Enhancement of hippocampal-thalamocortical temporal coordination during slow-frequency long-duration anterior thalamic spindles
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Abstract
Temporal nesting of cortical slow oscillations, thalamic spindles, and hippocampal ripples indicates multiregional neuronal interactions required for memory consolidation. However, how the thalamic activity during spindles organizes hippocampal dynamics remains largely undetermined. We analyzed simultaneous recordings of anterodorsal thalamus and CA1 in male mice to determine the contribution of thalamic spindles in cross-regional synchronization. Our results indicated that temporal hippocampo-thalamocortical coupling was more enhanced during slower and longer thalamic spindles. Additionally, spindles occurring closer to slow oscillation trough were more strongly coupled to ripples. We found that the temporal association between CA1 spiking/ripples and thalamic spindles was stronger following spatial exploration compared with baseline sleep. We further developed a hippocampal-thalamocortical model to explain the mechanism underlying the duration and frequency-dependent coupling of thalamic spindles to hippocampal activity. Our findings shed light on our understanding of the functional role of thalamic activity during spindles on multiregional information transfer. SIGNIFICANCE STATEMENT The contribution of thalamic spindles with differential properties to cross-regional synchronization and information transfer still remains poorly understood. Using simultaneous anterodorsal thalamic and hippocampal recordings from naturally sleeping mice before and after exploration, we found strong coupling of CA1 units to anterodorsal thalamic spindles and increase of this coupling following spatial experience. We further showed that the temporal coupling of CA1 units and hippocampal ripples with thalamic spindles and the spindle-associated modulation of CA1 units with ripples were stronger for spindles with slower frequency of oscillations. Our experimental as well as computational findings using a hippocampal-thalamocortical model provide the first demonstration that spindle frequency and duration can provide valuable information about the underlying multiregional interactions essential for memory consolidation computations.
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The anterior thalamus might be specifically involved in coordinating hippocampal memory replay with thalamocortical activity.
“The anterior thalamus might be specifically involved in coordinating hippocampal memory replay with thalamocortical activity.189”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [189]
The Abstract and Discussion report that anterodorsal thalamic spindles are temporally coupled with CA1 activity and hippocampal ripples, with stronger coupling after spatial exploration. This supports a possible coordinating role, but the paper measures spiking and ripples, not hippocampal memory replay itself. (LLM, conf=0.84)
Experimental — accuracy not yet measuredSleep spindles are associated with signs of increased synchronization between hippocampal and neocortical activity in both mice and humans.
“Indeed, sleep spindles have been found to be associated with signs of increased synchronization between hippocampal and neocortical activity in both mice 189 and humans.34”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [189]
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Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482 · see citing works
Delorme, A., & Makeig, S. (2004) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2003.10.009 · Cited by 24,371 · see citing works
Oostenveld, R., Fries, P., Maris, E., & Schoffelen, J.-M. (2011) · Computational Intelligence and Neuroscience · doi:10.1155/2011/156869 · Cited by 10,323 · see citing works
Diekelmann, S., & Born, J. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2762 · Cited by 3,760 · see citing works
<b>CircStat</b> : A <i>MATLAB</i> Toolbox for Circular Statistics
Berens, P. (2009) · Journal of Statistical Software · doi:10.18637/jss.v031.i10 · Cited by 3,099 · see citing works
Interplay of Hippocampus and Prefrontal Cortex in Memory
Preston, A. R., & Eichenbaum, H. (2013) · Current Biology · doi:10.1016/j.cub.2013.05.041 · Cited by 1,389 · see citing works
Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo
Klausberger, T., Magill, P. J., Márton, L. F., Roberts, J. D. B., Cobden, P. M., Buzsáki, G., & Somogyi, P. (2003) · Nature · doi:10.1038/nature01374 · Cited by 1,345 · see citing works
Circular Statistics in Biology
Jupp, P. E., & Batschelet, E. (1982) · Biometrics · doi:10.2307/2530079 · Cited by 1,330 · 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
Ylinen, A., Bragin, A., Nadasdy, Z., Jando, G., Szabo, I., Sik, A., & Buzsaki, G. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00030.1995 · Cited by 1,092 · 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
Communication between neocortex and hippocampus during sleep in rodents
Sirota, A., Csicsvari, J., Buhl, D., & Buzsáki, G. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0437938100 · Cited by 930 · see citing works
Brunel, N., & Wang, X. (2003) · Journal of Neurophysiology · doi:10.1152/jn.01095.2002 · Cited by 854 · see citing works
Staresina, B. P., Bergmann, T. O., Bonnefond, M., van der Meij, R., Jensen, O., Deuker, L., Elger, C. E., Axmacher, N., & Fell, J. (2015) · Nature Neuroscience · doi:10.1038/nn.4119 · Cited by 831 · see citing works
Sleep spindles: mechanisms and functions
Fernandez, L. M. J., & Lüthi, A. (2020) · Physiological Reviews · doi:10.1152/physrev.00042.2018 · Cited by 716 · 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
Fogel, S. M., & Smith, C. T. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.12.003 · Cited by 628 · see citing works
Latchoumane, C.-F. V., Ngo, H.-V. V., Born, J., & Shin, H.-S. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.025 · Cited by 561 · see citing works
Mölle, M., Bergmann, T. O., Marshall, L., & Born, J. (2011) · Sleep · doi:10.5665/sleep.1290 · Cited by 557 · see citing works
Reduced sleep spindle activity in schizophrenia patients
Ferrarelli, F., Huber, R., Peterson, M. J., Massimini, M., Murphy, M., Riedner, B. A., Watson, A., Bria, P., & Tononi, G. (2007) · American Journal of Psychiatry · doi:10.1176/appi.ajp.164.3.483 · Cited by 541 · see citing works
Reduced Sleep Spindle Activity in Schizophrenia Patients
Ferrarelli, F., Huber, R., Peterson, M. J., Massimini, M., Murphy, M., Riedner, B. A., Watson, A., Bria, P., & Tononi, G. (2007) · American Journal of Psychiatry · doi:10.1176/ajp.2007.164.3.483 · Cited by 531 · see citing works
Projections from neocortex mediate top-down control of memory retrieval
Rajasethupathy, P., Sankaran, S., Marshel, J. H., Kim, C. K., Ferenczi, E., Lee, S. Y., Berndt, A., Ramakrishnan, C., Jaffe, A., Lo, M., et al. (2015) · Nature · doi:10.1038/nature15389 · Cited by 509 · see citing works
Sleep Spindles in Humans: Insights from Intracranial EEG and Unit Recordings
Andrillon, T., Nir, Y., Staba, R. J., Ferrarelli, F., Cirelli, C., Tononi, G., & Fried, I. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.2604-11.2011 · Cited by 504 · see citing works
Old brains come uncoupled in sleep: slow wave-spindle synchrony, brain atrophy, and forgetting
Helfrich, R. F., Mander, B. A., Jagust, W. J., Knight, R. T., & Walker, M. P. (2018) · Neuron · doi:10.1016/j.neuron.2017.11.020 · Cited by 497 · see citing works
Long-duration hippocampal sharp wave ripples improve memory
Fernández-Ruiz, A., Oliva, A., Fermino de Oliveira, E., Rocha-Almeida, F., Tingley, D., & Buzsáki, G. (2019) · Science · doi:10.1126/science.aax0758 · Cited by 490 · see citing works
Alain Destexhe, A., Bal, T., McCormick, D. A., & B, T. J. S. A. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.3.2049 · Cited by 418 · see citing works
Multisensory Control of Hippocampal Spatiotemporal Selectivity
Ravassard, P., Kees, A. L., Willers, B., Ho, D. G., Aharoni, D. B., Cushman, J. D., Aghajan, Z. M., & Mehta, M. R. (2013) · Science · doi:10.1126/science.1232655 · Cited by 388 · see citing works
Witter, M. P., Doan, T. P., Jacobsen, B., Nilssen, E. S., & Ohara, S. (2017) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2017.00046 · Cited by 352 · see citing works
Hippocampal 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
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
The Critical Role of Sleep Spindles in Hippocampal-Dependent Memory: A Pharmacology Study
Mednick, S. C., McDevitt, E. A., Walsh, J. K., Wamsley, E. J., Paulus, M. P., Kanady, J. C., & Drummond, S. P. A. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3127-12.2013 · Cited by 318 · see citing works
Bal, T., von Krosigk, M., & McCormick, D. A. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp020612 · Cited by 316 · see citing works
The anterior thalamus provides a subcortical circuit supporting memory and spatial navigation
Jankowski, M. M., Rönnqvist, K. C., Tsanov, M., Vann, S. D., Wright, N. F., Erichsen, J. T., Aggleton, J. P., & O’Mara, S. M. (2013) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2013.00045 · Cited by 309 · see citing works
State-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
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
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
What Stops Synchronized Thalamocortical Oscillations?
Bal, T., & McCormick, D. A. (1996) · Neuron · doi:10.1016/s0896-6273(00)80161-0 · Cited by 250 · see citing works
FOGEL, S., SMITH, C., & COTE, K. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.02.037 · Cited by 246 · see citing works
Cortical circuit activity underlying sleep slow oscillations and spindles
Niethard, N., Ngo, H.-V. V., Ehrlich, I., & Born, J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1805517115 · Cited by 245 · see citing works
Interactions Between Membrane Conductances Underlying Thalamocortical Slow-Wave Oscillations
DESTEXHE, A., & SEJNOWSKI, T. J. (2003) · Physiological Reviews · doi:10.1152/physrev.00012.2003 · Cited by 241 · see citing works
Encoding Difficulty Promotes Postlearning Changes in Sleep Spindle Activity during Napping
Schmidt, C., Peigneux, P., Muto, V., Schenkel, M., Knoblauch, V., Münch, M. Y., de Quervain, D. J. ‐., Wirz‐Justice, A., & Cajochen, C. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2464-06.2006 · Cited by 230 · see citing works
Precise Slow Oscillation–Spindle Coupling Promotes Memory Consolidation in Younger and Older Adults
Muehlroth, B. E., Sander, M. C., Fandakova, Y., Grandy, T. H., Rasch, B., Shing, Y. L., & Werkle‐Bergner, M. (2019) · Scientific Reports · doi:10.1038/s41598-018-36557-z · Cited by 227 · see citing works
Bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans
Helfrich, R. F., Lendner, J. D., Mander, B. A., Guillen, H., Paff, M., Mnatsakanyan, L., Vadera, S., Walker, M. P., Lin, J. J., & Knight, R. T. (2019) · Nature Communications · doi:10.1038/s41467-019-11444-x · Cited by 222 · see citing works
Ladenbauer, J., Ladenbauer, J., Külzow, N., de Boor, R., Avramova, E., Grittner, U., & Flöel, A. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0260-17.2017 · Cited by 220 · see citing works
Fine‐tuned coupling between human parahippocampal ripples and sleep spindles
Clemens, Z., Mölle, M., Erőss, L., Jakus, R., Rásonyi, G., Halász, P., & Born, J. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07505.x · Cited by 214 · see citing works
Motor Sequence Learning Increases Sleep Spindles and Fast Frequencies in Post-Training Sleep
(2008) · Sleep · doi:10.5665/sleep/31.8.1149 · Cited by 213 · see citing works
Sleep spindle characteristics in healthy subjects of different age groups
Nicolas, A., Petit, D., Rompré, S., & Montplaisir, J. Y. (2001) · Clinical Neurophysiology · doi:10.1016/s1388-2457(00)00556-3 · Cited by 207 · see citing works
Periodicity of Thalamic Synchronized Oscillations: the Role of Ca2+-Mediated Upregulation of Ih
Lüthi, A., & McCormick, D. A. (1998) · Neuron · doi:10.1016/s0896-6273(00)80994-0 · Cited by 203 · see citing works
Fast and slow spindle involvement in the consolidation of a new motor sequence
Barakat, M., Doyon, J., Debas, K., Vandewalle, G., Morin, A., Poirier, G., Martin, N., Lafortune, M., Karni, A., Ungerleider, L. G., et al. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.10.019 · Cited by 203 · see citing works
Xia, F., Richards, B. A., Tran, M. M., Josselyn, S. A., Takehara‐Nishiuchi, K., & Frankland, P. W. (2017) · eLife · doi:10.7554/elife.27868 · Cited by 202 · see citing works
Corticothalamic Feedback Controls Sleep Spindle Duration In Vivo
Bonjean, M., Baker, T., Lemieux, M., Timofeev, I., B, T. J. S. A., & Bazhenov, M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0077-11.2011 · Cited by 187 · see citing works
Interindividual sleep spindle differences and their relation to learning-related enhancements
Schabus, M., Hoedlmoser, K., Pecherstorfer, T., Anderer, P., Gruber, G., Parapatics, S., Sauter, C., Kloesch, G., Klimesch, W., Saletu, B., et al. (2008) · Brain Research · doi:10.1016/j.brainres.2007.10.106 · Cited by 174 · see citing works
Sleep spindles mediate hippocampal-neocortical coupling during long-duration ripples
Ngo, H.-V. V., Fell, J., & Staresina, B. P. (2020) · eLife · doi:10.7554/elife.57011 · Cited by 155 · see citing works
Topographic organization of subcortical projections to the anterior thalamic nuclei in the rat
Shibata, H. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903230110 · Cited by 153 · see citing works
The Functional Influence of Burst and Tonic Firing Mode on Synaptic Interactions in the Thalamus
Kim, U., & McCormick, D. A. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-22-09500.1998 · Cited by 151 · see citing works
Coordination of cortical and thalamic activity during non-REM sleep in humans
Mak-McCully, R. A., Rolland, M., Sargsyan, A., Gonzalez, C. E., Magnin, M., Chauvel, P., Rey, M. F., Bastuji, H., & Halgren, E. (2017) · Nature Communications · doi:10.1038/ncomms15499 · Cited by 150 · see citing works
The Sleep EEG as a Marker of Intellectual Ability in School Age Children
Geiger, A., Huber, R., Kurth, S., Ringli, M., Jenni, O. G., & Achermann, P. (2011) · Sleep · doi:10.1093/sleep/34.2.181 · Cited by 148 · 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
Coupling 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
Spindle activity phase-locked to sleep slow oscillations
Klinzing, J. G., Mölle, M., Weber, F. D., Supp, G. G., Hipp, J. F., Engel, A. K., & Jan Born, A. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.04.031 · Cited by 130 · see citing works
Ongoing Network State Controls the Length of Sleep Spindles via Inhibitory Activity
Barthó, P., Slézia, A., Mátyás, F., Faradzs-Zade, L., Ulbert, I., Harris, K. D., & Acsády, L. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.046 · Cited by 123 · see citing works
Sleep Spindle Activity and Cognitive Performance in Healthy Children
Chatburn, A., Coussens, S. W., Lushington, K., Kennedy, D., Baumert, M., & Kohler, M. J. (2013) · SLEEP · doi:10.5665/sleep.2380 · Cited by 112 · see citing works
Periodicity of Thalamic Spindle Waves Is Abolished by ZD7288,a Blocker of I h
Lüthi, A., Bal, T., & McCormick, D. A. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.6.3284 · Cited by 97 · see citing works
Lustenberger, C., Wehrle, F. M., Tüshaus, L., Achermann, P., & Huber, R. (2015) · SLEEP · doi:10.5665/sleep.4820 · Cited by 92 · see citing works
A role for spindles in the onset of rapid eye movement sleep
Bandarabadi, M., Herrera, C. G., Gent, T. C., Bassetti, C. L., Schindler, K. A., & Adamantidis, A. (2020) · Nature Communications · doi:10.1038/s41467-020-19076-2 · Cited by 92 · see citing works
Ayoub, A., Aumann, D., Hörschelmann, A., Kouchekmanesch, A., Paul, P., Born, J., & Marshall, L. (2013) · Sleep · doi:10.5665/sleep.2722 · Cited by 91 · see citing works
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 88 · see citing works
Memmesheimer, R.-M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909615107 · Cited by 85 · see citing works
Major diencephalic inputs to the hippocampus
Vertes, R. P. (2015) · Progress in brain research · doi:10.1016/bs.pbr.2015.03.008 · Cited by 83 · see citing works
Non-REM Sleep Characteristics Predict Early Cognitive Impairment in an Aging Population
Taillard, J., Sagaspe, P., Berthomier, C., Brandewinder, M., Amieva, H., Dartigues, J., Rainfray, M., Harston, S., Micoulaud‐Franchi, J., & Philip, P. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00197 · Cited by 80 · see citing works
Rapid Generation of Somatic Mouse Mosaics with Locus-Specific, Stably Integrated Transgenic Elements
Kim, G. B., Pacheco, D. R. F., Saxon, D. S., Yang, A., Sabet, S., Dutra‐Clarke, M., Levy, R., Watkins, A., Park, H., Akhtar, A. A., et al. (2019) · Cell · doi:10.1016/j.cell.2019.08.013 · Cited by 72 · see citing works
Temporal associations between sleep slow oscillations, spindles and ripples
Oyanedel, C. N., Durán, E., Niethard, N., Inostroza, M., & Born, J. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14906 · Cited by 71 · see citing works
Characterization of Topographically Specific Sleep Spindles in Mice
Kim, D., Hwang, E., Lee, M., Sung, H., & Choi, J. H. (2014) · SLEEP · doi:10.5665/sleep.4330 · Cited by 61 · see citing works
Yang, M., Logothetis, N. K., & Eschenko, O. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.2107-18.2018 · Cited by 57 · see citing works
Monosynaptic Hippocampal-Prefrontal Projections Contribute to Spatial Memory Consolidation in Mice
Binder, S., Mölle, M., Lippert, M., Bruder, R., Aksamaz, S., Ohl, F. W., Wiegert, J. S., & Marshall, L. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2158-18.2019 · Cited by 55 · see citing works
Jiang, X., González-Martínez, J., & Halgren, E. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2858-18.2019 · Cited by 54 · see citing works
Gardner, R. J., Hughes, S. W., & Jones, M. W. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2197-13.2013 · Cited by 53 · see citing works
Varela, C., & Wilson, M. A. (2020) · eLife · doi:10.7554/elife.48881 · Cited by 52 · see citing works
Shibata, H., & Naito, J. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21523 · Cited by 51 · see citing works
An inhibitory hippocampal–thalamic pathway modulates remote memory retrieval
Vetere, G., Xia, F., Ramsaran, A. I., Tran, L. M., Josselyn, S. A., & Frankland, P. W. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00819-3 · Cited by 51 · see citing works
Precise coupling of the thalamic head-direction system to hippocampal ripples
Viejo, G., & Peyrache, A. (2019) · Nature Communications · doi:10.1038/s41467-020-15842-4 · Cited by 50 · see citing works
A thalamo-cortical neural mass model for the simulation of brain rhythms during sleep
Cona, F., Lacanna, M., & Ursino, M. (2014) · Journal of Computational Neuroscience · doi:10.1007/s10827-013-0493-1 · Cited by 49 · see citing works
Yuan, R. K., Lopez, M. R., Ramos‐Álvarez, M. M., Normandin, M. E., Thomas, A. S., Uygun, D. S., Cerda, V. R., Grenier, A. E., Wood, M. T., Gagliardi, C. M., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109234 · Cited by 41 · see citing works
Bazhenov, M., & Timofeev, I. (2006) · Scholarpedia · doi:10.4249/scholarpedia.1319 · Cited by 34 · see citing works
Azimi, A., Alizadeh, Z., & Ghorbani, M. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.118485 · Cited by 33 · see citing works
Self-citationSpontaneous slow oscillation—slow spindle features predict induced overnight memory retention
Dehnavi, F., Koo, P. C., Ghorbani, M., & Marshall, L. (2021) · SLEEP · doi:10.1093/sleep/zsab127 · Cited by 31 · see citing works
Self-citationSlow spindles are associated with cortical high frequency activity
Hashemi, N. S., Dehnavi, F., Moghimi, S., & Ghorbani, M. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.01.012 · Cited by 31 · see citing works
Self-citationNonlinear-dynamics theory of up-down transitions in neocortical neural networks.
Ghorbani, M., Mehta, M., Bruinsma, R., & Levine, A. (2012) · Physical review. E, Statistical, nonlinear, and soft matter physics · doi:10.1103/physreve.85.021908 · Cited by 28 · see citing works
Self-citationPeyrache, A., Petersen, P., & Buzsáki, G. (2015) · UC Berkeley · doi:10.6080/k0g15xs1 · Cited by 16 · see citing works
Slow spindles are associated with cortical high frequency activity
Ghorbani, M., Hashemi, N. S., Dehnavi, F., & Moghimi, S. (2019) · IBRO Reports · doi:10.1016/j.ibror.2019.07.1678 · Cited by 2 · see citing works
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Sleep—A brain-state serving systems memory consolidation
Brodt, S., Inostroza, M., Niethard, N., & Born, J. (2023) · Neuron · doi:10.1016/j.neuron.2023.03.005 · Cited by 343 · see citing works
Sleep’s contribution to memory formation
Lutz, N. D., Harkotte, M., & Jan Born, A. (2025) · Physiological Reviews · doi:10.1152/physrev.00054.2024 · Cited by 40 · see citing works
Fan, D., Chen, J., Hou, S., Song, Z., Baier, G., & Wang, Q. (2024) · Chaos Solitons & Fractals · doi:10.1016/j.chaos.2024.115754 · Cited by 8 · see citing works
The reuniens nucleus of the thalamus facilitates hippocampo-cortical dialogue during sleep
Basha, D., Azarmehri, A., Proulx, E., Chauvette, S., Ghorbani, M., & Timofeev, I. (2025) · eLife · doi:10.7554/elife.90826.3 · Cited by 3 · see citing works
Self-citationThe reuniens nucleus of the thalamus facilitates hippocampo-cortical dialogue during sleepPreprint
Basha, D., Azarmehri, A., Proulx, E., Chauvette, S., Ghorbani, M., & Timofeev, I. (2023) · eLife · doi:10.7554/elife.90826 · Cited by 3 · see citing works
Self-citationDual regulation of medial septum in the hippocampal transitions from theta to non-theta oscillations
Fan, D., Li, F., Song, Z., & Wang, Q. (2025) · The European Physical Journal Special Topics · doi:10.1140/epjs/s11734-025-01820-8 · Cited by 2 · see citing works
Sriram, S., Natiq, H., Rajagopal, K., Parastesh, F., & Jafari, S. (2023) · International Journal of Bifurcation and Chaos · doi:10.1142/s0218127423501092 · Cited by 2 · see citing works
Song, Z., Fan, D., Hou, S., & Wang, Q. (2024) · Physics Letters A · doi:10.1016/j.physleta.2024.130160 · Cited by 2 · see citing works
The reuniens nucleus of the thalamus facilitates hippocampo-cortical dialogue during sleepPreprint
Basha, D., Azarmehri, A., Proulx, É., Chauvette, S., Ghorbani, M., & Timofeev, I. (2025) · eLife · doi:10.7554/elife.90826.2 · Cited by 1 · see citing works
Self-citationThe reuniens nucleus of the thalamus facilitates hippocampo-cortical dialogue during sleepPreprint
Basha, D., Azarmehri, A., Proulx, É., Chauvette, S., Ghorbani, M., & Timofeev, I. (2023) · eLife · doi:10.7554/elife.90826.1
Self-citationBasha, D., Azarmehri, A., Proulx, É., Chauvette, S., Ghorbani, M., & Timofeev, I. (2023) · eLife · doi:10.7554/elife.90826.1.sa3
Self-citationSleep EEG oscillations and synaptic plasticity in memory consolidation across NREM and REM sleep
Chen, Y., Zhao, M., Cao, X., Zhou, G., & Zhang, Y. (2026) · Dialogues in Clinical Neuroscience · doi:10.1080/19585969.2026.2744744
- Authors
- Alizadeh, Z., Azimi, A., & Ghorbani, M.
- Affiliations
- Ferdowsi University of Mashhad (IR)
- Institute for Advanced Studies in Basic Sciences (IR)
- Corresponding author
- Ghorbani, Maryam
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2022-08-15
- Volume
- 42
- Issue
- 38
- Pages
- 7222-7243
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC9512580
- OpenAlex
- W4291618525
- Cited by
- 14
- References
- 89
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 2 · 2023: 7
- FWCI
- 1.68
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Keywords
- hippocampal ripples, slow oscillations, CA1, memory consolidation, spatial exploration, sleep
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