Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task
Open accessAbstract
Decision-making requires the coordinated activity of diverse brain structures. For example, in maze-based tasks, the prefrontal cortex must integrate spatial information encoded in the hippocampus with mnemonic information concerning route and task rules in order to direct behavior appropriately. Using simultaneous tetrode recordings from CA1 of the rat hippocampus and medial prefrontal cortex, we show that correlated firing in the two structures is selectively enhanced during behavior that recruits spatial working memory, allowing the integration of hippocampal spatial information into a broader, decision-making network. The increased correlations are paralleled by enhanced coupling of the two structures in the 4- to 12-Hz theta-frequency range. Thus the coordination of theta rhythms may constitute a general mechanism through which the relative timing of disparate neural activities can be controlled, allowing specialized brain structures to both encode information independently and to interact selectively according to current behavioral demands.
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?
Working and reference memory rely on efficient hippocampal connectivity between cortical areas.
“Working and reference memory rely on efficient hippocampal connectivity between cortical areas (Jones and Wilson, 2005).”
From Early stage alterations in white matter and decreased functional interhemispheric hippocampal connectivity in the 3xTg mouse model of Alzheimer’s disease. (2019) · cites this paper as Jones and Wilson, 2005
The Discussion reports functional connectivity between the hippocampus and prefrontal cortex during a spatial working-memory task, supporting the working-memory portion of the claim. Our copy does not establish that reference memory relies on this connectivity, nor that the observed coordination is necessary for either form of memory. (LLM, conf=0.86)
Experimental — accuracy not yet measured
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
No references could be resolved yet.
Research works printed but not linked: 63
- Steriade M Gloor P Llinas RR Lopes de Silva FH Mesulam MM Report of IFCN Committee on Basic Mechanisms. Basic mechanisms of cerebral rhythmic activities Electroencephalogr Clin Neurophysiol 1990 76 481 508 1701118
- Singer W Neuronal synchrony: A versatile code for the definition of relations? Neuron 1999 24 49 65 10677026
- Varela F Lachaux JP Rodriguez E Martinerie J The brainweb: Phase synchronization and large-scale integration Nat Rev Neurosci 2001 2 229 239 11283746
- Friston KJ Frith CD Schizophrenia: A disconnection syndrome? Clin Neurosci 1995 3 89 97 7583624
- Spencer KM Nestor PG Niznikiewicz MA Salisbury DF Shenton ME Abnormal neural synchrony in schizophrenia J Neurosci 2003 23 7407 7411 12917376 PMC2848257
- Mann CA Lubar JF Zimmerman AW Miller CA Muenchen RA Quantitative analysis of EEG in boys with attention-deficit-hyperactivity disorder: Controlled study with clinical implications Pediatr Neurol 1992 8 30 36 1558573
- Barry RJ Clarke AR Johnstone SJ A review of electrophysiology in attention-deficit/hyperactivity disorder: I. Qualitative and quantitative electroencephalography Clin Neurophysiol 2003 114 171 183 12559224
- Willis WG Weiler MD Neural substrates of childhood attention-deficit/hyperactivity disorder: Electroencephalographic and magnetic resonance imaging evidence Dev Neuropsychol 2005 27 135 182 15737945
- Salinas E Sejnowski TJ Correlated neuronal activity and the flow of neural information Nat Rev Neurosci 2001 2 539 550 11483997 PMC2868968
- Averbeck BB Lee D Coding and transmission of information by neural ensembles Trends Neurosci 2004 27 225 230 15046882
- Brown EN Kass RE Mitra PP Multiple neural spike train data analysis: State-of-the-art and future challenges Nat Neurosci 2004 7 456 461 15114358
- Singer W Gray CM Visual feature integration and the temporal correlation hypothesis Annu Rev Neurosci 1995 18 555 586 7605074
- Steinmetz PN Roy A Fitzgerald PJ Hsiao SS Johnson KO Attention modulates synchronized neuronal firing in primate somatosensory cortex Nature 2000 404 187 190 10724171
- Laubach M Wessberg J Nicolelis MA Cortical ensemble activity increasingly predicts behaviour outcomes during learning of a motor task Nature 2000 405 567 571 10850715
- Vanderwolf CH Hippocampal electrical activity and voluntary movement in the rat Electroencephalogr Clin Neurophysiol 1969 26 407 418 4183562
- Lee H Simpson GV Logothetis NK Rainer G Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex Neuron 2005 45 147 156 15629709
- Kahana MJ Sekuler R Caplan JB Kirschen M Madsen JR Human theta oscillations exhibit task dependence during virtual maze navigation Nature 1999 399 781 784 10391243
- Raghavachari S Kahana MJ Rizzuto DS Caplan JB Kirschen MP Gating of human theta oscillations by a working memory task J Neurosci 2001 21 3175 3183 11312302 PMC6762557
- Buzsaki G Theta oscillations in the hippocampus Neuron 2002 33 325 40 11832222
- O'Keefe J Nadel L The hippocampus as a cognitive map 1978 London Oxford University Press 570
- Mehta MR Lee AK Wilson MA Role of experience and oscillations in transforming a rate code into a temporal code Nature 2002 417 741 746 12066185
- O'Keefe J Recce ML Phase relationship between hippocampal place units and the EEG theta rhythm Hippocampus 1993 3 317 330 8353611
- Bland BH Oddie SD Theta band oscillation and synchrony in the hippocampal formation and associated structures: The case for its role in sensorimotor integration Behav Brain Res 2001 127 119 136 11718888
- Hasselmo ME Bodelon C Wyble BP A proposed function for hippocampal theta rhythm: Separate phases of encoding and retrieval enhance reversal of prior learning Neural Comput 2002 14 793 817 11936962
- Jensen O Lisman JE Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer Trends Neurosci 2005 28 67 72 15667928
- Colom LV Christie BR Bland BH Cingulate cell discharge patterns related to hippocampal EEG and their modulation by muscarinic and nicotinic agents Brain Res 1988 460 329 338 3224265
- Pare D Gaudreau H Projection cells and interneurons of the lateral and basolateral amygdala: Distinct firing patterns and differential relation to theta and delta rhythms in conscious cats J Neurosci 1996 16 3334 3350 8627370 PMC6579143
- Frank LM Brown EN Wilson MA A comparison of the firing properties of putative excitatory and inhibitory neurons from CA1 and the entorhinal cortex J Neurophysiol 2001 86 2029 2040 11600659
- Berke JD Okatan M Skurski J Eichenbaum HB Oscillatory entrainment of striatal neurons in freely moving rats Neuron 2004 43 883 896 15363398
- Siapas AG Lubenov EV Wilson MA Prefrontal phase locking to hippocampal theta oscillations Neuron 2005 46 141 151 15820700
- Hyman JM Zilli EA Paley AM Hasselmo ME Medial prefrontal cortex cells show dynamic modulation with the hippocampal theta rhythm dependent on behavior Hippocampus 2005 15 739 749 16015622
- Jones MW Wilson MA Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm Hippocampus 2005 15 867 873 16149084
- Swanson LW A direct projection from Ammon's horn to prefrontal cortex in the rat Brain Res 1981 217 150 154 7260612
- Jay TM Glowinski J Thierry AM Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat Brain Res 1989 505 337 340 2598054
- Jay TM Burette F Laroche S NMDA receptor-dependent long-term potentiation in the hippocampal afferent fibre system to the prefrontal cortex in the rat Eur J Neurosci 1995 7 247 250 7757261
- Siapas AG Wilson MA Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep Neuron 1998 21 1123 1128 9856467
- Brito GN Thomas GJ Davis BJ Gingold SI Prelimbic cortex, mediodorsal thalamus, septum, and delayed alternation in rats Exp Brain Res 1982 46 52 58 7067791
- Kesner RP Hunt ME Williams JM Long JM Prefrontal cortex and working memory for spatial response, spatial location, and visual object information in the rat Cereb Cortex 1996 6 311 318 8670659
- Floresco SB Seamans JK Phillips AG Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without a delay J Neurosci 1997 17 1880 1890 9030646 PMC6573377
- Jones MW A comparative review of rodent prefrontal cortex and working memory Curr Mol Med 2002 2 639 647 12420803
- Yang CR Seamans JK Gorelova N Electrophysiological and morphological properties of layers V-VI principal pyramidal cells in rat prefrontal cortex in vitro J Neurosci 1996 16 1904 1921 8774458 PMC6578693
- Degenetais E Thierry AM Glowinski J Gioanni Y Electrophysiological properties of pyramidal neurons in the rat prefrontal cortex: An in vivo intracellular recording study Cereb Cortex 2002 12 1 16 11734528
- Jay TM Witter MP Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin J Comp Neurol 1991 313 574 586 1783682
- Frank LM Brown EN Wilson M Trajectory encoding in the hippocampus and entorhinal cortex Neuron 2000 27 169 178 10939340
- Wood ER Dudchenko PA Robitsek RJ Eichenbaum H Hippocampal neurons encode information about different types of memory episodes occurring in the same location Neuron 2000 27 623 633 11055443
- Baeg EH Kim YB Huh K Mook-Jung I Kim HT Dynamics of population code for working memory in the prefrontal cortex Neuron 2003 40 177 188 14527442
- Skaggs WE McNaughton BL Gothard KM Markus EJ Hanson SJ Cowan JD Giles CL An information-theoretic approach to deciphering the hippocampal code Advances in neural processing systems 1993 Morgan Kauffman 1030 1037
- Fisher NI Statistical analysis of circular data 1993 Cambridge Cambridge University Press
- Buzsaki G Bickford RG Armstrong DM Ponomareff G Chen KS Electric activity in the neocortex of freely moving young and aged rats Neuroscience 1988 26 735 744 3200427
- Sakata S Yamamori T Sakurai Y 7–12 Hz cortical oscillations: Behavioral context and dynamics of prefrontal neuronal ensembles Neuroscience 2005 134 1099 1111 16019153
- Baddeley A Working memory Science 1992 255 556 559 1736359
- Miller EK Cohen JD An integrative theory of prefrontal cortex function Annu Rev Neurosci 2001 24 167 202 11283309
- Lisman JE Idiart MA Storage of 7 +/- 2 short-term memories in oscillatory subcycles Science 1995 267 1512 1515 7878473
- Tierney PL Degenetais E Thierry AM Glowinski J Gioanni Y Influence of the hippocampus on interneurons of the rat prefrontal cortex Eur J Neurosci 2004 20 514 524 15233760
- Klausberger T Marton LF Baude A Roberts JD Magill PJ Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo Nat Neurosci 2004 7 41 47 14634650
- Sesack SR Deutch AY Roth RH Bunney BS Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin J Comp Neurol 1989 290 213 242 2592611
- Coyle JT The GABA-glutamate connection in schizophrenia: Which is the proximate cause? Biochem Pharmacol 2004 68 1507 1514 15451393
- Weinberger DR A connectionist approach to the prefrontal cortex J Neuropsychiatry Clin Neurosci 1993 5 241 253 8369632
- Winterer G Coppola R Goldberg TE Egan MF Jones DW Prefrontal broadband noise, working memory, and genetic risk for schizophrenia Am J Psychiatry 2004 161 490 500 14992975
- Park S Holzman PS Schizophrenics show spatial working memory deficits Arch Gen Psychiatry 1992 49 975 982 1449384
- McHugh TJ Blum KI Tsien JZ Tonegawa S Wilson MA Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice Cell 1996 87 1339 1349 8980239
- Thompson DJ Spectrum estimation and harmonic analysis Proc IEEE 1982 70 1055 1096
- Jarvis MR Mitra PP Sampling properties of the spectrum and coherency of sequences of action potentials Neural Comput 2001 13 717 749 11255566
Cited by
Sorted by citations
Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures?
Fanselow, M. S., & Dong, H.-W. (2010) · Neuron · doi:10.1016/j.neuron.2009.11.031 · Cited by 3,358 · 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
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
Overnight therapy? The role of sleep in emotional brain processing
Walker, M. P., & van der Helm, E. (2009) · Psychological Bulletin · doi:10.1037/a0016570 · Cited by 1,087 · see citing works
The role of sleep in emotional brain function
Goldstein, A. N., & Walker, M. P. (2014) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-032813-153716 · Cited by 1,052 · see citing works
“P A A uthor M anuscript promote their integration into pre-existing autobiographical memory networks (Cahill 2000, Jones & Wilson 2005).”
BackgroundHippocampal 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
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
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
Basso, J. C., & Suzuki, W. A. (2016) · Brain Plasticity · doi:10.3233/bpl-160040 · Cited by 911 · 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
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
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
Rhythms of the hippocampal network
Colgin, L. L. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.21 · Cited by 654 · see citing works
Altered brain microRNA biogenesis contributes to phenotypic deficits in a 22q11-deletion mouse model
Stark, K. L., Xu, B., Bagchi, A., Lai, W.-S., Liu, H., Hsu, R., Wan, X., Pavlidis, P., Mills, A. A., Karayiorgou, M., et al. (2008) · Nature Genetics · doi:10.1038/ng.138 · Cited by 648 · 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
REM sleep, prefrontal theta, and the consolidation of human emotional memory
Nishida, M., Pearsall, J., Buckner, R. L., & Walker, M. P. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn155 · Cited by 603 · 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
Dendritic Inhibition in the Hippocampus Supports Fear Learning
Lovett-Barron, M., Kaifosh, P., Kheirbek, M. A., Danielson, N., Zaremba, J. D., Reardon, T. R., Turi, G. F., Hen, R., Zemelman, B. V., & Losonczy, A. (2014) · Science · doi:10.1126/science.1247485 · Cited by 509 · 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
Hippocampus leads ventral striatum in replay of place-reward information
Lansink, C. S., Goltstein, P. M., Lankelma, J. V., McNaughton, B. L., & Pennartz, C. M. A. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000173 · Cited by 400 · see citing works
Sleep transforms the cerebral trace of declarative memories
Gais, S., Albouy, G., Boly, M., Dang-Vu, T. T., Darsaud, A., Desseilles, M., Rauchs, G., Schabus, M., Sterpenich, V., Vandewalle, G., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705454104 · Cited by 412 · 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
Wulff, P., Ponomarenko, A. A., Bartos, M., Korotkova, T. M., Fuchs, E. C., Bähner, F., Both, M., Tort, A. B. L., Kopell, N. J., Wisden, W., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813176106 · Cited by 400 · 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
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
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
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
Modeling 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
Adhikari, A., Topiwala, M. A., & Gordon, J. A. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.027 · Cited by 285 · see citing works
Assessing transient cross-frequency coupling in EEG data
Cohen, M. X. (2008) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2007.10.012 · Cited by 262 · 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-citationComplementary learning systems
O’Reilly, R. C., Bhattacharyya, R., Howard, M. D., & Ketz, N. (2014) · Cognitive Science · doi:10.1111/j.1551-6709.2011.01214.x · Cited by 259 · see citing works
Delay activity of specific prefrontal interneuron subtypes modulates memory-guided behavior
Kamigaki, T., & Dan, Y. (2017) · Nature Neuroscience · doi:10.1038/nn.4554 · Cited by 208 · 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
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-citationFénelon, K., Mukai, J., Xu, B., Hsu, P.-K., Drew, L. J., Karayiorgou, M., Fischbach, G. D., MacDermott, A. B., & Gogos, J. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1101219108 · Cited by 202 · see citing works
Brain-wide Electrical Spatiotemporal Dynamics Encode Depression Vulnerability
Hultman, R., Ulrich, K., Sachs, B. D., Blount, C., Carlson, D. E., Ndubuizu, N., Bagot, R. C., Parise, E. M., Vu, M.-A. T., Gallagher, N. M., et al. (2018) · Cell · doi:10.1016/j.cell.2018.02.012 · Cited by 183 · see citing works
Apolipoprotein E4, inhibitory network dysfunction, and Alzheimer’s disease
Najm, R., Jones, E. A., & Huang, Y. (2019) · Molecular Neurodegeneration · doi:10.1186/s13024-019-0324-6 · Cited by 183 · see citing works
McNaughton, N., Kocsis, B., & Hajós, M. (2007) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e3282ee82e3 · Cited by 187 · see citing works
Oxytocin improves behavioral and electrophysiological deficits in a novel Shank3-deficient rat
Harony-Nicolas, H., Kay, M., Hoffmann, J. D., Klein, M. E., Bozdagi-Gunal, O., Riad, M., Daskalakis, N. P., Sonar, S., Castillo, P. E., Hof, P. R., et al. (2017) · eLife · doi:10.7554/elife.18904 · Cited by 168 · see citing works
Abbas, A. I., Sundiang, M. J. M., Henoch, B., Morton, M. P., Bolkan, S. S., Park, A. J., Harris, A. Z., Kellendonk, C., & Gordon, J. A. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.029 · Cited by 183 · 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
Takao, K., Kobayashi, K., Hagihara, H., Ohira, K., Shoji, H., Hattori, S., Koshimizu, H., Umemori, J., Toyama, K., Nakamura, H. K., et al. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.38 · Cited by 173 · 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
Cairney, S. A., Durrant, S. J., Power, R., & Lewis, P. A. (2015) · Cerebral Cortex · doi:10.1093/cercor/bht349 · Cited by 139 · see citing works
Neurobiological Correlates of EMDR Monitoring – An EEG Study
Pagani, M., Di Lorenzo, G., Verardo, A. R., Nicolais, G., Monaco, L., Lauretti, G., Russo, R., Niolu, C., Ammaniti, M., Fernandez, I., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045753 · Cited by 145 · see citing works
Sjulson, L., Peyrache, A., Cumpelik, A., Cassataro, D., & Buzsáki, G. (2018) · Neuron · doi:10.1016/j.neuron.2018.04.015 · Cited by 123 · see citing works
Prefrontal and hippocampal contributions to encoding and retrieval of spatial memory
Churchwell, J. C., Morris, A. M., Musso, N. D., & Kesner, R. P. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.12.008 · Cited by 132 · see citing works
The why, what, where, when and how of goal-directed choice: neuronal and computational principles
Verschure, P. F. M. J., Pennartz, C. M. A., & Pezzulo, G. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0483 · Cited by 131 · see citing works
Sleep and the processing of emotions
Deliens, G., Gilson, M., & Peigneux, P. (2014) · Experimental Brain Research · doi:10.1007/s00221-014-3832-1 · Cited by 119 · see citing works
Ruggiero, R. N., Rossignoli, M. T., Marques, D. B., de Sousa, B. M., Romcy-Pereira, R. N., Lopes-Aguiar, C., & Leite, J. P. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.732360 · Cited by 111 · see citing works
Cortical Control of Affective Networks
Kumar, S., Black, S. J., Hultman, R., Szabo, S. T., DeMaio, K. D., Du, J., Katz, B. M., Feng, G., Covington, H. E., & Dzirasa, K. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.0092-12.2013 · Cited by 110 · 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
Akam, T. E., & Kullmann, D. M. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002760 · Cited by 93 · see citing works
“Task-dependent changes in the power and inter-region coherence of oscillatory network activity are observed in many brain regions and behavioral tasks [1–3].”
BackgroundSleep and emotional memory processing
van der Helm, E., & Walker, M. P. (2011) · Sleep Medicine Clinics · doi:10.1016/j.jsmc.2010.12.010 · Cited by 102 · 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
Tuscher, J. J., Taxier, L. R., Fortress, A. M., & Frick, K. M. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.11.002 · Cited by 88 · 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
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-citationAvigan, P. D., Cammack, K., & Shapiro, M. L. (2020) · Hippocampus · doi:10.1002/hipo.23198 · Cited by 73 · see citing works
Lagler, M., Ozdemir, A. T., Lagoun, S., Malagon-Vina, H., Borhegyi, Z., Hauer, R., Jelem, A., & Klausberger, T. (2016) · Neuron · doi:10.1016/j.neuron.2016.08.010 · Cited by 67 · see citing works
Linking hippocampal multiplexed tuning, Hebbian plasticity and navigation
Moore, J. J., Cushman, J. D., Acharya, L., Popeney, B., & Mehta, M. R. (2021) · Nature · doi:10.1038/s41586-021-03989-z · Cited by 69 · 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
Thalamocortical interactions in cognition and disease: The mediodorsal and anterior thalamic nuclei
Perry, B. A. L., Lomi, E., & Mitchell, A. S. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.05.032 · Cited by 62 · 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
Manno, F. A. M., Isla, A. G., Manno, S. H. C., Ahmed, I., Cheng, S. H., Barrios, F. A., & Lau, C. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00039 · Cited by 49 · 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
Electrophysiology of Schizophrenia
Winterer, G., & McCarley, R. W. (2010) · Schizophrenia · doi:10.1002/9781444327298.ch15 · Cited by 23 · 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
Sensory mismatch induces autonomic responses associated with hippocampal theta waves in rats
Aitake, M., Hori, E., Matsumoto, J., Umeno, K., Fukuda, M., Ono, T., & Nishijo, H. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.02.011 · Cited by 17 · see citing works
Neural regulation of the time course for cocaine-cue extinction consolidation in rats
Szalay, Jordan, C. J., & Kantak, K. M. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12035 · Cited by 17 · 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
- Authors
- Jones, M. W., & Wilson, M. A.
- Affiliations
- Massachusetts Institute of Technology (US)
- Corresponding author
- Wilson, Matthew A
- Venue
- PLoS Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2005-11-15
- Volume
- 3
- Issue
- 12
- Pages
- e402
- ISSN
- 1544-9173 (ISSN-L)
- 1545-7885
- PMC
- PMC1283536
- OpenAlex
- W2007430976
- Cited by
- 1,036
- References
- 0
- Citations by year
- 2026: 31 · 2025: 53 · 2024: 60 · 2023: 49 · 2022: 54 · 2021: 58 · 2020: 71 · 2019: 55 · 2018: 62 · 2017: 65 · 2016: 51 · 2015: 65 · 2014: 48 · 2013: 64 · 2012: 41
- FWCI
- 10.09
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Explore Bristol Research (submittedVersion)
- Funders
- Massachusetts Institute of Technology
- Wellcome Trust
- National Institute of Mental Health (R01MH061976, R01 MH 61976, R01 MH-)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- theta oscillations, hippocampus, medial prefrontal cortex, spatial working memory, neuronal synchronization, CA1, decision-making, neural coupling, rats
- MeSH terms
- Animals, Hippocampus, Male, Memory, Space Perception, Theta Rhythm, Time Factors, Prefrontal Cortex, Rats, Long-Evans, 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
