A 4 Hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities
Open accessAbstract
Network oscillations support transient communication across brain structures. We show here, in rats, that task-related neuronal activity in the medial prefrontal cortex (PFC), the hippocampus, and the ventral tegmental area (VTA), regions critical for working memory, is coordinated by a 4 Hz oscillation. A prominent increase of power and coherence of the 4 Hz oscillation in the PFC and the VTA and its phase modulation of gamma power in both structures was present in the working memory part of the task. Subsets of both PFC and hippocampal neurons predicted the turn choices of the rat. The goal-predicting PFC pyramidal neurons were more strongly phase locked to both 4 Hz and hippocampal theta oscillations than nonpredicting cells. The 4 Hz and theta oscillations were phase coupled and jointly modulated both gamma waves and neuronal spikes in the PFC, the VTA, and the hippocampus. Thus, multiplexed timing mechanisms in the PFC-VTA-hippocampus axis may support processing of information, including working memory.
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?
An oscillation varying between 2-5 Hz could also be involved in PFC-hippocampus coupling.
“an oscillation varying between 2–5 Hz could also be involved in the PFC-hippocampus coupling”
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 Fujisawa and Buzsaki, 2011
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
An Integrative Theory of Prefrontal Cortex Function
Miller, E. K., & Cohen, J. D. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.167 · Cited by 12,803 · see citing works
Working memory: Looking back and looking forward
Baddeley, A. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1201 · Cited by 5,200 · see citing works
Gray, C. M., König, P., Engel, A. K., & Singer, W. (1989) · Nature · doi:10.1038/338334a0 · Cited by 4,183 · see citing works
Thalamocortical oscillations in the sleeping and aroused brain
Steriade, M., McCormick, D. A., & Sejnowski, T. J. (1993) · Science · doi:10.1126/science.8235588 · Cited by 3,564 · 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
Self-citationCellular basis of working memory
Goldman-Rakic, P. S. (1995) · Neuron · doi:10.1016/0896-6273(95)90304-6 · Cited by 2,663 · see citing works
High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex
Canolty, R. T., Edwards, E., Dalal, S. S., Soltani, M., Nagarajan, S. S., Kirsch, H. E., Berger, M. S., Barbaro, N. M., & Knight, R. T. (2006) · Science · doi:10.1126/science.1128115 · Cited by 2,650 · see citing works
Fuster, J. M. (1997) · Cited by 2,095 · see citing works
The hippocampal-VTA loop: controlling the entry of information into long-term memory
Lisman, J. E., & Grace, A. A. (2005) · Neuron · doi:10.1016/j.neuron.2005.05.002 · Cited by 1,983 · see citing works
Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection
Lakatos, P., Karmos, G., Mehta, A. D., Ulbert, I., & Schroeder, C. E. (2008) · Science · doi:10.1126/science.1154735 · Cited by 1,719 · see citing works
Behavioral Theories and the Neurophysiology of Reward
Schultz, W. (2006) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070229 · Cited by 1,637 · see citing works
Gevins, A. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.4.374 · Cited by 1,623 · see citing works
Modulation of memory fields by dopamine Dl receptors in prefrontal cortex
Williams, G. V., & Goldman-Rakic, P. S. (1995) · Nature · doi:10.1038/376572a0 · Cited by 1,593 · see citing works
Frontal theta activity in humans increases with memory load in a working memory task
Jensen, O., & Tesche, C. D. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.01975.x · Cited by 1,379 · see citing works
Internally Generated Cell Assembly Sequences in the Rat Hippocampus
Pastalkova, E., Itskov, V., Amarasingham, A., & Buzsáki, G. (2008) · Science · doi:10.1126/science.1159775 · Cited by 1,301 · see citing works
Self-citationTheta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task
Jones, M. W., & Wilson, M. A. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030402 · Cited by 1,036 · 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
Self-citationPrefrontal 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
Wood, E. R., Dudchenko, P. A., Robitsek, R. J., & Eichenbaum, H. (2000) · Neuron · doi:10.1016/s0896-6273(00)00071-4 · Cited by 992 · see citing works
Carr, D. B., & Sesack, S. R. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-10-03864.2000 · Cited by 880 · see citing works
Benchenane, K., Peyrache, A., Khamassi, M., Tierney, P. L., Gioanni, Y., Battaglia, F. P., & Wiener, S. I. (2010) · Neuron · doi:10.1016/j.neuron.2010.05.013 · Cited by 872 · see citing works
Control mechanisms in working memory: A possible function of EEG theta oscillations
Sauseng, P., Griesmayr, B., Freunberger, R., & Klimesch, W. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.12.006 · Cited by 853 · see citing works
Frontal midline EEG dynamics during working memory
Onton, J., Arnaud Delorme, A., & Makeig, S. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.04.014 · Cited by 846 · see citing works
Tort, A. B. L., Kramer, M., Thorn, C. A., Gibson, D. J., Kubota, Y., Graybiel, A. M., & Kopell, N. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810524105 · Cited by 842 · see citing works
Gating of human theta oscillations by a working memory task
Raghavachari, S., Kahana, M. J., Rizzuto, D. S., Caplan, J. B., Kirschen, M. P., Bourgeois, B., Madsen, J. R., & Lisman, J. E. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-09-03175.2001 · Cited by 792 · see citing works
Gamma Oscillations Correlate with Working Memory Load in Humans
Howard, M. W. (2003) · Cerebral Cortex · doi:10.1093/cercor/bhg084 · Cited by 766 · see citing works
Trajectory Encoding in the Hippocampus and Entorhinal Cortex
Frank, L. M., Brown, E. N., & Wilson, M. A. (2000) · Neuron · doi:10.1016/s0896-6273(00)00018-0 · Cited by 731 · see citing works
Synchronization between prefrontal and posterior association cortex during human working memory
Sarnthein, J., Petsche, H., Rappelsberger, P., Shaw, G. L., & von Stein, A. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.12.7092 · Cited by 723 · see citing works
Impaired hippocampal–prefrontal synchrony in a genetic mouse model of schizophrenia
Sigurdsson, T., Stark, K. L., Karayiorgou, M., Gogos, J. A., & Gordon, J. A. (2010) · Nature · doi:10.1038/nature08855 · Cited by 702 · 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
Self-citationHuman memory strength is predicted by theta-frequency phase-locking of single neurons
Rutishauser, U., Ross, I. B., Mamelak, A. N., & Schuman, E. M. (2010) · Nature · doi:10.1038/nature08860 · Cited by 622 · see citing works
Start/stop signals emerge in nigrostriatal circuits during sequence learning
Jin, X., & Costa, R. M. (2010) · Nature · doi:10.1038/nature09263 · Cited by 611 · see citing works
Phase-dependent neuronal coding of objects in short-term memory
Siegel, M., Warden, M. R., & Miller, E. K. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908193106 · Cited by 573 · see citing works
Frontal-midline theta from the perspective of hippocampal “theta”
Mitchell, D. J., McNaughton, N., Flanagan, D., & Kirk, I. J. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2008.09.005 · Cited by 549 · see citing works
Başar‐Eroğlu, C., Başar, E., Demıralp, T., & Schürmann, M. (1992) · International Journal of Psychophysiology · doi:10.1016/0167-8760(92)90055-g · Cited by 545 · see citing works
Oscillatory Entrainment of Striatal Neurons in Freely Moving Rats
Berke, J. D., Okatan, M., Skurski, J., & Eichenbaum, H. (2004) · Neuron · doi:10.1016/j.neuron.2004.08.035 · Cited by 507 · see citing works
Firing modes of midbrain dopamine cells in the freely moving rat
Hyland, B. I., Reynolds, J. N. J., HAY, J. G., Perk, C. G., & Miller, R. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00267-1 · Cited by 487 · see citing works
The pairwise phase consistency: A bias-free measure of rhythmic neuronal synchronization
Vinck, M. A., van Wingerden, M., Womelsdorf, T., Fries, P., & Pennartz, C. M. A. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.01.073 · Cited by 483 · see citing works
Influence of Reward Delays on Responses of Dopamine Neurons
Kobayashi, S., & Schultz, W. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1600-08.2008 · Cited by 431 · see citing works
Linking context with reward: a functional circuit from hippocampal CA3 to ventral tegmental area
Luo, A. H., Tahsili-Fahadan, P., Wise, R. A., Lupica, C. R., & Aston-Jones, G. (2011) · Science · doi:10.1126/science.1204622 · Cited by 425 · see citing works
Theta and gamma coordination of hippocampal networks during waking and rapid eye movement sleep.
Montgomery, S. M., Sirota, A., & Buzsaki, G. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1227-08.2008 · Cited by 371 · see citing works
Self-citationDistinct Representations and Theta Dynamics in Dorsal and Ventral Hippocampus
Royer, S., Sirota, A., Patel, J., & Buzsáki, G. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4681-09.2010 · Cited by 351 · see citing works
Self-citationMesocorticolimbic Glutamatergic Pathway
Yamaguchi, T., Wang, H.-L., Li, X., Ng, T. H., & Morales, M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1598-11.2011 · Cited by 332 · 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
Lewis, B. L. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.12.1168 · Cited by 287 · see citing works
Theta synchronization during episodic retrieval: neural correlates of conscious awareness
Klimesch, W., Doppelmayr, M., Yonelinas, A., Kroll, N. E. A., Lazzara, M., Röhm, D., & Gruber, W. (2001) · Cognitive Brain Research · doi:10.1016/s0926-6410(01)00024-6 · Cited by 266 · see citing works
Relationship between hippocampal theta activity and running speed in the rat.
McFarland, W. L., Teitelbaum, H., & Hedges, E. K. (1975) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0076177 · Cited by 237 · see citing works
Involvement of GABAergic and cholinergic medial septal neurons in hippocampal theta rhythm
Yoder, R. M., & Pang, K. C. H. (2005) · Hippocampus · doi:10.1002/hipo.20062 · Cited by 237 · see citing works
Increase of Extracellular Dopamine in Primate Prefrontal Cortex During a Working Memory Task
Watanabe, M., Kodama, T., & Hikosaka, K. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.5.2795 · Cited by 236 · see citing works
Mesocortical Dopamine Neurons Operate in Distinct Temporal Domains Using Multimodal Signaling
Lavin, A., Nogueira, L., Lapish, C. C., Wightman, R. M., Phillips, P. E. M., & Seamans, J. K. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.0557-05.2005 · Cited by 233 · see citing works
Stevens, R., & Cowey, A. (1973) · Brain Research · doi:10.1016/0006-8993(73)90659-8 · Cited by 232 · see citing works
Dopamine Neurons Mediate a Fast Excitatory Signal via Their Glutamatergic Synapses
Chuhma, N., Zhang, H., Masson, J., Zhuang, X., Sulzer, D. L., Hen, R., & Rayport, S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4317-03.2004 · Cited by 228 · see citing works
Theta-Coupled Periodic Replay in Working Memory
Fuentemilla, L., Penny, W. D., Cashdollar, N., Bunzeck, N., & Düzel, E. (2010) · Current Biology · doi:10.1016/j.cub.2010.01.057 · Cited by 216 · see citing works
Statistics of Midbrain Dopamine Neuron Spike Trains in the Awake Primate
Bayer, H. M., Lau, B., & Glimcher, P. W. (2007) · Journal of Neurophysiology · doi:10.1152/jn.01140.2006 · Cited by 184 · see citing works
Theta Modulation in the Medial and the Lateral Entorhinal Cortices
Deshmukh, S. S., Yoganarasimha, D., Voicu, H., & Knierim, J. J. (2010) · Journal of Neurophysiology · doi:10.1152/jn.01141.2009 · Cited by 149 · see citing works
Gaykema, R. P. A., & Záborszky, L. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19961028)374:4 · Cited by 103 · see citing works
Divac, I., Wikmark, R. G. E., & Gade, A. (1975) · Physiological Psychology · doi:10.3758/bf03326820 · Cited by 100 · see citing works
Lithium Ameliorates Nucleus Accumbens Phase-Signaling Dysfunction in a Genetic Mouse Model of Mania
Dzirasa, K., Coque, L., Sidor, M. M., Kumar, S., Dancy, E. A., Takahashi, J. S., McClung, C. A., & Nicolelis, M. A. L. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4289-10.2010 · Cited by 85 · see citing works
Chou, Y.-H., Halldin, C., & Farde, L. (2000) · Synapse · doi:10.1002/1098-2396(200011)38:2 · Cited by 57 · see citing works
Fitch, T. E., Sahr, R. N., Eastwood, B. J., Zhou, F., & Yang, C. R. (2006) · Journal of Neurophysiology · doi:10.1152/jn.01210.2005 · Cited by 45 · see citing works
Iravani, M. M., Muscat, R., & Kruk, Z. L. (1999) · Synapse · doi:10.1002/(sici)1098-2396(19990601)32:3 · Cited by 27 · see citing works
Frontal Lobe: Mental Functions and EEG
Mizuki, Y. (1987) · American Journal of EEG Technology · doi:10.1080/00029238.1987.11080219 · Cited by 23 · see citing works
Koós, T. Z., Tecuapetla, F., & Tepper, J. M. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.05.010 · Cited by 22 · see citing works
Flagged first, then by citations
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
Mechanisms of Gamma Oscillations
Buzsáki, G., & Wang, X.-J. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150444 · Cited by 2,796 · see citing works
Self-citationRasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
“Thus theta coherence in the prefrontal-hippocampal circuitry during the encoding of explicit memories might be a critical factor that tags these memories for later consolidation during sleep, with the prefrontal-hippocampal circuitry integrating also emotional and reward-predicting aspects of the encoded events (74, 4…”
BackgroundCanonical Microcircuits for Predictive Coding
Bastos, A. M., Usrey, W. M., Adams, R. A., Mangun, G. R., Fries, P., & Friston, K. J. (2012) · Neuron · doi:10.1016/j.neuron.2012.10.038 · Cited by 2,421 · see citing works
“, 1989; Singer, 1999), while others have emphasized inter-areal phase-synchronization or coherence (Varela et al., 2001; Fries, 2005; Fujisawa and Buzsáki, 2011).”
BackgroundThe 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
Lisman, J. E., & Jensen, O. (2013) · Neuron · doi:10.1016/j.neuron.2013.03.007 · Cited by 1,609 · 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
Self-citationGABA Neurons of the VTA Drive Conditioned Place Aversion
Tan, K. R., Yvon, C., Turiault, M., Mirzabekov, J. J., Doehner, J., Labouèbe, G., Deisseroth, K. A., Tye, K. M., & Lüscher, C. (2012) · Neuron · doi:10.1016/j.neuron.2012.02.015 · Cited by 635 · see citing works
Voytek, B., & Knight, R. T. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.04.016 · Cited by 556 · 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
Self-citationThe 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
Learning-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
Self-citationRidder, D. D., Vanneste, S., Weisz, N., Londero, A., Schlee, W., Elgoyhen, A. B., & Langguth, B. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.03.021 · Cited by 395 · see citing works
Respiration-Entrained Brain Rhythms Are Global but Often Overlooked
Tort, A. B. L., Brankačk, J., & Draguhn, A. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.01.007 · Cited by 335 · 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
Alekseichuk, I., Turi, Z., de Lara, G., Antal, A., & Paulus, W. (2016) · Current Biology · doi:10.1016/j.cub.2016.04.035 · Cited by 369 · see citing works
Feingold, J., Gibson, D. J., DePasquale, B., & Graybiel, A. M. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1517629112 · Cited by 370 · 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
Over the river, through the woods: cognitive maps in the hippocampus and orbitofrontal cortex
Wikenheiser, A. M., & Schoenbaum, G. M. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.56 · Cited by 353 · see citing works
Measuring macroscopic brain connections in vivo
Jbabdi, S., Sotiropoulos, S. N., Haber, S. N., Van Essen, D. C., & Behrens, T. E. (2015) · Nature Neuroscience · doi:10.1038/nn.4134 · Cited by 334 · 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
Beyond the Connectome: The Dynome
Kopell, N., Gritton, H. J., Whittington, M. A., & Kramer, M. (2014) · Neuron · doi:10.1016/j.neuron.2014.08.016 · Cited by 316 · 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
Jacobs, J. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0304 · Cited by 259 · 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
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
Bosman, C. A., Lansink, C. S., & Pennartz, C. M. A. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12606 · Cited by 225 · see citing works
Prefrontal neuronal assemblies temporally control fear behaviour
Déjean, C., Courtin, J., Karalis, N., Chaudun, F., Wurtz, H., Bienvenu, T., & Herry, C. (2016) · Nature · doi:10.1038/nature18630 · Cited by 216 · see citing works
VTA neurons coordinate with the hippocampal reactivation of spatial experience
Gomperts, S. N., Kloosterman, F., & Wilson, M. A. (2015) · eLife · doi:10.7554/elife.05360 · Cited by 191 · see citing works
Medial Prefrontal Cortex Reduces Memory Interference by Modifying Hippocampal Encoding
Guise, K. G., & Shapiro, M. L. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.011 · Cited by 202 · see citing works
Organization of prefrontal network activity by respiration-related oscillations
Biskamp, J., Bartos, M., & Sauer, J.-F. (2017) · Scientific Reports · doi:10.1038/srep45508 · Cited by 197 · see citing works
Slow Oscillations in the Mouse Hippocampus Entrained by Nasal Respiration
Yanovsky, Y., Ciatipis, M., Draguhn, A., Tort, A. B. L., & Brankačk, J. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.5287-13.2014 · Cited by 175 · see citing works
Selective entrainment of gamma subbands by different slow network oscillations
Zhong, W., Ciatipis, M., Wolfenstetter, T., Jessberger, J., Müller, C., Ponsel, S., Yanovsky, Y., Brankačk, J., Tort, A. B. L., & Draguhn, A. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1617249114 · Cited by 155 · see citing works
The potential role of dopamine D3 receptor neurotransmission in cognition
Nakajima, S., Gerretsen, P., Takeuchi, H., Caravaggio, F., Chow, T. W., Foll, B. L., Mulsant, B. H., Pollock, B. G., & Graff‐Guerrero, A. (2013) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2013.05.006 · Cited by 179 · see citing works
Klune, C. B., Jin, B., & DeNardo, L. A. (2021) · eLife · doi:10.7554/elife.64567 · Cited by 171 · see citing works
Volman, S. F., Lammel, S., Margolis, E. B., Kim, Y., Richard, J. M., Roitman, M. F., & Lobo, M. K. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3250-13.2013 · Cited by 168 · see citing works
Neuromodulation in circuits of aversive emotional learning
Likhtik, E., & Johansen, J. P. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0503-3 · Cited by 165 · see citing works
Emotion regulation by cognitive reappraisal - The role of frontal theta oscillations
Ertl, M., Hildebrandt, M., Ourina, K., Leicht, G., & Mulert, C. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.05.044 · Cited by 159 · see citing works
Regional Delta Waves In Human Rapid Eye Movement Sleep
Bernardi, G., Betta, M., Ricciardi, E., Pietrini, P., Tononi, G., & Siclari, F. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.2298-18.2019 · Cited by 156 · 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
The role of high-frequency oscillatory activity in reward processing and learning
Marco‐Pallarés, J., Münte, T. F., & Rodríguez‐Fornells, A. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.11.014 · Cited by 164 · 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
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
Murty, V. P., & Adcock, R. A. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht063 · Cited by 159 · see citing works
Wang, L., Saalmann, Y. B., Pinsk, M. A., Arcaro, M. J., & Kastner, S. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.033 · Cited by 158 · see citing works
Coherent delta-band oscillations between cortical areas correlate with decision making
Nácher, V., Ledberg, A., Deco, G., & Romo, R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1314681110 · Cited by 158 · see citing works
Brain activity mapping at multiple scales with silicon microprobes containing 1,024 electrodes
Shobe, J. L., Claar, L. D., Parhami, S., Bakhurin, K. I., & Masmanidis, S. C. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00464.2015 · Cited by 146 · see citing works
Dopaminergic and Prefrontal Basis of Learning from Sensory Confidence and Reward Value
Lak, A., Okun, M., Moss, M. M., Gurnani, H., Farrell, K., Wells, M. J., Reddy, C. B., Kepecs, Á., Harris, K. D., & Carandini, M. (2019) · Neuron · doi:10.1016/j.neuron.2019.11.018 · Cited by 128 · see citing works
A human prefrontal-subthalamic circuit for cognitive control
Kelley, R. M., Flouty, O. E., Emmons, E. B., Kim, Y.-C., Kingyon, J. R., Wessel, J. R., Oya, H., Greenlee, J. D. W., & Narayanan, N. S. (2017) · Brain · doi:10.1093/brain/awx300 · Cited by 142 · see citing works
Low, R. J., Gu, Y., & Tank, D. W. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421753111 · Cited by 141 · see citing works
Cognit activation: a mechanism enabling temporal integration in working memory
Fuster, J. M., & Bressler, S. L. (2012) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2012.03.005 · Cited by 139 · see citing works
Intrinsic dopamine and acetylcholine dynamics in the striatum of mice
Krok, A. C., Maltese, M., Mistry, P. N., Miao, X., Li, Y., & Tritsch, N. X. (2023) · Nature · doi:10.1038/s41586-023-05995-9 · Cited by 144 · see citing works
Lazaro, M. T., Taxidis, J., Shuman, T., Bachmutsky, I., Ikrar, T., Santos, R., Marcello, G. M., Mylavarapu, A., Chandra, S., Foreman, A., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.05.006 · Cited by 125 · see citing works
Segregation of cortical head direction cell assemblies on alternating theta cycles
Brandon, M. P., Bogaard, A. R., Schultheiss, N. W., & Hasselmo, M. E. (2013) · Nature Neuroscience · doi:10.1038/nn.3383 · Cited by 124 · see citing works
Development of Hippocampal–Prefrontal Cortex Interactions through Adolescence
Calabro, F. J., Murty, V. P., Jalbrzikowski, M., Tervo‐Clemmens, B., & Luna, B. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz186 · Cited by 125 · see citing works
Mid-frontal theta activity is diminished during cognitive control in Parkinson's disease
Singh, A. P., Richardson, S. P., Narayanan, N. S., & Cavanagh, J. F. (2018) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2018.05.020 · Cited by 125 · see citing works
Role of nicotinic acetylcholine receptors in regulating dopamine neuron activity
Faure, P., Tolu, S., Valverde, S., & Naudé, J. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.05.040 · Cited by 125 · 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
Parker, K. L., Kim, Y.-C., Kelley, R. M., Nessler, A. J., Chen, K.-H., Ewald, V. A. M., Andreasen, N. C., & Narayanan, N. S. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.50 · Cited by 118 · see citing works
Parker, K. L., Chen, K., Kingyon, J. R., Cavanagh, J. F., & Narayanan, N. S. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2772-14.2014 · Cited by 114 · see citing works
Nonoscillatory Phase Coding and Synchronization in the Bat Hippocampal Formation
Eliav, T., Geva-Sagiv, M., Yartsev, M. M., Finkelstein, A., Rubin, A., Las, L., & Ulanovsky, N. (2018) · Cell · doi:10.1016/j.cell.2018.09.017 · Cited by 106 · see citing works
Cho, R. Y., Walker, C. P. R., Polizzotto, N. R., Wozny, T. A., Fissell, C., Chen, C. A., & Lewis, D. A. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht341 · Cited by 109 · see citing works
Phillips, J. M., Vinck, M. A., Everling, S., & Womelsdorf, T. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht050 · Cited by 107 · see citing works
Frank, M. G., & Heller, H. C. (2018) · Handbook of experimental pharmacology · doi:10.1007/164_2018_140 · Cited by 109 · see citing works
The Role of Dopamine D3 Receptors in Antipsychotic Activity and Cognitive Functions
Groß, G., & Drescher, K. U. (2012) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-25758-2_7 · Cited by 109 · see citing works
McKlveen, J. M., Moloney, R. D., Scheimann, J. R., Myers, B., & Herman, J. P. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.04.032 · Cited by 109 · see citing works
Berger, B., Griesmayr, B., Minarik, T., Biel, A. L., Pinal, D., Sterr, A., & Sauseng, P. (2019) · Nature Communications · doi:10.1038/s41467-019-12057-0 · Cited by 100 · see citing works
Roy, A., Svensson, F. P., Mazeh, A., & Kocsis, B. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1374-6 · Cited by 99 · see citing works
Specialized medial prefrontal–amygdala coordination in other-regarding decision preference
Monte, O. D., Chu, C.-C. J., Fagan, N. A., & Chang, S. W. C. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0593-y · Cited by 99 · see citing works
Turning a Negative into a Positive: Ascending GABAergic Control of Cortical Activation and Arousal
Brown, R. E., & McKenna, J. T. (2015) · Frontiers in Neurology · doi:10.3389/fneur.2015.00135 · Cited by 89 · see citing works
Kim, Y.-C., Han, S.-W., Alberico, S. L., Ruggiero, R. N., Corte, B. J. D., Chen, K., & Narayanan, N. S. (2016) · Current Biology · doi:10.1016/j.cub.2016.11.029 · Cited by 95 · see citing works
In vivo functional diversity of midbrain dopamine neurons within identified axonal projections
Farassat, N., Costa, K. M., Stojanovic, S., Albert, S., Kovacheva, L., Shin, J., Egger, R., Somayaji, M., Duvarci, S., Schneider, G., et al. (2019) · eLife · doi:10.7554/elife.48408 · Cited by 94 · see citing works
Intrahemispheric theta rhythm desynchronization impairs working memory
Alekseichuk, I., Pabel, S. C., Antal, A., & Paulus, W. (2017) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-160714 · Cited by 89 · see citing works
Zielinski, M. C., Tang, W., & Jadhav, S. P. (2017) · Hippocampus · doi:10.1002/hipo.22821 · Cited by 95 · see citing works
Lohani, S., Martig, A. K., Deisseroth, K. A., Witten, I. B., & Moghaddam, B. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.03.012 · Cited by 88 · see citing works
Timing variability and midfrontal ~4 Hz rhythms correlate with cognition in Parkinson’s disease
Singh, A. P., Cole, R. C., Espinoza, A. I., Evans, A., Cao, S., Cavanagh, J. F., & Narayanan, N. S. (2021) · npj Parkinson s Disease · doi:10.1038/s41531-021-00158-x · Cited by 90 · see citing works
Flexible frequency control of cortical oscillations enables computations required for working memory
Dipoppa, M., & Gutkin, B. S. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1303270110 · Cited by 88 · 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 90 · see citing works
Self-citationCorticostriatal Coordination through Coherent Phase-Amplitude Coupling
von Nicolai, C., Engler, G., Sharott, A., Engel, A. K., Moll, C. K. E., & Siegel, M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.5007-13.2014 · Cited by 83 · see citing works
Sáez, I., Lin, J. J., Stolk, A., Chang, E. F., Parvizi, J., Schalk, G., Knight, R. T., & Hsu, M. (2018) · Current Biology · doi:10.1016/j.cub.2018.07.045 · Cited by 79 · see citing works
Functional myelin in cognition and neurodevelopmental disorders
Khelfaoui, H., Ibaceta-González, C., & Angulo, M. C. (2024) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-024-05222-2 · Cited by 83 · see citing works
Dopamine D3 receptor antagonism—still a therapeutic option for the treatment of schizophrenia
Groß, G., Wicke, K. M., & Drescher, K. U. (2012) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-012-0806-3 · Cited by 86 · see citing works
Ehrlich, D. E., Ryan, S. J., & Rainnie, D. G. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.237453 · Cited by 86 · see citing works
Reversal of theta rhythm flow through intact hippocampal circuits
Jackson, J., Amilhon, B., Goutagny, R., Bott, J.-B., Manseau, F., Kortleven, C., Bressler, S. L., & Williams, S. (2014) · Nature Neuroscience · doi:10.1038/nn.3803 · Cited by 83 · see citing works
Donnelly, N. A., Holtzman, T., Rich, P. D., Nevado‐Holgado, A. J., Fernando, A. B. P., Dijck, G. V., Holzhammer, T., Paul, O., Ruther, P., Paulsen, O., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0111300 · Cited by 84 · see citing works
Ventral tegmental area GABA neurons mediate stress-induced blunted reward-seeking in mice
Lowes, D. C., Chamberlin, L. A., Kretsge, L. N., Holt, E. S., Abbas, A. I., Park, A. J., Yusufova, L., Bretton-Granatoor, Z., Firdous, A., Enikolopov, A. G., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23906-2 · Cited by 81 · see citing works
Transcranial slow oscillation stimulation during sleep enhances memory consolidation in rats
Binder, S., Berg, K., Gasca, F., Lafon, B., Parra, L. C., Born, J., & Marshall, L. (2014) · Brain Stimulation · doi:10.1016/j.brs.2014.03.001 · Cited by 74 · see citing works
Synchronization of Medial Temporal Lobe and Prefrontal Rhythms in Human Decision Making
Guitart‐Masip, M., Barnes, G. R., Horner, A. J., Bauer, M., Dolan, R. J., & Düzel, E. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2573-12.2013 · Cited by 79 · see citing works
Thorn, C. A., & Graybiel, A. M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1782-13.2014 · Cited by 76 · see citing works
Ortiz‐Mantilla, S., Hämäläinen, J. A., Realpe-Bonilla, T., & BENASICH, A. A. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1162-16.2016 · Cited by 78 · see citing works
A θ–γ Oscillation Code for Neuronal Coordination during Motor Behavior
Igarashi, J., Isomura, Y., Arai, K., Harukuni, R., & Fukai, T. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2126-13.2013 · Cited by 79 · see citing works
Multiple modes of hippocampal–prefrontal interactions in memory-guided behavior
Shin, J. D., & Jadhav, S. P. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.07.015 · Cited by 77 · see citing works
Multivariate cross-frequency coupling via generalized eigendecomposition
Cohen, M. X. (2017) · eLife · doi:10.7554/elife.21792 · Cited by 72 · see citing works
Kunz, L., Wang, L., Piza, D. L., Zhang, H., Brandt, A., Dümpelmann, M., Reinacher, P. C., Coenen, V. A., Chen, D., Wang, W.-X., et al. (2019) · Science Advances · doi:10.1126/sciadv.aav8192 · Cited by 77 · see citing works
Dembrow, N. C., Zemelman, B. V., & Johnston, D. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4673-14.2015 · Cited by 75 · see citing works
Laubach, M., Caetano, M. S., & Narayanan, N. S. (2015) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2014.12.001 · Cited by 76 · see citing works
Zorzo, C., Méndez-López, M., Méndez, M., & Arias, J. L. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.03.011 · Cited by 75 · see citing works
Negrón-Oyarzo, I., Aboitiz, F., & Fuentealba, P. (2016) · Neural Plasticity · doi:10.1155/2016/7539065 · Cited by 75 · see citing works
Brain Rhythms Connect Impaired Inhibition to Altered Cognition in Schizophrenia
Pittman-Polletta, B., Kocsis, B., Vijayan, S., Whittington, M. A., & Kopell, N. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.02.005 · Cited by 75 · see citing works
- Authors
- Fujisawa, S., & Buzsáki, G.
- Affiliations
- Rutgers, The State University of New Jersey (US)
- Corresponding author
- Buzsáki, György
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2011-10
- Volume
- 72
- Issue
- 1
- Pages
- 153-165
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3235795
- OpenAlex
- W1988220777
- Cited by
- 501
- References
- 63
- Citations by year
- 2026: 14 · 2025: 27 · 2024: 36 · 2023: 28 · 2022: 23 · 2021: 37 · 2020: 31 · 2019: 42 · 2018: 51 · 2017: 41 · 2016: 40 · 2015: 28 · 2014: 33 · 2013: 43 · 2012: 26
- FWCI
- 16.71
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 691 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH054671, MH54671)
- National Institute of Neurological Disorders and Stroke (R01NS034994, NS-34994)
- 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
- working memory, medial prefrontal cortex, ventral tegmental area, hippocampus, theta oscillations, gamma oscillations, phase synchronization, phase locking, goal prediction
- MeSH terms
- Action Potentials, Animals, Choice Behavior, Hippocampus, Male, Memory, Short-Term, Neurons, Prefrontal Cortex, Ventral Tegmental Area, Rats, Brain Waves
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