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Hippocampal sharp wave bursts coincide with neocortical “up-state” transitions
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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.
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“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).”
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Levenstein, D., Buzsáki, G., & Rinzel, J. (2019) · Nature Communications · doi:10.1038/s41467-019-10327-5 · Cited by 155
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 128
Memory reactivation and consolidation during sleepPreprint
Paller, K. A., & Voss, J. L. (2004) · Learning & Memory · doi:10.1101/lm.75704 · Cited by 120
“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
“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
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
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 132
Diversity of sharp-wave–ripple LFP signatures reveals differentiated brain-wide dynamical events
Ramírez-Villegas, J. F., Logothetis, N. K., & Besserve, M. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1518257112 · Cited by 105
Hippocampal–cortical interaction in decision making
Yu, J. Y., & Frank, L. M. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.02.002 · Cited by 119
“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 107
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 132
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
“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 101
Modeling sharp wave‐ripple complexes through a CA3‐CA1 network model with chemical synapses
Taxidis, J., Coombes, S., Mason, R., & Owen, M. R. (2011) · Hippocampus · doi:10.1002/hipo.20930 · Cited by 97
“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
Hippocampal memory consolidation during sleep: a comparison of mammals and birds
Rattenborg, N. C., Martínez-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 128
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
“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. F., Carpenter, F., & Barry, C. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.035 · Cited by 142
“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 101
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 99
Bermudez-Contreras, E. J., Gómez-Palacio-Schjetnan, A., Muhammad, A., Barthó, P., McNaughton, B. L., Kolb, B. E., Gruber, A. J., & Luczak, A. (2013) · Neuron · doi:10.1016/j.neuron.2013.06.013 · Cited by 88
“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
Tatsuno, M., Lipa, P., & McNaughton, B. L. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3317-06.2006 · Cited by 86
“…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. J., Logothetis, N. K., & Eschenko, O. (2016) · Learning & Memory · doi:10.1101/lm.040923.115 · Cited by 116
“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. A., Schmitz, D., & Buzsáki, G. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2200931119 · Cited by 99
Laufs, H., Walker, M., & Lund, T. (2007) · Brain : a journal of neurology · doi:10.1093/brain/awm084 · Cited by 84
“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 78
Sharp Wave Ripples during Visual Exploration in the Primate Hippocampus
Leonard, T. K., Mikkila, J. M., Eskandar, E. N., Gerrard, J. L., Kaping, D., Patel, S. R., Womelsdorf, T., & Hoffman, K. L. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0864-15.2015 · Cited by 82
“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
“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
Young, C. K., & Eggermont, J. J. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.06.002 · Cited by 71
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
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
“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. Q., Kopell, N., & Cash, S. S. (2017) · eLife · doi:10.7554/elife.18894 · Cited by 92
“…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. L., Battaglia, F. P., Harris, K., MacLean, J. N., Marshall, L., & Mehta, M. R. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3501-07.2007 · Cited by 66
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).”
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 65
Metadata
- 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
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