Cited by 351 · see citing works
Self-citationHippocampal Sharp Wave-Ripples Linked to Slow Oscillations in Rat Slow-Wave Sleep
Mölle, M., Yeshenko, O., Marshall, L., Sara, S. J., & Born, J. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00014.2006 · Cited by 337 · 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
Sleep and the single neuron: the role of global slow oscillations in individual cell rest
Vyazovskiy, V. V., & Harris, K. D. (2013) · Nature reviews. Neuroscience · doi:10.1038/nrn3494 · Cited by 362 · see citing works
Mölle, 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
“…of ripples, like that of spindles, is grouped by the slow oscillation, with there being minimum ripple activity during the hyperpolarization down-state in rats, mice, and humans (Sirota et al., 2003; Battaglia et al., 2004; Isomura et al., 2006; Mölle et al., 2006; Clemens et al., 2007).”
BackgroundSullivan, 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
“Finally, fluctuation of the strength of subcortical inputs may also contribute to the irregular nature of SPW-Rs (Buzsáki et al., 1983; Buzsáki 1989).”
InfluentialState-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep
Wierzynski, C. M., Lubenov, E. V., Gu, M., & Siapas, A. G. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.011 · Cited by 289 · see citing works
“5 Hz) or up and down states (Mölle et al., 2006; Hahn et al., 2006, 2007; Isomura et al., 2006; Battaglia et al., 2004; Sirota et al., 2003; Ji and Wilson, 2007).”
Sustained 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
“Moreover, hippocampal ripples and cortical spindles tend to group around the slow oscillations typical of SWS, thus promoting hippocampal–cortical communication during this sleep stage (Siapas and Wilson 1998; Sirota et al. 2003; Battaglia et al. 2004; Mölle et al. 2006).”
BackgroundSlow oscillations orchestrating fast oscillations and memory consolidation
Mölle, M., & Born, J. (2011) · Progress in Brain Research · doi:10.1016/b978-0-444-53839-0.00007-7 · Cited by 270 · 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
“…widespread, synchronized, oscillatory patterns that are defined primarily by spatially coherent delta waves (Achermann and Borbely, 1997) during which spiking activity of nearly all principal cells and interneurons in the neocortex is suspended (Steriade and Buzsáki, 1990;Battaglia et al., 2004).”
BackgroundInfluentialSleep-related hippocampo-cortical interplay during emotional memory recollection
Sterpenich, V., Albouy, G., Boly, M., Vandewalle, G., Darsaud, A., Balteau, E., Dang-Vu, T. T., Desseilles, M., D'Argembeau, A., Gais, S., et al. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050282 · Cited by 265 · see citing works
Inhibition recruitment in prefrontal cortex during sleep spindles and gating of hippocampal inputs
Peyrache, A., Battaglia, F. P., & Destexhe, A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1103612108 · Cited by 254 · see citing works
“SPWRs were phase-locked to spindles (26), but at larger timescales SPWRs preceded spindle occurrence (25), possibly because of common modulation by the slow oscillation (3, 24, 26, 29), in particular its DOWN phase (Fig.”
BackgroundSelf-citationHigh frequency oscillations in the intact brain
Buzsáki, G., & Lopes, F. H. D. S. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.02.004 · Cited by 247 · see citing works
“These effects are mediated largely by the entorhinal cortex and the medial prefrontal cortex (Chrobak and Buzsá ki, 1994, 1996; Battaglia et al., 2004; Wierzynski et al., 2009).”
The role of REM sleep theta activity in emotional memory
Hutchison, I. C., & Rathore, S. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01439 · Cited by 245 · see citing works
“…traces from the hippocampus to the neocortex (Rasch and Born, 2013) by providing windows of wide-spread depolarization during which higher frequency activity (including spindles) is synchronized across various brain regions (Battaglia et al., 2004; Compte et al., 2008; Mölle and Born, 2009, 2011).”
BackgroundWolansky, T., Clement, E., Peters, S. R., Palczak, M. A., & Dickson, C. T. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5594-05.2006 · Cited by 226 · see citing works
“, 2003 ; Battaglia et al .”
Packet-based communication in the cortex
Luczak, A., McNaughton, B. L., & Harris, K. D. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn4026 · Cited by 192 · see citing works
Self-citationFacilitation of epileptic activity during sleep is mediated by high amplitude slow waves
Frauscher, B., von Ellenrieder, N., Ferrari-Marinho, T., Avoli, M., Dubeau, F., & Gotman, J. (2015) · Brain : a journal of neurology · doi:10.1093/brain/awv073 · Cited by 228 · see citing works
“Moreover, the ‘up’ state was shown to coordinate the coupling between hippocampal HFOs and scalp spindles, which is of importance for memory consolidation (Sirota et al., 2003; Battaglia et al., 2004; Isomura et al., 2006; Mölle et al., 2006; Clemens et al., 2007, 2011).”
BackgroundSleep Spindles and Hippocampal Functional Connectivity in Human NREM Sleep
Andrade, K. C., Spoormaker, V. I., Dresler, M., Wehrle, R., Holsboer, F., Sämann, P., & Czisch, M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5660-10.2011 · Cited by 208 · see citing works
“Temporal coupling between spindles, hippocampal ripples, and slow-oscillations has been described before in that during the up state of cortical slow oscillations, both spindle activity and hippocampal high-frequency ripple activity were increased (Sirota et al., 2003; Battaglia et al., 2004).”
BackgroundEschenko, O., Magri, C., Panzeri, S., & Sara, S. J. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr121 · Cited by 194 · see citing works
“The sharp wave/ripple complexes recorded in hippocampus are likewise grouped by slow oscillations (Sirota et al. 2003; Battaglia et al. 2004; Moïle et al. 2006).”
Le Van Quyen, M., Staba, R., Bragin, A., Dickson, C., Valderrama, M., Fried, I., & Engel, J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5049-09.2010 · Cited by 189 · see citing works
“These observations are consistent with others reporting a temporal association between sharp waves and cortical slow waves in rodents (Battaglia et al., 2004) or humans (Clemens et al., 2007; Axmacher et al., 2008), suggesting a common driving influence of the slow oscillation on both hippocampal…”
ResultSleep, dreams, and memory consolidation: the role of the stress hormone cortisol
Payne, J. D., & Nadel, L. (2004) · Learning & Memory · doi:10.1101/lm.77104 · Cited by 184 · see citing works
“Over the course of the night, the brain oscillates between a”
BackgroundNREM and REM Sleep: Complementary Roles in Recovery after Wakefulness
Vyazovskiy, V. V., & Delogu, A. (2014) · The Neuroscientist · doi:10.1177/1073858413518152 · Cited by 169 · see citing works
Preferential Reactivation of Motivationally Relevant Information in the Ventral Striatum
Lansink, C. S., Goltstein, P. M., Lankelma, J. V., Joosten, R. N. J. M. A., McNaughton, B. L., & Pennartz, C. M. A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1054-08.2008 · Cited by 168 · see citing works
“…occurs during hippocampal ripples and shortly thereafter, these high-frequency oscillations and the associated transitions in neocortical states (Battaglia et al., 2004; Siapas et al., 2005) may act as a release mechanism by which the principal cells of VS reactivate motivational information…”
BackgroundSelf-citationThe rodent hippocampus and spatial memory: from synapses to systems
Martin, S. J., & Clark, R. E. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-6336-3 · Cited by 165 · see citing works
EEG Sharp Waves and Sparse Ensemble Unit Activity in the Macaque Hippocampus
Skaggs, W. E., McNaughton, B. L., Permenter, M. R., Archibeque, M., Vogt, J. A., Amaral, D. G., & Barnes, C. A. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00401.2007 · Cited by 138 · see citing works
Self-citationHippocampal sharp-wave ripples in waking and sleeping states
Roumis, D. K., & Frank, L. M. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.05.001 · Cited by 155 · see citing works
UP-DOWN cortical dynamics reflect state transitions in a bistable network
Jercog, D., Roxin, A., Barthó, P., Luczak, A., Compte, A., & de la Rocha, J. (2017) · eLife · doi:10.7554/elife.22425 · Cited by 159 · see citing works
“We postulate that these spontaneous bumps (DeWeese and Zador, 2006; Tan et al., 2013; Taub et al., 2013) (1) are caused by synchronous external inputs impinging on the neocortex, possibly from thalamocortical neurons (Crunelli and Hughes, 2010), since spontaneous bumps resemble sensory evoked responses (DeWeese and Za…”
BackgroundInfluentialPhase-locking of hippocampal interneurons' membrane potential to neocortical up-down states
Hahn, T. T. G., Sakmann, B., & Mehta, M. (2006) · Nature Neuroscience · doi:10.1038/nn1788 · Cited by 144 · see citing works
Priming of hippocampal population bursts by individual perisomatic-targeting interneurons
Ellender, T., Nissen, W., Colgin, L., Mann, E., & Paulsen, O. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3962-09.2010 · Cited by 142 · see citing works
“…sleep (Bragin et al., 1995), and, recently, a number of studies have shown the influence of the cortical slow oscillation on sharp wave–ripple generation in the hippocampus in both rodents (Sirota et al., 2003; Battaglia et al., 2004; Isomura et al., 2006) and humans (Clemens et al., 2007).”
BackgroundCoupling of Thalamocortical Sleep Oscillations Are Important for Memory Consolidation in Humans
Niknazar, M., Krishnan, G., Bazhenov, M., & Mednick, S. (2015) · PLoS ONE · doi:10.1371/journal.pone.0144720 · Cited by 138 · see citing works
The mystery of sleep function: Current perspectives and future directions
Frank, M. G. (2006) · Reviews in the Neurosciences · doi:10.1515/revneuro.2006.17.4.375 · Cited by 136 · see citing works
Reactivation, Replay, and Preplay: How It Might All Fit Together
Buhry, L., Azizi, A. H., & Cheng, S. (2011) · Neural Plasticity · doi:10.1155/2011/203462 · Cited by 134 · see citing works
“SWRs in the hippocampus apparently appear more frequently during down states, particularly near the transition from the down to the up state [46–48].”
BackgroundJohnson, L. A., Euston, D. R., Tatsuno, M., & McNaughton, B. L. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1617-09.2010 · Cited by 160 · see citing works
Self-citationSpatiotemporal patterns of neocortical activity around hippocampal sharp-wave ripples
Abadchi, J. K., Nazari-Ahangarkolaee, M., Gattas, S., Bermudez-Contreras, E. J., Luczak, A., McNaughton, B. L., & Mohajerani, M. H. (2020) · eLife · doi:10.7554/elife.51972 · Cited by 124 · see citing works
“Battaglia et al.(Battaglia et al., 2004) however, have mentioned a midline bias in the modulation of firing rate of different neocortical regions around SWRs, but they left the detailed analysis of such regional effect for future studies.”
BackgroundMethodResultInfluentialSelf-citationPropagation of hippocampal ripples to the neocortex by way of a subiculum-retrosplenial pathway
Nitzan, N., McKenzie, S., Beed, P. S., English, D. F., Oldani, S., Tukker, J. J., Buzsáki, G., & Schmitz, D. (2020) · Nature Communications · doi:10.1038/s41467-020-15787-8 · Cited by 129 · see citing works
NREM sleep in the rodent neocortex and hippocampus reflects excitable dynamics
Levenstein, D., Buzsáki, G., & Rinzel, J. (2019) · Nature Communications · doi:10.1038/s41467-019-10327-5 · Cited by 148 · see citing works
The physics of living neural networks
Eckmann, J., Feinerman, O., Gruendlinger, L., Moses, E., Soriano, J., & Tlusty, T. (2007) · Physics Reports · doi:10.1016/j.physrep.2007.02.014 · Cited by 119 · see citing works
Memory reactivation and consolidation during sleepPreprint
Paller, K. A., & Voss, J. L. (2004) · Learning & Memory · doi:10.1101/lm.75704 · Cited by 117 · see citing works
“Physiological studies in animals are described in two articles in this special issue (Battaglia et al. 2004; Ribeiro and Nicolelis 2004).”
BackgroundInfluentialSynaptic Mechanisms of Memory Consolidation during Sleep Slow Oscillations
Wei, Y., Krishnan, G. P., & Bazhenov, M. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.3648-15.2016 · Cited by 116 · see citing works
“Several studies supported the hypothesis that SPW-R events occur mainly in the neocortical transition from Down to Up states (Battaglia et al., 2004), and suppression of hippocampal ripple results in poor performance in memory tasks (Ego-Stengel and Wilson, 2010).”
BackgroundSleep and the functional connectome
Picchioni, D., Duyn, J. H., & Horovitz, S. G. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.05.067 · Cited by 115 · see citing works
Differential responses of hippocampal subfields to cortical up–down states
Hahn, T. T. G., Sakmann, B., & Mehta, M. (2007) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0700222104 · Cited by 114 · see citing works
Cellular and System Biology of Memory: Timing, Molecules, and Beyond
Körte, M., & Schmitz, D. (2016) · Physiological Reviews · doi:10.1152/physrev.00010.2015 · Cited by 123 · see citing works
Diversity of sharp-wave–ripple LFP signatures reveals differentiated brain-wide dynamical events
Ramirez-Villegas, J. F., Logothetis, N., & Besserve, M. (2015) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1518257112 · Cited by 111 · see citing works
Hippocampal-cortical interaction in decision making
Yu, J. Y., & Frank, L. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.02.002 · Cited by 110 · see citing works
“The PFC shows time locked LFP changes to SWRs depending on sleep state (Siapas and Wilson 1998; Sirota et al. 2003; Battaglia et al. 2004; Molle et al. 2006; Wierzynski et al. 2009).”
BackgroundHippocampal–cortical interactions and the dynamics of memory trace reactivation
Schwindel, C. D., & McNaughton, B. L. (2011) · Progress in brain research · doi:10.1016/b978-0-444-53839-0.00011-9 · Cited by 101 · see citing works
Self-citationReplay, the default mode network and the cascaded memory systems model
Kaefer, K., Stella, F., McNaughton, B. L., & Battaglia, F. P. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00620-6 · Cited by 124 · see citing works
Self-citationReplay 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 · see citing works
“There is evidence for coordination between oscillations across the cortex and hippocampus (Battaglia, Sutherland, & McNaughton, 2004; Sirota, Csicsvari, Buhl, & Buzsáki, 2003; Mölle, Yeshenko, Marshall, Sara, & Born, 2006; Siapas & Wilson, 1998), suggesting that sleep rhythms can mediate the…”
Two distinct activity patterns of fast-spiking interneurons during neocortical UP states
Puig, M. V., Ushimaru, M., & Kawaguchi, Y. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0712219105 · Cited by 98 · see citing works
Modeling sharp wave‐ripple complexes through a CA3‐CA1 network model with chemical synapses
Taxidis, J., Coombes, S., Mason, R., & Owen, M. (2012) · Hippocampus · doi:10.1002/hipo.20930 · Cited by 104 · see citing works
“Correlations between ripples and cortical slow oscillations during deep sleep (Siapas and Wilson, 1998; Sirota et al., 2003; Battaglia et al., 2004; Isomura et al., 2006) and the fast-scale replay, during SPWRs, of temporal patterns of correlated place cells in forward (Wilson and McNaughton, 1994;…”
BackgroundInfluentialHippocampo-cortical circuits for selective memory encoding, routing, and replay
Harvey, R. E., Robinson, H. L., Liu, C., Oliva, A., & Fernandez-Ruiz, A. (2023) · Neuron · doi:10.1016/j.neuron.2023.04.015 · Cited by 101 · see citing works
Hippocampal memory consolidation during sleep: a comparison of mammals and birds
Rattenborg, N. C., Martı́nez-González, D., Roth, T. C., & Витальевич, П. В. (2010) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2010.00165.x · Cited by 121 · see citing works
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 105 · see citing works
“This is in line with a number of studies showing that hippocampal ripple activity occurs preferentially during the depolarized up states of cortical slow oscillation (Sirota et al., 2003; Isomura et al., 2006; Mölle et al., 2006; Nir et al., 2011; but see Battaglia et al., 2004; Hahn et al., 2007).”
ResultTask Demands Predict a Dynamic Switch in the Content of Awake Hippocampal Replay
Ólafsdóttir, H., Carpenter, F., & Barry, C. (2017) · bioRxiv · doi:10.1016/j.neuron.2017.09.035 · Cited by 94 · see citing works
“It is unlikely that the observed difference between engaged and disengaged periods result from theta sequences (Foster and Wilson, 2006; Gupta et al., 2012; Johnson and Redish, 2007) or phase precession(O’Keefe and Recce, 1993): theta power during engaged and disengaged replay events did not differ (log(theta/delta) p…”
BackgroundInfluentialCommon oscillatory mechanisms across multiple memory systems
Headley, D. B., & Paré, D. (2017) · npj Science of Learning · doi:10.1038/s41539-016-0001-2 · Cited by 94 · see citing works
Differential roles of sleep spindles and sleep slow oscillations in memory consolidation
Wei, Y., Krishnan, G. P., Komarov, M., & Bazhenov, M. (2018) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006322 · Cited by 92 · see citing works
Contreras, E. B., Schjetnan, A. G.-P., Muhammad, A., Barthó, P., McNaughton, B., Kolb, B., Gruber, A., & Luczak, A. (2013) · Neuron · doi:10.1016/j.neuron.2013.06.013 · Cited by 88 · see citing works
“Although multiple studies show that most memory replay occurs during synchronized states (e.g., during slow wave sleep; Battaglia et al., 2004; Xu et al., 2012), the importance of the brain state during encoding is not clear.”
BackgroundSelf-citationAlger, S. E., Lau, H., & Fishbein, W. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2012.06.003 · Cited by 86 · see citing works
Tatsuno, M., Lipa, P., & McNaughton, B. L. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3317-06.2006 · Cited by 86 · see citing works
“…that the spontaneous reactivation of memory-traces in the hippocampus during subsequent sleep may orchestrate memory consolidation in neocortical circuits (Marr, 1971; Buzsaki, 1989; Chrobak and Buzsaki, 1994; McClelland et al., 1995; Hoffman and McNaughton, 2002; Battaglia et al., 2004).”
BackgroundSelf-citationNovitskaya, Y., Sara, S., Logothetis, N., & Eschenko, O. (2016) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.040923.115 · Cited by 86 · see citing works
“cortical up-states and sleep spindles (Siapas and Wilson 1998; Battaglia et al. 2004; Molle et al. 2006), we reasoned that LC”
BackgroundBrain-wide interactions during hippocampal sharp wave ripples
Nitzan, N., Swanson, R., Schmitz, D., & Buzsáki, G. (2022) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.2200931119 · Cited by 84 · see citing works
Laufs, H., Walker, M., & Lund, T. (2007) · Brain : a journal of neurology · doi:10.1093/brain/awm084 · Cited by 84 · see citing works
“3, SP/KC), which is in agreement with studies at the cellular level (Amzica and Steriade, 1997) and the observation in rats that KC mark the transition from ‘down-to-up’ states, whilst Sp activity typically occurs in the subsequent upstate (Molle et al., 2002; Battaglia et al., 2004).”
ResultThe beneficial role of memory reactivation for language learning during sleep: A review
Schreiner, T., & Rasch, B. (2016) · Brain and Language · doi:10.1016/j.bandl.2016.02.005 · Cited by 72 · see citing works
Sharp Wave Ripples during Visual Exploration in the Primate Hippocampus
Leonard, T. K., Mikkila, J. M., Eskandar, E., Gerrard, J., Kaping, D., Patel, S. R., Womelsdorf, T., & Hoffman, K. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0864-15.2015 · Cited by 80 · see citing works
“The sharp-wave ripple (SWR) is a highly synchronized hippocampal field potential complex associated with widespread activation of the neocortex (Chrobak, and Buzsáki, 1994; Siapas and Wilson, 1998; Sirota et al., 2003; Battaglia et al., 2004; Isomura et al., 2006; Mölle et al., 2006; Logothetis et al., 2012).”
BackgroundInfluentialSleep regulation of the distribution of cortical firing rates
Levenstein, D., Watson, B., Rinzel, J., & Buzsáki, G. (2017) · bioRxiv · doi:10.1101/084731 · Cited by 78
“SPW-Rs are temporally coordinated with slow wave activity [59], and have been found to both precede [58,60] and follow [61] the cortical DOWN state.”
Origin of Gamma Frequency Power during Hippocampal Sharp-Wave Ripples
Oliva, A., Fernández-Ruiz, A., de Oliveira, E. F., & Buzsáki, G. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.10.066 · Cited by 75 · see citing works
“However, other factors, such as various network patterns in the neocortex, entorhinal cortex, and dentate gyrus, can also bias the exact occurrence and probability of SPW-Rs (Battaglia et al., 2004; Isomura et al., 2006; Headley et al., 2017; Sirota et al., 2003; Sullivan et al., 2011).”
BackgroundHippocampo-cortical circuits for selective memory encoding, routing, and replayPreprint
Harvey, R. E., Robinson, H. L., Liu, C., Oliva, A., & Fernández-Ruiz, A. (2022) · bioRxiv · doi:10.1101/2022.09.25.509420 · Cited by 74 · see citing works
Young, C. K., & Eggermont, J. (2009) · Progress in neurobiology · doi:10.1016/j.pneurobio.2009.06.002 · Cited by 74 · see citing works
Hippocampal network oscillations at the interplay between innate anxiety and learned fear
Çalışkan, G., & Stork, O. (2019) · Psychopharmacology · doi:10.1007/s00213-018-5109-z · Cited by 72 · see citing works
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 · see citing works
“Increased SWR probability at both the down-to-upstate and up-to-down-state transitions (Battaglia et al., 2004; Peyrache et al., 2009; Wilber et al., 2017) led to the conceptualization of SWRs as “toggle-switches”, which facilitate cortical network state transitions (Genzel, Kroes, Dresler, & Battaglia, 2014).”
BackgroundInfluentialSelf-citationFrontal beta-theta network during REM sleep
Vijayan, S., Lepage, K., Kopell, N., & Cash, S. (2017) · eLife · doi:10.7554/elife.18894 · Cited by 72 · see citing works
“…field potentials, namely by the interaction of hippocampal ripples (80–250 Hz) with neocortical spindles (11–16 Hz) and slow (<1 Hz) oscillations (Battaglia et al., 2004; Ji and Wilson, 2007; Lee and Wilson, 2002; Mölle et al., 2006; Siapas and Wilson, 1998; Sirota et al., 2003; Skaggs and…”
BackgroundThe Upshot of Up States in the Neocortex: From Slow Oscillations to Memory Formation
Hoffman, K., Battaglia, F., Harris, K., MacLean, J., Marshall, L., & Mehta, M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3501-07.2007 · Cited by 72 · see citing works
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 71 · see citing works
“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).”
BackgroundDeciphering 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 64 · see citing works
- Authors
- Battaglia, F. P., Sutherland, G. R., & McNaughton, B. L.
- Affiliations
- University of Arizona (US)
- Centre National de la Recherche Scientifique (FR)
- Venue
- Learning & Memory
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2004-11
- Volume
- 11
- Issue
- 6
- Pages
- 697-704
- ISSN
- 1072-0502 (ISSN-L)
- 1549-5485
- PMC
- PMC534698
- OpenAlex
- W1986823100
- Cited by
- 310
- References
- 43
- Citations by year
- 2026: 2 · 2025: 15 · 2024: 14 · 2023: 11 · 2022: 17 · 2021: 13 · 2020: 19 · 2019: 14 · 2018: 17 · 2017: 25 · 2016: 20 · 2015: 14 · 2014: 16 · 2013: 13 · 2012: 10
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Learning & Memory (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (R01MH046823, R37MH046823)
- National Institute of General Medical Sciences (T32GM008400)
- 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
- sleep, hippocampal-neocortical interaction, sleep depth, delta oscillations, memory consolidation
- MeSH terms
- Animals, Cortical Synchronization, Electroencephalography, Hippocampus, Membrane Potentials, Neural Pathways, Neurons, Sleep, Neocortex, 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
