Prefrontal phase locking to hippocampal theta oscillations
Open accessAbstract
The interactions between cortical and hippocampal circuits are critical for memory formation, yet their basic organization at the neuronal network level is not well understood. Here, we demonstrate that a significant portion of neurons in the medial prefrontal cortex of freely behaving rats are phase locked to the hippocampal theta rhythm. In addition, we show that prefrontal neurons phase lock best to theta oscillations delayed by approximately 50 ms and confirm this hippocampo-prefrontal directionality and timing at the level of correlations between single cells. Finally, we find that phase locking of prefrontal cells is predicted by the presence of significant correlations with hippocampal cells at positive delays up to 150 ms. The theta-entrained activity across cortico-hippocampal circuits described here may be important for gating information flow and guiding the plastic changes that are believed to underlie the storage of information across these networks.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Theta waves are maintained, probably by an external input, while local gamma oscillations reduce their presence by a putative imbalance of excitatory-inhibitory activity as a consequence of the loss of perisomatic synapses on PV cells.
“Based on these results, we hypothesize that u waves are maintained, probably by an external input (Siapas et al., 2005;Sirota et al., 2008), while the local g oscillations reduce their presence by a putative imbalance of the excitatory-inhibitory activity as a consequence of the loss of perisomatic synapses on PV cells.”
From Perineuronal Nets Regulate the Inhibitory Perisomatic Input onto Parvalbumin Interneurons and γ Activity in the Prefrontal Cortex (2020) · cites this paper as Siapas et al., 2005
PFC-hippocampal projections generate oscillatory synchronization and support the concept of a directional pathway from hippocampus towards PFC as focal for information processing.
“This illustrates that the PFC-hippocampal projections generate an oscillatory synchronization and supports the concept of a directional pathway of hippocampus towards the PFC as focal for information processing”
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 Siapas et al., 2005
A portion of PFC neurons were coupled to the theta rhythm (4-10 Hz) of the hippocampus and best matched with a delay of approximately 50 ms.
“a portion of the PFC neurons were found to be coupled to the theta rhythm (4–10 Hz) of the hippocampus and to best match with a delay of approximately 50 ms”
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 Siapas et al., 2005
Cites
Baltosser, W. H., & Zar, J. H. (1996) · Ecology · doi:10.2307/2265725 · Cited by 35,166 · see citing works
Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans.
Squire, L. R. (1992) · Psychological Review · doi:10.1037/0033-295x.99.2.195 · Cited by 5,376 · 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
Theta oscillations in the hippocampus
Buzsáki, G. (2002) · Neuron · doi:10.1016/s0896-6273(02)00586-x · Cited by 3,332 · see citing works
Statistics of Directional Data.
Gokhale, D. V., & Mardia, K. V. (1973) · Biometrics · doi:10.2307/2529189 · Cited by 2,459 · see citing works
The Prefrontal Cortex: Anatomy, Physiology, and Neuropsychology of the Frontal Lobe
Fuster, J. M. (1980) · Cited by 2,367 · see citing works
Dynamics of the Hippocampal Ensemble Code for Space
Wilson, M. A., & McNaughton, B. L. (1993) · Science · doi:10.1126/science.8351520 · Cited by 2,350 · see citing works
Self-citationStatistical Analysis of Circular Data.
LANGE, N. D., & Fisher, N. I. (1995) · Journal of the American Statistical Association · doi:10.2307/2291098 · Cited by 2,167 · see citing works
Hippocampal electrical activity and voluntary movement in the rat
Vanderwolf, C. H. (1969) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(69)90092-3 · Cited by 1,928 · see citing works
Statistical Analysis of Circular Data
Fisher, N. I. (1993) · Cambridge University Press eBooks · doi:10.1017/cbo9780511564345 · Cited by 1,695 · see citing works
Statistics of Directional Data
(1972) · Elsevier eBooks · doi:10.1016/c2013-0-07425-7 · Cited by 1,636 · see citing works
Neuronal Spike Trains and Stochastic Point Processes
Perkel, D. H., Gerstein, G. L., & Moore, G. (1967) · Biophysical Journal · doi:10.1016/s0006-3495(67)86596-2 · Cited by 1,482 · see citing works
HIPPOCAMPAL ELECTRICAL ACTIVITY IN AROUSAL
Green, J. D., & Arduini, A. (1954) · Journal of Neurophysiology · doi:10.1152/jn.1954.17.6.533 · Cited by 1,392 · see citing works
Frontal lobes and human memory: Insights from functional neuroimaging
Fletcher, P. C. (2001) · Brain · doi:10.1093/brain/124.5.849 · Cited by 1,348 · see citing works
Neuronal Spike Trains and Stochastic Point Processes
Perkel, D. H., Gerstein, G. L., & Moore, G. P. (1967) · Biophysical Journal · doi:10.1016/s0006-3495(67)86597-4 · Cited by 1,310 · see citing works
The prefrontal cortex: Anatomy, physiology, and neuropsychology of the frontal lobe
Holmes, G. L. (1989) · Journal of Epilepsy · doi:10.1016/0896-6974(89)90035-2 · Cited by 1,210 · see citing works
Statistics of Directional Data
Watson, G. S., & Mardia, K. V. (1973) · Technometrics · doi:10.2307/1267404 · Cited by 1,178 · see citing works
Resonance, oscillation and the intrinsic frequency preferences of neurons
Hutcheon, B., & Yarom, Y. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01547-2 · Cited by 1,121 · see citing works
Halliday, D. M., Rosenberg, J. R., Amjad, A. M., Breeze, P., Conway, B. A., & Farmer, S. F. (1995) · Progress in Biophysics and Molecular Biology · doi:10.1016/s0079-6107(96)00009-0 · Cited by 1,107 · see citing works
The Involvement of the Anterior Cingulate Cortex in Remote Contextual Fear Memory
Frankland, P., Bontempi, B., Talton, L., Kaczmarek, L., & Silva, A. J. (2004) · Science · doi:10.1126/science.1094804 · Cited by 952 · 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
Time-dependent reorganization of brain circuitry underlying long-term memory storage
Bontempi, B., Laurent-Demir, C., Destrade, C., & Jaffard, R. (1999) · Nature · doi:10.1038/23270 · Cited by 673 · see citing works
Sites of Neocortical Reorganization Critical for Remote Spatial Memory
Maviel, T., Durkin, T., Menzaghi, F., & Bontempi, B. (2004) · Science · doi:10.1126/science.1098180 · Cited by 659 · see citing works
Human theta oscillations exhibit task dependence during virtual maze navigation
Kahana, M. J., Sekuler, R., Caplan, J. B., Kirschen, M., & Madsen, J. R. (1999) · Nature · doi:10.1038/21645 · Cited by 649 · see citing works
A direct projection from Ammon's horn to prefrontal cortex in the rat
Swanson, L. W. (1981) · Brain Research · doi:10.1016/0006-8993(81)90192-x · Cited by 533 · see citing works
Modern Techniques in Neuroscience Research
Windhorst, U., & Johansson, H. (1999) · Springer eBooks · doi:10.1007/978-3-642-58552-4 · Cited by 453 · see citing works
Hu, H., Vervaeke, K., & Storm, J. F. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.029249 · Cited by 410 · see citing works
Takehara‐Nishiuchi, K., Kawahara, S., & Kirino, Y. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-30-09897.2003 · Cited by 343 · see citing works
Cortico-Hippocampal Interplay and the Representation of Contexts in the Brain
Miller, R. J. (1991) · Studies of brain function · doi:10.1007/978-3-662-21732-0 · Cited by 341 · see citing works
Wiltgen, B. J., Brown, R. A. M., Talton, L. E., & Silva, A. J. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.015 · Cited by 309 · see citing works
Laroche, S., Jay, T. M., & Thierry, A. M. (1990) · Neuroscience Letters · doi:10.1016/0304-3940(90)90069-l · Cited by 250 · see citing works
Ferino, F., Thierry, A. M., & Glowinski, J. (1987) · Experimental Brain Research · doi:10.1007/bf00236315 · Cited by 246 · see citing works
Hippocampal theta rhythm and the firing of neurons in walking and urethane anesthetized rats
Fox, S. E., Wolfson, S., & Ranck, J. B. (1986) · Experimental Brain Research · doi:10.1007/bf00236028 · Cited by 244 · see citing works
Paré, D., & Gaudreau, H. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03334.1996 · Cited by 230 · see citing works
Neuronal sources of theta rhythm in the entorhinal cortex of the rat
Alonso, A., & García-Austt, E. (1987) · Experimental Brain Research · doi:10.1007/bf00247283 · Cited by 212 · 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
Jay, T. M., Thierry, A., Wiklund, L., & Glowinski, J. (1992) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1992.tb00154.x · Cited by 187 · see citing works
Jay, T. M., Burette, F., & Laroche, S. (1995) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1995.tb01060.x · Cited by 172 · see citing works
Spike timing dependent synaptic plasticity in biological systems
Roberts, P. D., & Bell, C. C. (2002) · Biological Cybernetics · doi:10.1007/s00422-002-0361-y · Cited by 156 · see citing works
Leung, L.-W. S., & Huiwen, Y. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.3.1592 · Cited by 150 · 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
Dégenètais, E. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.7.782 · Cited by 127 · see citing works
Buzsáki, G., & Eidelberg, E. (1983) · Brain Research · doi:10.1016/0006-8993(83)90665-0 · Cited by 121 · see citing works
Cortico-hippocampal interplay and the representation of contexts in the brain
Bruyn, G. W. (1991) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(91)90227-x · Cited by 117 · see citing works
Kocsis, B., & Vertes, R. P. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.68.4.1463 · Cited by 103 · see citing works
Induction of stable long‐term depression in vivo in the hippocampal–prefrontal cortex pathway
Takita, M., Izaki, Y., Jay, T. M., Kaneko, H., & Suzuki, S. S. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00870.x · Cited by 101 · see citing works
Depth profiles of hippocampal rhythmic slow activity (‘theta rhythm’) depend on behaviour
Buzsáki, G., Rappelsberger, P., & Kellényi, L. (1985) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(85)91075-2 · Cited by 81 · see citing works
Time and Frequency Domain Analysis of Spike Train and Time Series Data
Halliday, D. M., & Rosenberg, J. R. (1999) · Springer eBooks · doi:10.1007/978-3-642-58552-4_18 · Cited by 57 · see citing works
Colom, L. V., Christie, B. R., & Bland, B. H. (1988) · Brain Research · doi:10.1016/0006-8993(88)90377-0 · Cited by 57 · see citing works
Ventral tegmental nucleus of Gudden: A pontine hippocampal theta generator?
Bassant, M., & Poindessous‐Jazat, F. (2001) · Hippocampus · doi:10.1002/hipo.1096 · Cited by 49 · see citing works
Pedemonte, M., Pe�a, J. J., & Velluti, R. A. (1996) · Experimental Brain Research · doi:10.1007/bf00227176 · Cited by 39 · see citing works
Measuring The Association Of Point Processes: A Case History
Brillinger, D. R. (2011) · Springer eBooks · doi:10.1007/978-1-4614-1344-8_31 · Cited by 33 · see citing works
Measuring the Association of Point Processes: A Case History
Brillinger, D. R. (1976) · American Mathematical Monthly · doi:10.2307/2318824 · Cited by 25 · see citing works
Sleep and wakefulness auditory processing: Cortical units vs. hippocampal theta rhythm
Pedemonte, M., Pérez-Perera, L., Peña, J. L., et al. (2001) · Cited by 21 · see citing works
Hippocampal theta rhythm synchronizes visual neurons in sleep and waking
Gambini, J. P., Velluti, R. A., & Pedemonte, M. (2002) · Brain Research · doi:10.1016/s0006-8993(01)03321-2 · Cited by 20 · see citing works
[Theta-bursts of hippocampal and septal neurons].
Vinogradova, O. S., & Brazhnik, E. S. (1978) · PubMed · Cited by 4 · 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
Cited by
Sorted by citations
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
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
Coordinated memory replay in the visual cortex and hippocampus during sleep
Ji, D., & Wilson, M. A. (2007) · Nature Neuroscience · doi:10.1038/nn1825 · Cited by 1,669 · see citing works
Self-citationThe 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
Spectral fingerprints of large-scale neuronal interactions
Siegel, M., Donner, T. H., & Engel, A. K. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3137 · Cited by 1,295 · 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
High-frequency, long-range coupling between prefrontal and visual cortex during attention
Gregoriou, G. G., Gotts, S. J., Zhou, H., & Desimone, R. (2009) · Science · doi:10.1126/science.1171402 · Cited by 1,194 · 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
Pape, H.-C., & Pare, D. (2010) · Physiological Reviews · doi:10.1152/physrev.00037.2009 · Cited by 994 · see citing works
EEG and MEG: Relevance to Neuroscience
Lopes da Silva, F. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.017 · Cited by 900 · 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
Hippocampal replay of extended experience
Davidson, T. J., Kloosterman, F., & Wilson, M. A. (2009) · Neuron · doi:10.1016/j.neuron.2009.07.027 · Cited by 806 · see citing works
“…with weak place-related firing (peak rate in tuning curve <3 Hz), leaving 47, 34, 23, 32, and 21 spatially tuned single units in rats 1–5 (cluster quality measures: L ratio 0.12 ± 0.17; isolation distance 17 ± 9; calculated using peak amplitude on each channel [Schmitzer-Torbert et al., 2005]).”
InfluentialSelf-citationBenchenane, 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
Prefrontal–hippocampal interactions in episodic memory
Eichenbaum, H. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.74 · Cited by 870 · see citing works
Cross-Frequency Phase–Phase Coupling between Theta and Gamma Oscillations in the Hippocampus
Belluscio, M. A., Mizuseki, K., Schmidt, R., Kempter, R., & Buzsáki, G. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.4122-11.2012 · Cited by 784 · see citing works
Hippocampal–prefrontal input supports spatial encoding in working memory
Spellman, T., Rigotti, M., Ahmari, S. E., Fusi, S., Gogos, J. A., & Gordon, J. A. (2015) · Nature · doi:10.1038/nature14445 · Cited by 693 · see citing works
Adhikari, A., Topiwala, M. A., & Gordon, J. A. (2010) · Neuron · doi:10.1016/j.neuron.2009.12.002 · Cited by 729 · see citing works
Mizuseki, K., Sirota, A., Pastalkova, E., & Buzsáki, G. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.037 · Cited by 718 · see citing works
Human 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
Prefrontal entrainment of amygdala activity signals safety in learned fear and innate anxiety
Likhtik, E., Stujenske, J. M., A Topiwala, M., Harris, A. Z., & Gordon, J. A. (2014) · Nature Neuroscience · doi:10.1038/nn.3582 · Cited by 577 · 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
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
Hasselmo, M. E. (2005) · Hippocampus · doi:10.1002/hipo.20116 · Cited by 502 · 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
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
Padilla-Coreano, N., Bolkan, S. S., Pierce, G. M., Blackman, D. R., Hardin, W. D., Garcia-Garcia, A. L., Spellman, T. J., & Gordon, J. A. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.011 · Cited by 463 · see citing works
Inhibition of mediodorsal thalamus disrupts thalamofrontal connectivity and cognition
Parnaudeau, S., O’Neill, P.-K., Bolkan, S. S., Ward, R. D., Abbas, A. I., Roth, B. L., Balsam, P. D., Gordon, J. A., & Kellendonk, C. (2013) · Neuron · doi:10.1016/j.neuron.2013.01.038 · Cited by 387 · 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
Inhibition-induced theta resonance in cortical circuits
Stark, E., Eichler, R., Roux, L., Fujisawa, S., Rotstein, H. G., & Buzsáki, G. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.033 · Cited by 326 · see citing works
Cognitive impairment in epilepsy: the role of network abnormalities
Holmes, G. L. (2015) · Epileptic Disorders · doi:10.1684/epd.2015.0739 · Cited by 334 · see citing works
Cannabinoids reveal importance of spike timing coordination in hippocampal function
Robbe, D., Montgomery, S. M., Thome, A., Rueda-Orozco, P. E., McNaughton, B. L., & Buzsaki, G. (2006) · Nature Neuroscience · doi:10.1038/nn1801 · Cited by 333 · 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).”
BackgroundState-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
Self-citationModeling madness in mice: one piece at a time
Arguello, P. A., & Gogos, J. A. (2006) · Neuron · doi:10.1016/j.neuron.2006.09.023 · Cited by 309 · 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
Hippocampal-prefrontal theta oscillations support memory integration
Backus, A. R., Schoffelen, J.-M., Szebényi, S., Hanslmayr, S., & Doeller, C. F. (2016) · Current Biology · doi:10.1016/j.cub.2015.12.048 · Cited by 288 · see citing works
Interaction between neocortical and hippocampal networks via slow oscillations
Sirota, A., & Buzsáki, G. (2005) · Thalamus and Related Systems · doi:10.1017/s1472928807000258 · Cited by 270 · see citing works
Adhikari, A., Topiwala, M. A., & Gordon, J. A. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.027 · Cited by 285 · see citing works
Lesting, J., Narayanan, R. T., Kluge, C., Sangha, S., Seidenbecher, T., & Pape, H.-C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021714 · Cited by 275 · see citing works
Varela, C., Kumar, S., Yang, J. Y., & Wilson, M. A. (2014) · Brain Structure and Function · doi:10.1007/s00429-013-0543-5 · Cited by 277 · see citing works
Self-citationThe role of REM sleep theta activity in emotional memory
Hutchison, I. C., & Rathore, S. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01439 · Cited by 245 · see citing works
Prototypic and arkypallidal neurons in the dopamine-intact external globus pallidus
Abdi, A., Mallet, N., Mohamed, F. Y., Sharott, A., Dodson, P. D., Nakamura, K. C., Suri, S., Avery, S. V., Larvin, J. T., Garas, F. N., et al. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.4662-14.2015 · Cited by 247 · see citing works
Anderson, K. L., Rajagovindan, R., Ghacibeh, G. A., Meador, K. J., & Ding, M. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp223 · Cited by 222 · see citing works
Effects of sleep on memory for conditioned fear and fear extinction.
Pace-Schott, E. F., Germain, A., & Milad, M. R. (2015) · Psychological Bulletin · doi:10.1037/bul0000014 · Cited by 218 · 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
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
Self-citationEschenko, O., Magri, C., Panzeri, S., & Sara, S. J. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr121 · Cited by 194 · see citing works
Brockmann, M. D., Pöschel, B., Cichon, N., & Hanganu-Opatz, I. L. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.041 · Cited by 186 · 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
Direct recording of Theta oscillations in primate prefrontal and anterior cingulate cortices
Tsujimoto, T., Shimazu, H., & Isomura, Y. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00730.2005 · Cited by 184 · see citing works
Hippocampal-prefrontal reactivation during learning is stronger in awake compared with sleep states
Tang, W., Shin, J. D., Frank, L. M., & Jadhav, S. P. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.2291-17.2017 · Cited by 160 · see citing works
Preferential Reactivation of Motivationally Relevant Information in the Ventral Striatum
Lansink, C. S., Goltstein, P. M., Lankelma, J. V., Joosten, R. N. J. M. A., McNaughton, B. L., & Pennartz, C. M. A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1054-08.2008 · Cited by 168 · see citing works
Neuronal coherence during selective attentional processing and sensory–motor integration
Womelsdorf, T., & Fries, P. (2006) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2007.01.005 · Cited by 156 · 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
Early Cognitive Experience Prevents Adult Deficits in a Neurodevelopmental Schizophrenia Model
Lee, H., Dvorak, D., Kao, H.-Y., Duffy, Á. M., Scharfman, H. E., & Fenton, A. A. (2012) · Neuron · doi:10.1016/j.neuron.2012.06.016 · Cited by 122 · see citing works
Carceller, H., Guirado, R., Ripolles-Campos, E., Teruel-Marti, V., & Nacher, J. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.0291-20.2020 · Cited by 112 · see citing works
Astrocytic signaling supports hippocampal–prefrontal theta synchronization and cognitive function
Sardinha, V. M., Guerra‐Gomes, S., Caetano, I., Tavares, G., Martins, M., Reis, J. S., Correia, J. S., Teixeira‐Castro, A., Pinto, L., Sousa, N., et al. (2017) · Glia · doi:10.1002/glia.23205 · Cited by 105 · see citing works
Lesting, J., Daldrup, T., Narayanan, V., Himpe, C., Seidenbecher, T., & Pape, H.-C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077707 · Cited by 105 · see citing works
Tamura, M., Mukai, J., Gordon, J. A., & Gogos, J. A. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.025 · Cited by 98 · 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
Burton, B. G., Hok, V., Save, E., & Poucet, B. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.11.045 · Cited by 86 · 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
Hippocampal network oscillations at the interplay between innate anxiety and learned fear
Çalışkan, G., & Stork, O. (2019) · Psychopharmacology · doi:10.1007/s00213-018-5109-z · Cited by 72 · see citing works
All My Circuits: Using Multiple Electrodes to Understand Functioning Neural Networks
Miller, E. K., & Wilson, M. A. (2008) · Neuron · doi:10.1016/j.neuron.2008.10.033 · Cited by 76 · see citing works
Self-citationPihlajamäki, M., & Sperling, R. A. (2009) · Behavioural Neurology · doi:10.1155/2009/276384 · Cited by 102 · see citing works
Kleen, J. K., Wu, E. X., Holmes, G. L., Scott, R. C., & Lenck-Santini, P.-P. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.2196-11.2011 · Cited by 68 · see citing works
The hippocampus and exploration: dynamically evolving behavior and neural representations
Johnson, A., Varberg, Z., Benhardus, J., Maahs, A., & Schrater, P. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00216 · Cited by 61 · see citing works
Chronic stress disrupts neural coherence between cortico-limbic structures
Oliveira, J. F., Dias, N. S., Correia, M., Gama-Pereira, F., Sardinha, V. M., Lima, A., Oliveira, A. F., Jacinto, L. R., Ferreira, D. S., Silva, A. M., et al. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00010 · Cited by 55 · see citing works
Varela, C., & Wilson, M. A. (2020) · eLife · doi:10.7554/elife.48881 · Cited by 52 · see citing works
Self-citationLocal targeted memory reactivation in human sleep
Bar, E., Marmelshtein, A., Arzi, A., Perl, O., Livne, E., Hizmi, E., Paz, R., Sobel, N., Dudai, Y., & Nir, Y. (2020) · Current Biology · doi:10.1016/j.cub.2020.01.091 · Cited by 50 · see citing works
Different simultaneous sleep states in the hippocampus and neocortex
Emrick, J. J., Gross, B. A., Riley, B. T., & Poe, G. R. (2016) · Sleep · doi:10.5665/sleep.6326 · Cited by 38 · see citing works
Altered Hippocampal-Prefrontal Neural Dynamics in Mouse Models of Down Syndrome
Chang, P., Bush, D., Schorge, S., Good, M., Canonica, T., Shing, N., Noy, S., Wiseman, F. K., Burgess, N., Tybulewicz, V. L. J., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2019.12.065 · Cited by 47 · see citing works
A bird-brain view of episodic memory
Rattenborg, N. C., & Martinez-Gonzalez, D. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.03.030 · Cited by 45 · see citing works
Banks, P. J., Burroughs, A. C., Barker, G. R. I., Brown, J. T., Warburton, E. C., & Bashir, Z. I. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1512064112 · Cited by 42 · see citing works
Lopes Aguiar, C., Romcy-Pereira, R. N., Escorsim Szawka, R., Galvis-Alonso, O. Y., Anselmo-Franci, J. A., & Pereira Leite, J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.02.040 · Cited by 42 · see citing works
Hypothalamic Supramammillary Control of Cognition and Motivation
Kesner, A. J., Mozaffarilegha, M., Thirtamara Rajamani, K., Arima, Y., Harony-Nicolas, H., Hashimotodani, Y., Ito, H. T., Song, J., & Ikemoto, S. (2023) · The Journal of Neuroscience · doi:10.1523/jneurosci.1320-23.2023 · Cited by 35 · see citing works
Romani, A., Antonietti, A., Bella, D., Budd, J., Giacalone, E., Kurban, K., Sáray, S., Abdellah, M., Arnaudon, A., Boci, E., et al. (2024) · PLOS Biology · doi:10.1371/journal.pbio.3002861 · Cited by 39 · see citing works
Differential Impact of Acute and Chronic Stress on CA1 Spatial Coding and Gamma Oscillations
Tomar, A., Polygalov, D., & McHugh, T. J. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.710725 · Cited by 21 · see citing works
Calcyon upregulation in adolescence impairs response inhibition and working memory in adulthood
Vazdarjanova, A., Bunting, K., Muthusamy, N., & Bergson, C. (2011) · Molecular Psychiatry · doi:10.1038/mp.2011.14 · Cited by 20 · see citing works
Dunn, S. L. S., Town, S. M., Bizley, J. K., & Bendor, D. (2022) · Nature Communications · doi:10.1038/s41467-022-33507-2 · Cited by 17 · see citing works
Circuit mechanisms for disentangled representations and generalization in the hippocampus
Tang, W., Chang, H., Liu, C., Perez-Hernandez, S., Zheng, W. Y., Park, J., Karaba, L. A., Oliva, A., & Fernandez-Ruiz, A. (2026) · Nature Neuroscience · doi:10.1038/s41593-026-02491-x
- Authors
- Siapas, A. G., Lubenov, E. V., & Wilson, M. A.
- Affiliations
- California Institute of Technology (US)
- Massachusetts Institute of Technology (US)
- Corresponding author
- Siapas, Athanassios G.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2005-04
- Volume
- 46
- Issue
- 1
- Pages
- 141-151
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2129217278
- Cited by
- 1,014
- References
- 58
- Citations by year
- 2026: 33 · 2025: 47 · 2024: 53 · 2023: 47 · 2022: 47 · 2021: 63 · 2020: 54 · 2019: 40 · 2018: 50 · 2017: 55 · 2016: 45 · 2015: 56 · 2014: 47 · 2013: 63 · 2012: 48
- FWCI
- 17.04
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (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 › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- phase locking, hippocampal theta rhythm, medial prefrontal cortex, neuronal synchronization, memory formation, single-unit activity
- MeSH terms
- Animals, Hippocampus, Male, Neural Pathways, Neurons, Theta Rhythm, Prefrontal Cortex, 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