Coherent theta oscillations and reorganization of spike timing in the hippocampal- prefrontal network upon learning
Open accessAbstract
To study the interplay between hippocampus and medial prefrontal cortex (Pfc) and its importance for learning and memory consolidation, we measured the coherence in theta oscillations between these two structures in rats learning new rules on a Y maze. Coherence peaked at the choice point, most strongly after task rule acquisition. Simultaneously, Pfc pyramidal neurons reorganized their phase, concentrating at hippocampal theta trough, and synchronous cell assemblies emerged. This synchronous state may result from increased inhibition exerted by interneurons on pyramidal cells, as measured by cross-correlation, and could be modulated by dopamine: we found similar hippocampal-Pfc theta coherence increases and neuronal phase shifts following local administration of dopamine in Pfc of anesthetized rats. Pfc cell assemblies emerging during high coherence were preferentially replayed during subsequent sleep, concurrent with hippocampal sharp waves. Thus, hippocampal/prefrontal coherence could lead to synchronization of reward predicting activity in prefrontal networks, tagging it for subsequent memory consolidation.
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?
In rats, prefrontal cell assemblies that fired during learning when EEG theta coherence between prefrontal cortex and hippocampus was increased had increased probability of reactivation during subsequent SWS.
“In rats, prefrontal cell assemblies that fired during learning when EEG theta coherence between the prefrontal cortex and hippocampus was increased showed a distinctly increased probability to be reactivated during subsequent SWS (73).”
From About Sleep's Role in Memory (2013) · cites this paper as [73]
In a reward-based Y-maze learning paradigm, theta coherence between the PFC and hippocampus was increased, especially after rats had learned how to reliably procure food.
“the theta coherence between the PFC and hippocampus was increased, especially after rats had learned how to reliably procure food”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Benchenane et al., 2010
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
Hebb, D. O. (2005) · doi:10.4324/9781410612403 · Cited by 9,825 · see citing works
A neural substrate of prediction and reward
Schultz, W., Dayan, P., & Montague, P. R. (1997) · Science · doi:10.1126/science.275.5306.1593 · Cited by 9,388 · see citing works
Distributed hierarchical processing in the primate cerebral cortex
Felleman, D. J., & Van Essen, D. C. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.1.1 · Cited by 7,783 · see citing works
indicated, N. A. (1950) · Journal of Consulting Psychology · doi:10.1037/h0049612 · Cited by 6,984 · see citing works
McClelland, J. L., McNaughton, B. L., & O'Reilly, R. C. (1995) · Psychological Review · doi:10.1037/0033-295x.102.3.419 · Cited by 5,256 · see citing works
The brainweb: phase synchronization and large-scale integration
Varela, F., Lachaux, J.-P., Rodriguez, E., & Martinerie, J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35067550 · Cited by 4,761 · see citing works
Bi, G.-Q., & Poo, M.-M. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-24-10464.1998 · Cited by 4,744 · see citing works
A mechanism for cognitive dynamics: neuronal communication through neuronal coherence.
Fries, P. (2005) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2005.08.011 · Cited by 4,284 · see citing works
Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs
Markram, H., Lübke, J., Frotscher, M., & Sakmann, B. (1997) · Science · doi:10.1126/science.275.5297.213 · Cited by 3,832 · see citing works
Dynamic predictions: Oscillations and synchrony in top–down processing
Engel, A. K., Fries, P., & Singer, W. (2001) · Nature Reviews Neuroscience · doi:10.1038/35094565 · Cited by 3,454 · see citing works
Theta oscillations in the hippocampus
Buzsáki, G. (2002) · Neuron · doi:10.1016/s0896-6273(02)00586-x · Cited by 3,332 · see citing works
Statistical Analysis of Circular Data.
LANGE, N. D., & Fisher, N. I. (1995) · Journal of the American Statistical Association · doi:10.2307/2291098 · Cited by 2,155 · see citing works
The organization of recent and remote memories
Frankland, P. W., & Bontempi, B. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1607 · Cited by 2,138 · see citing works
Large-scale recording of neuronal ensembles
Buzsáki, G. (2004) · Nature Neuroscience · doi:10.1038/nn1233 · Cited by 1,875 · see citing works
A cortical–hippocampal system for declarative memory
Eichenbaum, H. (2000) · Nature reviews. Neuroscience · doi:10.1038/35036213 · Cited by 1,725 · see citing works
Two-stage model of memory trace formation: A role for “noisy” brain states
Buzsáki, G. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90423-5 · Cited by 1,709 · see citing works
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
Self-citationMedial Frontal Cortex Mediates Perceptual Attentional Set Shifting in the Rat
Birrell, J. M., & Brown, V. J. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-11-04320.2000 · Cited by 1,421 · see citing works
Modulation of Neuronal Interactions Through Neuronal Synchronization
Womelsdorf, T., Schoffelen, J.-M., Oostenveld, R., Singer, W., Desimone, R., Engel, A. K., & Fries, P. (2007) · Science · doi:10.1126/science.1139597 · Cited by 1,367 · 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
Harris, K. D., Henze, D. A., Csicsvari, J. L., Hirase, H., & Buzsáki, G. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.84.1.401 · Cited by 1,153 · see citing works
Analysis of Dynamic Brain Imaging Data
Mitra, P. P., & Pesaran, B. (1999) · Biophysical Journal · doi:10.1016/s0006-3495(99)77236-x · Cited by 1,044 · see citing works
Fries, P., Nikolić, D., & Singer, W. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.05.005 · Cited by 1,044 · see citing works
Entrainment of Neocortical Neurons and Gamma Oscillations by the Hippocampal Theta Rhythm
Sirota, A., Montgomery, S., Fujisawa, S., Isomura, Y., Zugaro, M., & Buzsáki, G. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.014 · Cited by 1,015 · see citing works
Prefrontal phase locking to hippocampal theta oscillations
Siapas, A. G., Lubenov, E. V., & Wilson, M. A. (2005) · Neuron · doi:10.1016/j.neuron.2005.02.028 · Cited by 1,014 · see citing works
Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point
Johnson, A., & Redish, A. D. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3761-07.2007 · Cited by 1,003 · see citing works
Analysis of Dynamic Brain Imaging Data
Mitra, P. P., & Pesaran, B. (1998) · Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) · Cited by 898 · see citing works
Moscovitch, M., Rosenbaum, R. S., Gilboa, A., Addis, D. R., Westmacott, R., Grady, C., McAndrews, M. P., Levine, B., Black, S., Winocur, G., et al. (2005) · Journal of Anatomy · doi:10.1111/j.1469-7580.2005.00421.x · Cited by 893 · see citing works
Barthó, P., Hirase, H., Monconduit, L., Zugaro, M. B., Harris, K. D., & Buzsáki, G. (2004) · Journal of Neurophysiology · doi:10.1152/jn.01170.2003 · Cited by 888 · see citing works
Organization of cell assemblies in the hippocampus
Harris, K. D., Csicsvari, J., Hirase, H., Dragoi, G., & Buzsáki, G. (2003) · Nature · doi:10.1038/nature01834 · Cited by 869 · see citing works
Reward, Motivation, and Reinforcement Learning
Dayan, P., & Balleine, B. W. (2002) · Neuron · doi:10.1016/s0896-6273(02)00963-7 · Cited by 855 · see citing works
Jay, T. M., & Witter, M. P. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903130404 · Cited by 841 · see citing works
Statistical Analysis of Circular Data.
Sprent, P., & Fischer, N. I. (1994) · Journal of Applied Ecology · doi:10.2307/2404554 · Cited by 791 · see citing works
Replay of rule-learning related neural patterns in the prefrontal cortex during sleep
Peyrache, A., Khamassi, M., Benchenane, K., Wiener, S. I., & Battaglia, F. P. (2009) · Nature Neuroscience · doi:10.1038/nn.2337 · Cited by 767 · see citing works
Floresco, S., Seamans, J. K., & Phillips, A. G. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-05-01880.1997 · Cited by 734 · see citing works
Human memory formation is accompanied by rhinal–hippocampal coupling and decoupling
Fell, J., Klaver, P., Lehnertz, K., Grünwald, T., Schaller, C., Elger, C. E., & Fernández, G. (2001) · Nature Neuroscience · doi:10.1038/nn759 · Cited by 692 · see citing works
Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex
Fujisawa, S., Amarasingham, A., Harrison, M. T., & Buzsáki, G. (2008) · Nature Neuroscience · doi:10.1038/nn.2134 · Cited by 679 · see citing works
Doya, K. (2008) · Nature Neuroscience · doi:10.1038/nn2077 · Cited by 642 · see citing works
Hazan, L., Zugaro, M. B., & Buzsáki, G. (2006) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2006.01.017 · Cited by 492 · see citing works
A theory for cerebral neocortex
Marr, D. (1970) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1970.0040 · Cited by 463 · see citing works
Tseng, K. Y., & O'Donnell, P. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1021-04.2004 · Cited by 402 · see citing works
Role of GABAergic inhibition in hippocampal network oscillations
Mann, E. O., & Paulsen, O. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.05.003 · Cited by 389 · see citing works
Gurden, H., Takita, M., & Jay, T. M. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-22-j0003.2000 · Cited by 366 · see citing works
Orientation and Direction Selectivity of Synaptic Inputs in Visual Cortical Neurons
Monier, C., Chavane, F., Baudot, P., Graham, L. J., & Frégnac, Y. (2003) · Neuron · doi:10.1016/s0896-6273(03)00064-3 · Cited by 356 · see citing works
Constantinidis, C., & Goldman-Rakic, P. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00188.2002 · Cited by 337 · see citing works
Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts
Cassenaer, S., & Laurent, G. (2007) · Nature · doi:10.1038/nature05973 · Cited by 331 · see citing works
Gireesh, E. D., & Plenz, D. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0800537105 · Cited by 328 · see citing works
Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep
Poe, G. R., Nitz, D. A., McNaughton, B. L., & Barnes, C. A. (2000) · Brain Research · doi:10.1016/s0006-8993(99)02310-0 · Cited by 318 · see citing works
Blatow, M., Rozov, A., Katona, I., Hormuzdi, S. G., Meyer, A. H., Whittington, M. A., Caputi, A., & Monyer, H. (2003) · Neuron · doi:10.1016/s0896-6273(03)00300-3 · Cited by 316 · see citing works
Hyman, J. M., Zilli, E. A., Paley, A., & Hasselmo, M. E. (2005) · Hippocampus · doi:10.1002/hipo.20106 · Cited by 313 · see citing works
Dynamic Analysis of Learning in Behavioral Experiments
Smith, A. C., Frank, L. M., Wirth, S., Yanike, M., Hu, D., Kubota, Y., Graybiel, A. M., SUZUKI, W. A., & Brown, E. N. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2908-03.2004 · Cited by 313 · see citing works
Covert expectation-of-reward in rat ventral striatum at decision points
van der Meer, M. A. A. (2009) · Frontiers in Integrative Neuroscience · doi:10.3389/neuro.07.001.2009 · Cited by 296 · see citing works
Hippocampal place cell assemblies are speed-controlled oscillators
Geisler, C. E., Robbe, D., Zugaro, M., Sirota, A., & Buzsáki, G. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610121104 · Cited by 273 · see citing works
Couey, J. J., Meredith, R. M., Spijker, S., Poorthuis, R. B., Smit, A. B., Brussaard, A. B., & Mansvelder, H. D. (2007) · Neuron · doi:10.1016/j.neuron.2007.03.006 · Cited by 253 · see citing works
NMDA Receptor Antagonism Blocks Experience-Dependent Expansion of Hippocampal “Place Fields”
Ekstrom, A. D., Meltzer, J., McNaughton, B. L., & Barnes, C. A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00401-9 · Cited by 245 · see citing works
Zhang, J.-C., Lau, P.-M., & Bi, G. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900546106 · Cited by 228 · see citing works
Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm
Jones, M. W., & Wilson, M. A. (2005) · Hippocampus · doi:10.1002/hipo.20119 · Cited by 213 · see citing works
Influence of the hippocampus on interneurons of the rat prefrontal cortex
Tierney, P. L., Dégenètais, E., Thierry, A., Glowinski, J., & Gioanni, Y. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03501.x · Cited by 192 · see citing works
Chapin, J. K., & Nicolelis, M. A. L. (1999) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(99)00130-2 · Cited by 186 · see citing works
Delatour, B., & Gisquet-Verrier, P. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00168-0 · Cited by 170 · see citing works
van der Meer, M. A. A. (2009) · Frontiers in Integrative Neuroscience · doi:10.3389/neuro.07.009.2009 · Cited by 156 · see citing works
Episodic memory and cortico–hippocampal interactions
Shastri, L. (2002) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(02)01868-5 · Cited by 136 · see citing works
Chapman, C. A., & Lacaille, J. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.81.3.1296 · Cited by 135 · see citing works
Peyrache, A., Benchenane, K., Khamassi, M., Wiener, S. I., & Battaglia, F. P. (2009) · Journal of Computational Neuroscience · doi:10.1007/s10827-009-0154-6 · Cited by 134 · see citing works
Dégenètais, E. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.7.782 · Cited by 127 · see citing works
Schreiber, S., Fellous, J., Tiesinga, P. H. E., & B, T. J. S. A. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00556.2003 · Cited by 95 · see citing works
van der Meulen, J. A. J., Joosten, R. N. J. M. A., de Bruin, J. P. C., & Feenstra, M. G. P. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl057 · Cited by 74 · see citing works
Learning-Induced Enduring Changes in Functional Connectivity among Prefrontal Cortical Neurons
Baeg, E. H., Kim, Y. B., Kim, J., Ghim, J.-W., Kim, J. J., & Jung, M. W. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4759-06.2007 · Cited by 59 · see citing works
Dopamine Modulates Temporal Dynamics of Feedforward Inhibition in Rat Prefrontal Cortex In Vivo
Tierney, P. L., Thierry, A. M., Glowinski, J., Deniau, J., & Gioanni, Y. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm252 · Cited by 41 · see citing works
Dopaminergic Modulation of Local Network Activity in Rat Prefrontal Cortex
Bandyopadhyay, S., & Hablitz, J. J. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00898.2006 · Cited by 36 · see citing works
Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways.
Lavenex (2000) · Pure Amsterdam UMC · doi:10.1002/1098-1063(2000)10:4 · Cited by 1 · see citing works
Flagged first, then by citations
1 of the 73 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Dynamic functional connectivity: Promise, issues, and interpretations
Hutchison, R. M., Womelsdorf, T., Allen, E. A., Bandettini, P. A., Calhoun, V. D., Corbetta, M., Della Penna, S., Duyn, J. H., Glover, G. H., Gonzalez-Castillo, J., et al. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.05.079 · Cited by 2,962 · see citing works
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
Frontal theta as a mechanism for cognitive control
Cavanagh, J. F., & Frank, M. J. (2014) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2014.04.012 · Cited by 2,726 · see citing works
The functional role of cross-frequency coupling
Canolty, R. T., & Knight, R. T. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.09.001 · Cited by 2,101 · see citing works
Vinck, M., Oostenveld, R., van Wingerden, M., Battaglia, F., & Pennartz, C. M. A. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.01.055 · Cited by 1,753 · 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
The role of phase synchronization in memory processes
Fell, J., & Axmacher, N. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn2979 · Cited by 1,620 · see citing works
Lisman, J. E., & Jensen, O. (2013) · Neuron · doi:10.1016/j.neuron.2013.03.007 · Cited by 1,609 · see citing works
Neural syntax: cell assemblies, synapsembles, and readers
Buzsáki, G. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.023 · Cited by 1,289 · see citing works
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
Mechanisms of systems memory consolidation during sleep
Klinzing, J. G., Niethard, N., & Born, J. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0467-3 · Cited by 1,176 · see citing works
Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval
Carr, M. F., Jadhav, S. P., & Frank, L. M. (2011) · Nature Neuroscience · doi:10.1038/nn.2732 · Cited by 958 · see citing works
How schema and novelty augment memory formation
van Kesteren, M. T. R., Ruiter, D. J., Fernández, G., & Henson, R. N. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.02.001 · Cited by 860 · see citing works
Prefrontal–hippocampal interactions in episodic memory
Eichenbaum, H. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.74 · Cited by 870 · see citing works
Viewpoints: how the hippocampus contributes to memory, navigation and cognition
Lisman, J., Buzsáki, G., Eichenbaum, H., Nadel, L., Ranganath, C., & Redish, A. D. (2017) · Nature Neuroscience · doi:10.1038/nn.4661 · Cited by 851 · see citing works
The Consolidation and Transformation of Memory
Dudai, Y., Karni, A., & Born, J. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.004 · Cited by 741 · see citing works
The Restless Engram: Consolidations Never End
Dudai, Y. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150500 · Cited by 644 · see citing works
Schema-dependent gene activation and memory encoding in neocortex
Tse, D., Takeuchi, T., Kakeyama, M., Kajii, Y., Okuno, H., Tohyama, C., Bito, H., & Morris, R. G. M. (2011) · Science · doi:10.1126/science.1205274 · Cited by 618 · see citing works
Mechanisms and functions of theta rhythms
Colgin, L. L. (2013) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062012-170330 · Cited by 559 · 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
Exploration versus exploitation in space, mind, and society
Hills, T. T., Todd, P. M., Lazer, D. M. J., Redish, A. D., & Couzin, I. D. (2014) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2014.10.004 · Cited by 552 · see citing works
Neural Basis of Reinforcement Learning and Decision Making
Lee, D., Seo, H., & Jung, M. W. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150512 · Cited by 542 · see citing works
Prefrontal parvalbumin interneurons shape neuronal activity to drive fear expression
Courtin, J., Chaudun, F., Rozeske, R. R., Karalis, N., Gonzalez-Campo, C., Wurtz, H., Abdi, A., Baufreton, J., Bienvenu, T. C. M., & Herry, C. (2014) · Nature · doi:10.1038/nature12755 · Cited by 524 · see citing works
Hsieh, L.-T., & Ranganath, C. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2013.08.003 · Cited by 525 · see citing works
A 4 Hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities
Fujisawa, S., & Buzsáki, G. (2011) · Neuron · doi:10.1016/j.neuron.2011.08.018 · Cited by 501 · see citing works
Redish, A. D. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2015.30 · Cited by 463 · see citing works
Encoding of fear learning and memory in distributed neuronal circuits
Herry, C., & Johansen, J. P. (2014) · Nature Neuroscience · doi:10.1038/nn.3869 · Cited by 474 · see citing works
A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP
Lisman, J., Grace, A. A., & Duzel, E. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.07.006 · Cited by 465 · see citing works
Brain circuit dysfunction in post-traumatic stress disorder: from mouse to man
Fenster, R. J., Lebois, L. A. M., Ressler, K. J., & Suh, J. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0039-7 · Cited by 456 · see citing works
The hippocampal–prefrontal pathway: The weak link in psychiatric disorders?
Godsil, B. P., Kiss, J., Spedding, M., & Jay, T. M. (2013) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2012.10.018 · Cited by 434 · see citing works
Hippocampal theta sequences reflect current goals
Wikenheiser, A. M., & Redish, A. D. (2015) · Nature Neuroscience · doi:10.1038/nn.3909 · Cited by 367 · see citing works
4-Hz oscillations synchronize prefrontal–amygdala circuits during fear behavior
Karalis, N., Déjean, C., Chaudun, F., Khoder, S., Rozeske, R. R., Wurtz, H., Bagur, S., Benchenane, K., Sirota, A., Courtin, J., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4251 · Cited by 379 · see citing works
Oscillations in the prefrontal cortex: a gateway to memory and attention
Benchenane, K., Tiesinga, P. H., & Battaglia, F. P. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.01.004 · Cited by 366 · see citing works
Self-citationPreservation of a remote fear memory requires new myelin formation
Pan, S., Mayoral, S. R., Choi, H. S., Chan, J. R., & Kheirbek, M. A. (2020) · Nature Neuroscience · doi:10.1038/s41593-019-0582-1 · Cited by 366 · 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
Hippocampal-Prefrontal Interactions in Cognition, Behavior and Psychiatric Disease
Sigurdsson, T., & Duvarci, S. (2016) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00190 · Cited by 309 · see citing works
Oscillations and hippocampal-prefrontal synchrony
Colgin, L. L. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.04.006 · Cited by 299 · see citing works
Identification of a Functional Connectome for Long-Term Fear Memory in Mice
Wheeler, A. L., Teixeira, C. M., Wang, A. H., Xiong, X., Kovacevic, N., Lerch, J. P., McIntosh, A. R., Parkinson, J., & Frankland, P. W. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002853 · Cited by 315 · see citing works
Prefrontal-Hippocampal Interactions in Memory and Emotion
Jin, J., & Maren, S. (2015) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00170 · Cited by 313 · see citing works
“Medial prefrontal cortex firing lags behind the hippocampal LFP, suggesting that information flow is from the HPC to mPFC (Hyman et al., 2005, 2010; Jones and Wilson, 2005; Siapas et al., 2005; Benchenane et al., 2010; Sigurdsson et al., 2010).”
BackgroundNovelty and Dopaminergic Modulation of Memory Persistence: A Tale of Two Systems
Duszkiewicz, A. J., McNamara, C. G., Takeuchi, T., & Genzel, L. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.10.002 · Cited by 307 · see citing works
Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval
Watrous, A. J., Tandon, N., Conner, C. R., Pieters, T., & Ekstrom, A. D. (2013) · Nature Neuroscience · doi:10.1038/nn.3315 · Cited by 296 · see citing works
O’Neill, P.-K., Gordon, J. A., & Sigurdsson, T. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2378-13.2013 · Cited by 294 · see citing works
Communication between Brain Areas Based on Nested Oscillations
Bonnefond, M., Kästner, S., & Jensen, O. B. (2017) · eNeuro · doi:10.1523/eneuro.0153-16.2017 · Cited by 270 · see citing works
Bocchio, M., Nabavi, S., & Capogna, M. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.022 · Cited by 260 · see citing works
Sleep for Preserving and Transforming Episodic Memory
Inostroza, M., & Jan Born, A. (2013) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062012-170429 · Cited by 265 · see citing works
Ekstrom, A. D., Arnold, A. E. G. F., & Iaria, G. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00803 · Cited by 263 · see citing works
Memory: organization and control.
Eichenbaum, H. (2017) · Annual Review of Psychology · doi:10.1146/annurev-psych-010416-044131 · Cited by 257 · see citing works
Synchronous and asynchronous theta and gamma activity during episodic memory formation
Burke, J. F., Zaghloul, K. A., Jacobs, J., Williams, R. B., Sperling, M. R., Sharan, A. D., & Kahana, M. J. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2057-12.2013 · Cited by 250 · see citing works
Jadhav, S. P., Rothschild, G., Roumis, D. K., & Frank, L. M. (2016) · Neuron · doi:10.1016/j.neuron.2016.02.010 · Cited by 250 · see citing works
Johnson, L. A., Alekseichuk, I., Krieg, J. D. S., Doyle, A. M., Yu, Y., Vitek, J. L., Johnson, M. D., & Opitz, A. (2020) · Science Advances · doi:10.1126/sciadv.aaz2747 · Cited by 230 · see citing works
Theta Phase Precession in Rat Ventral Striatum Links Place and Reward Information
van der Meer, M. A. A., & Redish, A. D. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4869-10.2011 · Cited by 222 · 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
Ognjanovski, N., Schaeffer, S. M., Wu, J., Mofakham, S., Maruyama, D., Żochowski, M., & Aton, S. J. (2017) · Nature Communications · doi:10.1038/ncomms15039 · Cited by 221 · see citing works
van Kesteren, M. T. R., Rijpkema, M., Ruiter, D. J., & Fernández, G. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2674-10.2010 · Cited by 224 · see citing works
Prestimulus theta activity predicts correct source memory retrieval
Addante, R. J., Watrous, A. J., Yonelinas, A. P., Ekstrom, A. D., & Ranganath, C. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1014528108 · Cited by 204 · see citing works
Neural Oscillations Associated with Item and Temporal Order Maintenance in Working Memory
Hsieh, L., Ekstrom, A. D., & Ranganath, C. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0828-11.2011 · Cited by 219 · see citing works
Shin, J. D., Tang, W., & Jadhav, S. P. (2019) · Neuron · doi:10.1016/j.neuron.2019.09.012 · Cited by 199 · see citing works
Contextual encoding by ensembles of medial prefrontal cortex neurons
Hyman, J. M., Ma, L., Balaguer‐Ballester, E., Durstewitz, D., & Seamans, J. K. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114415109 · Cited by 222 · see citing works
Surge of neurophysiological coherence and connectivity in the dying brain
Borjigin, J., Lee, U., Liu, T., Pal, D., Huff, S., Klarr, D., Sloboda, J., Hernandez, J., Wang, M. M., & Mashour, G. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1308285110 · Cited by 219 · see citing works
der Weel, M. J. D.-V., Griffin, A. L., Ito, H., Shapiro, M. L., Witter, M. P., Vertes, R. P., & Allen, T. A. (2019) · Learning & Memory · doi:10.1101/lm.048389.118 · Cited by 201 · see citing works
Bidirectional prefrontal-hippocampal interactions support context-guided memory
Place, R., Farovik, A., Brockmann, M., & Eichenbaum, H. (2016) · Nature Neuroscience · doi:10.1038/nn.4327 · Cited by 200 · see citing works
The research domain criteria framework: The case for anterior cingulate cortex
Holroyd, C. B., & Umemoto, A. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.09.021 · Cited by 187 · see citing works
Detecting cell assemblies in large neuronal populations
Lopes‐dos‐Santos, V., Ribeiro, S. T. G., & Tort, A. B. L. (2013) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2013.04.010 · Cited by 176 · see citing works
Slow oscillations in two pairs of dopaminergic neurons gate long-term memory formation in Drosophila
Plaçais, P.-Y., Trannoy, S., Isabel, G., Aso, Y., Siwanowicz, I., Belliart-Guérin, G., Vernier, P., Birman, S., Tanimoto, H., & Préat, T. (2012) · Nature Neuroscience · doi:10.1038/nn.3055 · Cited by 178 · see citing works
Gruber, A. J., & McDonald, R. J. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00050 · Cited by 173 · see citing works
Building on Prior Knowledge: Schema-dependent Encoding Processes Relate to Academic Performance
van Kesteren, M. T. R., Rijpkema, M., Ruiter, D. J., Morris, R., & Fernández, G. (2014) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00630 · Cited by 169 · see citing works
Hippocampal 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
Long-Range Neural Synchrony in Behavior
Harris, A. Z., & Gordon, J. A. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-034111 · Cited by 165 · see citing works
Parallel detection of theta and respiration-coupled oscillations throughout the mouse brain
Tort, A. B. L., Ponsel, S., Jessberger, J., Yanovsky, Y., Brankačk, J., & Draguhn, A. (2018) · Scientific Reports · doi:10.1038/s41598-018-24629-z · Cited by 159 · see citing works
Merre, P. L., Esmaeili, V., Charrière, E., Galan, K., Salin, P. A., Petersen, C. C. H., & Crochet, S. (2017) · Neuron · doi:10.1016/j.neuron.2017.11.031 · Cited by 164 · see citing works
Oscillations and hippocampal–prefrontal synchrony
Gordon, J. A. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.02.012 · Cited by 159 · see citing works
Chao, O. Y., de Souza Silva, M. A., Yang, Y.-M., & Huston, J. P. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.04.007 · Cited by 158 · see citing works
Prefrontal microcircuit underlies contextual learning after hippocampal loss
Zelikowsky, M., Bissière, S., Hast, T. A., Bennett, R. Z., Abdipranoto, A., Vissel, B., & Fanselow, M. S. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301691110 · Cited by 156 · see citing works
How the amygdala affects emotional memory by altering brain network properties.
Hermans, E., Battaglia, F., Atsak, P., de Voogd, L. D., Fernández, G., & Roozendaal, B. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.02.005 · Cited by 152 · see citing works
Murty, V. P., & Adcock, R. A. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht063 · Cited by 159 · see citing works
Disconnection and reconnection: The morphological basis of (mal)adaptation to stress
Sousa, N., & Almeida, O. F. X. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.08.006 · Cited by 159 · see citing works
Reset of hippocampal–prefrontal circuitry facilitates learning
Park, A. J., Harris, A. Z., Martyniuk, K. M., Chang, C., Abbas, A. I., Lowes, D. C., Kellendonk, C., Gogos, J. A., & Gordon, J. A. (2021) · Nature · doi:10.1038/s41586-021-03272-1 · Cited by 153 · see citing works
Voloh, B., Valiante, T. A., Everling, S., & Womelsdorf, T. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1500438112 · Cited by 157 · see citing works
Selective Theta-Synchronization of Choice-Relevant Information Subserves Goal-Directed Behavior
Womelsdorf, T., Vinck, M. A., Leung, L.-W. S., & Everling, S. (2010) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2010.00210 · Cited by 157 · see citing works
Sosa, M., & Giocomo, L. M. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00479-z · Cited by 142 · see citing works
Improved measures of phase-coupling between spikes and the Local Field Potential
Vinck, M. A., Battaglia, F. P., Womelsdorf, T., & Pennartz, C. M. A. (2011) · Journal of Computational Neuroscience · doi:10.1007/s10827-011-0374-4 · Cited by 145 · see citing works
The Role of Prefrontal Dopamine D1 Receptors in the Neural Mechanisms of Associative Learning
Puig, M. V., & Miller, E. K. (2012) · Neuron · doi:10.1016/j.neuron.2012.04.018 · Cited by 146 · see citing works
Frontal Midline Theta Reflects Individual Task Performance in a Working Memory Task
Maurer, U., Brem, S., Liechti, M. D., Maurizio, S., Michels, L., & Brandeis, D. (2014) · Brain Topography · doi:10.1007/s10548-014-0361-y · Cited by 143 · see citing works
Movement-Related Theta Rhythm in Humans: Coordinating Self-Directed Hippocampal Learning
Kaplan, R., Doeller, C. F., Barnes, G. R., Vladimir Litvak, A., Düzel, E., Bandettini, P. A., & Burgess, N. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001267 · Cited by 141 · see citing works
Oscillatory activity during maintenance of spatial and temporal information in working memory
Roberts, B. M., Hsieh, L., & Ranganath, C. (2012) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2012.10.009 · Cited by 139 · see citing works
Prefrontal dopamine in associative learning and memory
Puig, M. V., Antzoulatos, E. G., & Miller, E. K. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.09.026 · Cited by 138 · see citing works
Replay of behavioral sequences in the medial prefrontal cortex during rule switching
Kaefer, K., Nardin, M., Blahna, K., & Csicsvari, J. (2020) · Neuron · doi:10.1016/j.neuron.2020.01.015 · Cited by 120 · 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
Medial prefrontal theta phase coupling during spatial memory retrieval
Kaplan, R., Bush, D., Bonnefond, M., Bandettini, P. A., Barnes, G. R., Doeller, C. F., & Burgess, N. (2014) · Hippocampus · doi:10.1002/hipo.22255 · Cited by 138 · see citing works
Drew, L., Crabtree, G. W., Markx, S., Stark, K. L., Chaverneff, F., Xu, B., Mukai, J., Fénelon, K., Hsu, P.-K., Gogos, J. A., et al. (2010) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2010.09.007 · Cited by 137 · see citing works
The brain in motion: How ensemble fluidity drives memory-updating and flexibility
Mau, W., Hasselmo, M. E., & Cai, D. J. (2020) · eLife · doi:10.7554/elife.63550 · Cited by 139 · see citing works
Li, M., Long, C., & Yang, L. (2015) · BioMed Research International · doi:10.1155/2015/810548 · Cited by 137 · see citing works
Two sources of dopamine for the hippocampus
McNamara, C. G., & Dupret, D. (2017) · Trends in Neurosciences · doi:10.1016/j.tins.2017.05.005 · Cited by 135 · see citing works
The rhythm of memory: how breathing shapes memory function
Heck, D. H., Kozma, R., & Kay, L. M. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00200.2019 · Cited by 134 · see citing works
Neural circuits underlying the generation of theta oscillations
Pignatelli, M., Beyeler, A., & Leinekugel, X. (2011) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2011.09.007 · Cited by 124 · see citing works
Poe, G. R. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0820-16.2017 · Cited by 130 · see citing works
Separate elements of episodic memory subserved by distinct hippocampal-prefrontal connections
Barker, G. R. I., Banks, P. J., Scott, H., Ralph, G. S., Mitrophanous, K. A., Wong, L.-F., Bashir, Z. I., Uney, J. B., & Warburton, E. C. (2017) · Nature Neuroscience · doi:10.1038/nn.4472 · Cited by 124 · see citing works
Multiple time-scales of decision-making in the hippocampus and prefrontal cortex
Tang, W., Shin, J. D., & Jadhav, S. P. (2021) · eLife · doi:10.7554/elife.66227 · Cited by 134 · see citing works
Expected reward modulates encoding-related theta activity before an event
Gruber, M. J., Watrous, A. J., Ekstrom, A. D., Ranganath, C., & Otten, L. J. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2012.07.064 · Cited by 108 · see citing works
Thalamic pathways underlying prefrontal cortex–medial temporal lobe oscillatory interactions
Ketz, N., Jensen, O. B., & O’Reilly, R. C. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.09.007 · Cited by 117 · see citing works
- Authors
- Benchenane, K., Peyrache, A., Khamassi, M., Tierney, P. L., Gioanni, Y., Battaglia, F. P., & Wiener, S. I.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- McGovern Institute for Brain Research (US)
- Inserm (FR)
- Corresponding author
- Benchenane, Karim
- Battaglia, Francesco P.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2010-06
- Volume
- 66
- Issue
- 6
- Pages
- 921-936
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2130674184
- Cited by
- 872
- References
- 73
- Citations by year
- 2026: 35 · 2025: 53 · 2024: 55 · 2023: 41 · 2022: 45 · 2021: 70 · 2020: 65 · 2019: 49 · 2018: 61 · 2017: 88 · 2016: 57 · 2015: 60 · 2014: 55 · 2013: 57 · 2012: 34
- FWCI
- 26.57
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- UvA-DARE (University of Amsterdam) (publishedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- HAL (submittedVersion, other-oa)
- UvA-DARE (University of Amsterdam) (submittedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Elsevier eBooks
- Funders
- Johns Hopkins University
- Fondation Fyssen
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- hippocampus, medial prefrontal cortex, theta oscillations, neural coherence, spike timing, rule induction, Y-maze, memory consolidation, dopamine, interneurons, pyramidal neurons, sharp-wave ripples, reward prediction
- MeSH terms
- Action Potentials, Animals, Behavior, Animal, Dopamine, Hippocampus, Male, Neural Inhibition, Neural Pathways, Neurons, Periodicity, Reward, Spectrum Analysis, Time Factors, Prefrontal Cortex, Maze Learning, Rats, Long-Evans, Principal Component Analysis, 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
