{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T13:44:47Z","timestamp":1791294287505,"version":"4.1.0"},"reference-count":83,"publisher":"Springer Science and Business Media LLC","issue":"7593","license":[{"start":{"date-parts":[[2016,3,1]],"date-time":"2016-03-01T00:00:00Z","timestamp":1456790400000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nature"],"published-print":{"date-parts":[[2016,3]]},"DOI":"10.1038\/nature17144","type":"journal-article","created":{"date-parts":[[2016,3,2]],"date-time":"2016-03-02T06:08:48Z","timestamp":1456898928000},"page":"185-190","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":240,"title":["A hippocampal network for spatial coding during immobility and sleep"],"prefix":"10.1038","volume":"531","author":[{"given":"Kenneth","family":"Kay","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marielena","family":"Sosa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jason E.","family":"Chung","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mattias P.","family":"Karlsson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Margaret C.","family":"Larkin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Loren M.","family":"Frank","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2016,3,2]]},"reference":[{"key":"BFnature17144_CR1","unstructured":"O\u2019Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Oxford Univ. Press, 1978)"},{"key":"BFnature17144_CR2","first-page":"1055","volume":"261","author":"MA Wilson","year":"1993","unstructured":"Wilson, M. A. & McNaughton, B. L. Dynamics of the hippocampal ensemble code for space. Science 261, 1055\u20131058 (1993)","journal-title":"Dynamics of the hippocampal ensemble code for space. Science"},{"key":"BFnature17144_CR3","doi-asserted-by":"publisher","first-page":"130","DOI":"10.1038\/nn.3304","volume":"16","author":"G Buzs\u00e1ki","year":"2013","unstructured":"Buzs\u00e1ki, G. & Moser, E. I. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nature Neurosci. 16, 130\u2013138 (2013)","journal-title":"Nature Neurosci."},{"key":"BFnature17144_CR4","doi-asserted-by":"publisher","first-page":"764","DOI":"10.1016\/j.neuron.2014.07.032","volume":"83","author":"H Eichenbaum","year":"2014","unstructured":"Eichenbaum, H. & Cohen, N. J. Can we reconcile the declarative memory and spatial navigation views on hippocampal function? Neuron 83, 764\u2013770 (2014)","journal-title":"Neuron"},{"key":"BFnature17144_CR5","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1016\/S0166-4328(89)80102-0","volume":"34","author":"D Eilam","year":"1989","unstructured":"Eilam, D. & Golani, I. Home base behavior of rats (Rattus norvegicus) exploring a novel environment. Behav. Brain Res. 34, 199\u2013211 (1989)","journal-title":"Behav. Brain Res."},{"key":"BFnature17144_CR6","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1007\/s10071-006-0023-x","volume":"9","author":"DG Wallace","year":"2006","unstructured":"Wallace, D. G., Hamilton, D. A. & Whishaw, I. Q. Movement characteristics support a role for dead reckoning in organizing exploratory behavior. Anim. Cogn. 9, 219\u2013228 (2006)","journal-title":"Anim. Cogn."},{"key":"BFnature17144_CR7","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1016\/j.neubiorev.2004.03.004","volume":"28","author":"DM Bannerman","year":"2004","unstructured":"Bannerman, D. M. et al. Regional dissociations within the hippocampus\u2014memory and anxiety. Neurosci. Biobehav. Rev. 28, 273\u2013283 (2004)","journal-title":"Neurosci. Biobehav. Rev."},{"key":"BFnature17144_CR8","doi-asserted-by":"publisher","first-page":"2185","DOI":"10.1111\/j.1460-9568.2006.04754.x","volume":"23","author":"NS Pentkowski","year":"2006","unstructured":"Pentkowski, N. S., Blanchard, D. C., Lever, C., Litvin, Y. & Blanchard, R. J. Effects of lesions to the dorsal and ventral hippocampus on defensive behaviors in rats. Eur. J. Neurosci. 23, 2185\u20132196 (2006)","journal-title":"Eur. J. Neurosci."},{"key":"BFnature17144_CR9","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1038\/nrn3492","volume":"14","author":"S Maren","year":"2013","unstructured":"Maren, S., Phan, K. L. & Liberzon, I. The contextual brain: implications for fear conditioning, extinction and psychopathology. Nature Rev. Neurosci. 14, 417\u2013428 (2013)","journal-title":"Nature Rev. Neurosci."},{"key":"BFnature17144_CR10","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1101\/lm.59603","volume":"10","author":"KM Christian","year":"2003","unstructured":"Christian, K. M. & Thompson, R. F. Neural substrates of eyeblink conditioning: acquisition and retention. Learn. Mem. 10, 427\u2013455 (2003)","journal-title":"Learn. Mem."},{"key":"BFnature17144_CR11","doi-asserted-by":"publisher","first-page":"556","DOI":"10.1152\/jn.91159.2008","volume":"102","author":"M Takahashi","year":"2009","unstructured":"Takahashi, M., Lauwereyns, J., Sakurai, Y. & Tsukada, M. A code for spatial alternation during fixation in rat hippocampal CA1 neurons. J. Neurophysiol. 102, 556\u2013567 (2009)","journal-title":"J. Neurophysiol."},{"key":"BFnature17144_CR12","doi-asserted-by":"publisher","first-page":"14607","DOI":"10.1523\/JNEUROSCI.1537-13.2013","volume":"33","author":"CJ MacDonald","year":"2013","unstructured":"MacDonald, C. J., Carrow, S., Place, R. & Eichenbaum, H. Distinct hippocampal time cell sequences represent odor memories in immobilized rats. J. Neurosci. 33, 14607\u201314616 (2013)","journal-title":"J. Neurosci."},{"key":"BFnature17144_CR13","doi-asserted-by":"publisher","first-page":"655","DOI":"10.1002\/hipo.22401","volume":"25","author":"S Hattori","year":"2015","unstructured":"Hattori, S., Chen, L., Weiss, C. & Disterhoft, J. F. Robust hippocampal responsivity during retrieval of consolidated associative memory. Hippocampus 25, 655\u2013669 (2015)","journal-title":"Hippocampus"},{"key":"BFnature17144_CR14","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1038\/nn.2732","volume":"14","author":"MF Carr","year":"2011","unstructured":"Carr, M. F., Jadhav, S. P. & Frank, L. M. Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nature Neurosci. 14, 147\u2013153 (2011)","journal-title":"Nature Neurosci."},{"key":"BFnature17144_CR15","doi-asserted-by":"publisher","first-page":"74","DOI":"10.1038\/nature12112","volume":"497","author":"BE Pfeiffer","year":"2013","unstructured":"Pfeiffer, B. E. & Foster, D. J. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497, 74\u201379 (2013)","journal-title":"Nature"},{"key":"BFnature17144_CR16","doi-asserted-by":"publisher","first-page":"1025","DOI":"10.1126\/science.1589772","volume":"256","author":"G Buzs\u00e1ki","year":"1992","unstructured":"Buzs\u00e1ki, G., Horvath, Z., Urioste, R., Hetke, J. & Wise, K. High-frequency network oscillation in the hippocampus. Science 256, 1025\u20131027 (1992)","journal-title":"Science"},{"key":"BFnature17144_CR17","doi-asserted-by":"publisher","first-page":"1073","DOI":"10.1002\/hipo.22488","volume":"10","author":"G Buzs\u00e1ki","year":"2015","unstructured":"Buzs\u00e1ki, G. Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning. Hippocampus 10, 1073\u20131188 (2015)","journal-title":"Hippocampus"},{"key":"BFnature17144_CR18","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1016\/0165-0173(83)90037-1","volume":"6","author":"G Buzs\u00e1ki","year":"1983","unstructured":"Buzs\u00e1ki, G., Leung, L. W. & Vanderwolf, C. H. Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 6, 139\u2013171 (1983)","journal-title":"Brain Res."},{"key":"BFnature17144_CR19","doi-asserted-by":"publisher","first-page":"585","DOI":"10.1016\/S0896-6273(00)00135-5","volume":"28","author":"J Csicsvari","year":"2000","unstructured":"Csicsvari, J., Hirase, H., Mamiya, A. & Buzsaki, G. Ensemble patterns of hippocampal CA3\u2013CA1 neurons during sharp wave-associated population events. Neuron 28, 585\u2013594 (2000)","journal-title":"Neuron"},{"key":"BFnature17144_CR20","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1002\/(SICI)1098-1063(1997)7:4<437::AID-HIPO9>3.0.CO;2-F","volume":"7","author":"M Penttonen","year":"1997","unstructured":"Penttonen, M., Kamondi, A., Sik, A., Acsady, L. & Buzsaki, G. Feed-forward and feed-back activation of the dentate gyrus in vivo during dentate spikes and sharp wave bursts. Hippocampus 7, 437\u2013450 (1997)","journal-title":"Hippocampus"},{"key":"BFnature17144_CR21","doi-asserted-by":"publisher","first-page":"913","DOI":"10.1038\/nn.2344","volume":"12","author":"MP Karlsson","year":"2009","unstructured":"Karlsson, M. P. & Frank, L. M. Awake replay of remote experiences in the hippocampus. Nature Neurosci. 12, 913\u2013918 (2009)","journal-title":"Nature Neurosci."},{"key":"BFnature17144_CR22","doi-asserted-by":"publisher","first-page":"497","DOI":"10.1016\/j.neuron.2009.07.027","volume":"63","author":"TJ Davidson","year":"2009","unstructured":"Davidson, T. J., Kloosterman, F. & Wilson, M. A. Hippocampal replay of extended experience. Neuron 63, 497\u2013507 (2009)","journal-title":"Neuron"},{"key":"BFnature17144_CR23","doi-asserted-by":"publisher","first-page":"695","DOI":"10.1016\/j.neuron.2010.01.034","volume":"65","author":"AS Gupta","year":"2010","unstructured":"Gupta, A. S., van der Meer, M. A., Touretzky, D. S. & Redish, A. D. Hippocampal replay is not a simple function of experience. Neuron 65, 695\u2013705 (2010)","journal-title":"Neuron"},{"key":"BFnature17144_CR24","doi-asserted-by":"publisher","first-page":"e5494","DOI":"10.1371\/journal.pone.0005494","volume":"4","author":"SM Kim","year":"2009","unstructured":"Kim, S. M. & Frank, L. M. Hippocampal lesions impair rapid learning of a continuous spatial alternation task. PLoS ONE 4, e5494 (2009)","journal-title":"PLoS ONE"},{"key":"BFnature17144_CR25","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1007\/BF00237147","volume":"52","author":"BL McNaughton","year":"1983","unstructured":"McNaughton, B. L., Barnes, C. A. & O\u2019Keefe, J. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp. Brain Res. 52, 41\u201349 (1983)","journal-title":"Exp. Brain Res."},{"key":"BFnature17144_CR26","doi-asserted-by":"publisher","first-page":"828","DOI":"10.1038\/nature02058","volume":"425","author":"J Huxter","year":"2003","unstructured":"Huxter, J., Burgess, N. & O\u2019Keefe, J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425, 828\u2013832 (2003)","journal-title":"Nature"},{"key":"BFnature17144_CR27","doi-asserted-by":"publisher","first-page":"924","DOI":"10.1002\/hipo.22415","volume":"25","author":"C Zheng","year":"2015","unstructured":"Zheng, C., Bieri, K. W., Trettel, S. G. & Colgin, L. L. The relationship between gamma frequency and running speed differs for slow and fast gamma rhythms in freely behaving rats. Hippocampus 25, 924\u2013938 (2015)","journal-title":"Hippocampus"},{"key":"BFnature17144_CR28","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1016\/j.neuron.2014.12.001","volume":"85","author":"EA Mankin","year":"2015","unstructured":"Mankin, E. A., Diehl, G. W., Sparks, F. T., Leutgeb, S. & Leutgeb, J. K. Hippocampal CA2 activity patterns change over time to a larger extent than between spatial contexts. Neuron 85, 190\u2013201 (2015)","journal-title":"Neuron"},{"key":"BFnature17144_CR29","doi-asserted-by":"publisher","first-page":"1078","DOI":"10.1016\/j.neuron.2015.07.007","volume":"87","author":"L Lu","year":"2015","unstructured":"Lu, L., Igarashi, K. M., Witter, M. P., Moser, E. I. & Moser, M. B. Topography of place maps along the CA3-to-CA2 axis of the hippocampus. Neuron 87, 1078\u20131092 (2015)","journal-title":"Neuron"},{"key":"BFnature17144_CR30","doi-asserted-by":"publisher","first-page":"1093","DOI":"10.1016\/j.neuron.2015.07.012","volume":"87","author":"H Lee","year":"2015","unstructured":"Lee, H., Wang, C., Deshmukh, S. S. & Knierim, J. J. Neural population evidence of functional heterogeneity along the CA3 transverse axis: pattern completion versus pattern separation. Neuron 87, 1093\u20131105 (2015)","journal-title":"Neuron"},{"key":"BFnature17144_CR31","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1016\/j.neuron.2009.08.037","volume":"64","author":"K Mizuseki","year":"2009","unstructured":"Mizuseki, K., Sirota, A., Pastalkova, E. & Buzsaki, G. Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 64, 267\u2013280 (2009)","journal-title":"Neuron"},{"key":"BFnature17144_CR32","doi-asserted-by":"publisher","first-page":"242","DOI":"10.1016\/0006-8993(86)91483-6","volume":"398","author":"G Buzs\u00e1ki","year":"1986","unstructured":"Buzs\u00e1ki, G. Hippocampal sharp waves: their origin and significance. Brain Res. 398, 242\u2013252 (1986)","journal-title":"Brain Res."},{"key":"BFnature17144_CR33","doi-asserted-by":"publisher","first-page":"1373","DOI":"10.1523\/JNEUROSCI.22-04-01373.2002","volume":"22","author":"B Jarosiewicz","year":"2002","unstructured":"Jarosiewicz, B., McNaughton, B. L. & Skaggs, W. E. Hippocampal population activity during the small-amplitude irregular activity state in the rat. J. Neurosci. 22, 1373\u20131384 (2002)","journal-title":"J. Neurosci."},{"key":"BFnature17144_CR34","doi-asserted-by":"publisher","first-page":"407","DOI":"10.1016\/0013-4694(69)90092-3","volume":"26","author":"CH Vanderwolf","year":"1969","unstructured":"Vanderwolf, C. H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26, 407\u2013418 (1969)","journal-title":"Electroencephalogr. Clin. Neurophysiol."},{"key":"BFnature17144_CR35","doi-asserted-by":"publisher","first-page":"560","DOI":"10.1016\/j.neuron.2010.04.013","volume":"66","author":"V Chevaleyre","year":"2010","unstructured":"Chevaleyre, V. & Siegelbaum, S. A. Strong CA2 pyramidal neuron synapses define a powerful disynaptic cortico-hippocampal loop. Neuron 66, 560\u2013572 (2010)","journal-title":"Neuron"},{"key":"BFnature17144_CR36","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1038\/nn.3614","volume":"17","author":"K Kohara","year":"2014","unstructured":"Kohara, K. et al. Cell type-specific genetic and optogenetic tools reveal hippocampal CA2 circuits. Nature Neurosci. 17, 269\u2013279 (2014)","journal-title":"Nature Neurosci."},{"key":"BFnature17144_CR37","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1038\/nature13028","volume":"508","author":"FL Hitti","year":"2014","unstructured":"Hitti, F. L. & Siegelbaum, S. A. The hippocampal CA2 region is essential for social memory. Nature 508, 88\u201392 (2014)","journal-title":"Nature"},{"key":"BFnature17144_CR38","doi-asserted-by":"publisher","first-page":"1580","DOI":"10.1126\/science.2740902","volume":"244","author":"TC Foster","year":"1989","unstructured":"Foster, T. C., Castro, C. A. & McNaughton, B. L. Spatial selectivity of rat hippocampal neurons: dependence on preparedness for movement. Science 244, 1580\u20131582 (1989)","journal-title":"Science"},{"key":"BFnature17144_CR39","doi-asserted-by":"publisher","first-page":"663","DOI":"10.1038\/nrn1932","volume":"7","author":"BL McNaughton","year":"2006","unstructured":"McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I. & Moser, M. B. Path integration and the neural basis of the \u2018cognitive map\u2019. Nature Rev. Neurosci. 7, 663\u2013678 (2006)","journal-title":"Nature Rev. Neurosci."},{"key":"BFnature17144_CR40","doi-asserted-by":"publisher","first-page":"827","DOI":"10.1002\/hipo.20113","volume":"15","author":"G Buzs\u00e1ki","year":"2005","unstructured":"Buzs\u00e1ki, G. Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15, 827\u2013840 (2005)","journal-title":"Hippocampus"},{"key":"BFnature17144_CR41","doi-asserted-by":"publisher","first-page":"656","DOI":"10.1002\/hipo.22124","volume":"23","author":"AJ Watrous","year":"2013","unstructured":"Watrous, A. J. et al. A comparative study of human and rat hippocampal low-frequency oscillations during spatial navigation. Hippocampus 23, 656\u2013661 (2013)","journal-title":"Hippocampus"},{"key":"BFnature17144_CR42","doi-asserted-by":"publisher","first-page":"13144","DOI":"10.1073\/pnas.1302351110","volume":"110","author":"MJ Jutras","year":"2013","unstructured":"Jutras, M. J., Fries, P. & Buffalo, E. A. Oscillatory activity in the monkey hippocampus during visual exploration and memory formation. Proc. Natl Acad. Sci. USA 110, 13144\u201313149 (2013)","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFnature17144_CR43","doi-asserted-by":"publisher","first-page":"224","DOI":"10.1038\/nn1829","volume":"10","author":"N Ulanovsky","year":"2007","unstructured":"Ulanovsky, N. & Moss, C. F. Hippocampal cellular and network activity in freely moving echolocating bats. Nature Neurosci. 10, 224\u2013233 (2007)","journal-title":"Nature Neurosci."},{"key":"BFnature17144_CR44","doi-asserted-by":"publisher","first-page":"1183","DOI":"10.1016\/S0896-6273(02)01096-6","volume":"36","author":"AK Lee","year":"2002","unstructured":"Lee, A. K. & Wilson, M. A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36, 1183\u20131194 (2002)","journal-title":"Neuron"},{"key":"BFnature17144_CR45","doi-asserted-by":"publisher","first-page":"1222","DOI":"10.1038\/nn.2384","volume":"12","author":"G Girardeau","year":"2009","unstructured":"Girardeau, G., Benchenane, K., Wiener, S. I., Buzsaki, G. & Zugaro, M. B. Selective suppression of hippocampal ripples impairs spatial memory. Nature Neurosci. 12, 1222\u20131223 (2009)","journal-title":"Nature Neurosci."},{"key":"BFnature17144_CR46","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/hipo.20707","volume":"20","author":"V Ego-Stengel","year":"2010","unstructured":"Ego-Stengel, V. & Wilson, M. A. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20, 1\u201310 (2010)","journal-title":"Hippocampus"},{"key":"BFnature17144_CR47","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1038\/nrn.2015.22","volume":"17","author":"SM Dudek","year":"2016","unstructured":"Dudek, S. M., Alexander, G. M. & Farris, S. Rediscovering area CA2: unique properties and functions. Nature Rev. Neurosci. 17, 89\u2013102 (2016)","journal-title":"Nature Rev. Neurosci."},{"key":"BFnature17144_CR48","doi-asserted-by":"publisher","first-page":"14889","DOI":"10.1523\/JNEUROSCI.1046-13.2013","volume":"33","author":"DC Rowland","year":"2013","unstructured":"Rowland, D. C. et al. Transgenically targeted rabies virus demonstrates a major monosynaptic projection from hippocampal area CA2 to medial entorhinal layer II neurons. J. Neurosci. 33, 14889\u201314898 (2013)","journal-title":"J. Neurosci."},{"key":"BFnature17144_CR49","doi-asserted-by":"publisher","first-page":"1281","DOI":"10.1038\/nn.4074","volume":"18","author":"M Valero","year":"2015","unstructured":"Valero, M. et al. Determinants of different deep and superficial CA1 pyramidal cell dynamics during sharp-wave ripples. Nature Neurosci. 18, 1281\u20131290 (2015)","journal-title":"Nature Neurosci."},{"key":"BFnature17144_CR50","first-page":"113","volume":"46","author":"R Lorente de N\u00f3","year":"1934","unstructured":"Lorente de N\u00f3, R. Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. Journal f\u00fcr Psychologie und Neurologie . 46, 113\u2013177 (1934)","journal-title":"II. Continuation of the study of the ammonic system. Journal f\u00fcr Psychologie und Neurologie"},{"key":"BFnature17144_CR51","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1016\/0165-0270(95)00085-2","volume":"63","author":"CM Gray","year":"1995","unstructured":"Gray, C. M., Maldonado, P. E., Wilson, M. & McNaughton, B. Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex. J. Neurosci. Methods 63, 43\u201354 (1995)","journal-title":"J. Neurosci. Methods"},{"key":"BFnature17144_CR52","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1016\/j.mcn.2008.10.003","volume":"40","author":"GB Potter","year":"2009","unstructured":"Potter, G. B., et al. Generation of Cre-transgenic mice using Dlx1\/Dlx2 enhancers and their characterization in GABAergic interneurons. Mol. Cell Neurosci. 40, 167\u2013186 (2009)","journal-title":"Mol. Cell Neurosci."},{"key":"BFnature17144_CR53","doi-asserted-by":"publisher","first-page":"3848","DOI":"10.1523\/JNEUROSCI.6038-11.2012","volume":"32","author":"JP Neunuebel","year":"2012","unstructured":"Neunuebel, J. P. & Knierim, J. J. Spatial firing correlates of physiologically distinct cell types of the rat dentate gyrus. J. Neurosci. 32, 3848\u20133858 (2012)","journal-title":"J. Neurosci."},{"key":"BFnature17144_CR54","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1002\/cne.903620103","volume":"362","author":"N Ishizuka","year":"1995","unstructured":"Ishizuka, N., Cowan, W. M. & Amaral, D. G. A quantitative analysis of the dendritic organization of pyramidal cells in the rat hippocampus. J. Comp. Neurol. 362, 17\u201345 (1995)","journal-title":"J. Comp. Neurol."},{"key":"BFnature17144_CR55","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1002\/hipo.1993.4500030733","volume":"3","author":"PL Woodhams","year":"1993","unstructured":"Woodhams, P. L., Celio, M. R., Ulfig, N. & Witter, M. P. Morphological and functional correlates of borders in the entorhinal cortex and hippocampus. Hippocampus 3, 303\u2013311 (1993)","journal-title":"Hippocampus"},{"key":"BFnature17144_CR56","unstructured":"Amaral, D. G. & Lavenex, P. in The Hippocampus Book (eds Andersen, P. et al. ) 37\u2013114 (Oxford Univ. Press, 2007)"},{"key":"BFnature17144_CR57","doi-asserted-by":"publisher","first-page":"1844","DOI":"10.1002\/cne.23263","volume":"521","author":"Z Cui","year":"2013","unstructured":"Cui, Z., Gerfen, C. R. & Young, W. S., III . Hypothalamic and other connections with dorsal CA2 area of the mouse hippocampus. J. Comp. Neurol. 521, 1844\u20131866 (2013)","journal-title":"J. Comp. Neurol."},{"key":"BFnature17144_CR58","doi-asserted-by":"publisher","first-page":"RC20","DOI":"10.1523\/JNEUROSCI.19-16-j0001.1999","volume":"19","author":"J Csicsvari","year":"1999","unstructured":"Csicsvari, J., Hirase, H., Czurko, A., Mamiya, A. & Buzsaki, G. Fast network oscillations in the hippocampal CA1 region of the behaving rat. J. Neurosci . 19, RC20 (1999)","journal-title":"J. Neurosci"},{"key":"BFnature17144_CR59","doi-asserted-by":"publisher","first-page":"462","DOI":"10.1016\/0014-4886(73)90290-2","volume":"41","author":"JB Ranck Jr.","year":"1973","unstructured":"Ranck, J. B. Jr. Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. Exp. Neurol. 41, 462\u2013531 (1973)","journal-title":"Exp. Neurol."},{"key":"BFnature17144_CR60","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1007\/BF00238898","volume":"41","author":"SE Fox","year":"1981","unstructured":"Fox, S. E. & Ranck, J. B. Jr. Electrophysiological characteristics of hippocampal complex-spike cells and theta cells. Exp. Brain Res. 41, 399\u2013410 (1981)","journal-title":"Exp. Brain Res."},{"key":"BFnature17144_CR61","doi-asserted-by":"publisher","first-page":"1870","DOI":"10.1126\/science.271.5257.1870","volume":"271","author":"WE Skaggs","year":"1996","unstructured":"Skaggs, W. E. & McNaughton, B. L. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271, 1870\u20131873 (1996)","journal-title":"Science"},{"key":"BFnature17144_CR62","doi-asserted-by":"publisher","first-page":"274","DOI":"10.1523\/JNEUROSCI.19-01-00274.1999","volume":"19","author":"J Csicsvari","year":"1999","unstructured":"Csicsvari, J., Hirase, H., Czurko, A., Mamiya, A. & Buzsaki, G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J. Neurosci. 19, 274\u2013287 (1999)","journal-title":"J. Neurosci."},{"key":"BFnature17144_CR63","doi-asserted-by":"publisher","first-page":"e73114","DOI":"10.1371\/journal.pone.0073114","volume":"8","author":"C Kemere","year":"2013","unstructured":"Kemere, C., Carr, M. F., Karlsson, M. P. & Frank, L. M. Rapid and continuous modulation of hippocampal network state during exploration of new places. PLoS ONE 8, e73114 (2013)","journal-title":"PLoS ONE"},{"key":"BFnature17144_CR64","doi-asserted-by":"publisher","first-page":"e21408","DOI":"10.1371\/journal.pone.0021408","volume":"6","author":"Z Chen","year":"2011","unstructured":"Chen, Z., Resnik, E., McFarland, J. M., Sakmann, B. & Mehta, M. R. Speed controls the amplitude and timing of the hippocampal gamma rhythm. PLoS ONE 6, e21408 (2011)","journal-title":"PLoS ONE"},{"key":"BFnature17144_CR65","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1016\/S0896-6273(00)00018-0","volume":"27","author":"LM Frank","year":"2000","unstructured":"Frank, L. M., Brown, E. N. & Wilson, M. Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27, 169\u2013178 (2000)","journal-title":"Neuron"},{"key":"BFnature17144_CR66","doi-asserted-by":"publisher","first-page":"623","DOI":"10.1016\/S0896-6273(00)00071-4","volume":"27","author":"ER Wood","year":"2000","unstructured":"Wood, E. R., Dudchenko, P. A., Robitsek, R. J. & Eichenbaum, H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27, 623\u2013633 (2000)","journal-title":"Neuron"},{"key":"BFnature17144_CR67","doi-asserted-by":"publisher","first-page":"50","DOI":"10.1038\/nature14396","volume":"522","author":"HT Ito","year":"2015","unstructured":"Ito, H. T., Zhang, S. J., Witter, M. P., Moser, E. I. & Moser, M. B. A prefrontal-thalamo-hippocampal circuit for goal-directed spatial navigation. Nature 522, 50\u201355 (2015)","journal-title":"Nature"},{"key":"BFnature17144_CR68","doi-asserted-by":"publisher","first-page":"534","DOI":"10.1038\/nature08010","volume":"459","author":"EV Lubenov","year":"2009","unstructured":"Lubenov, E. V. & Siapas, A. G. Hippocampal theta oscillations are travelling waves. Nature 459, 534\u2013539 (2009)","journal-title":"Nature"},{"key":"BFnature17144_CR69","doi-asserted-by":"publisher","first-page":"1174","DOI":"10.1038\/nn.2894","volume":"14","author":"K Mizuseki","year":"2011","unstructured":"Mizuseki, K., Diba, K., Pastalkova, E. & Buzsaki, G. Hippocampal CA1 pyramidal cells form functionally distinct sublayers. Nature Neurosci. 14, 1174\u20131181 (2011)","journal-title":"Nature Neurosci."},{"key":"BFnature17144_CR70","doi-asserted-by":"publisher","first-page":"1454","DOI":"10.1126\/science.1217230","volume":"336","author":"SP Jadhav","year":"2012","unstructured":"Jadhav, S. P., Kemere, C., German, P. W. & Frank, L. M. Awake hippocampal sharp-wave ripples support spatial memory. Science 336, 1454\u20131458 (2012)","journal-title":"Science"},{"key":"BFnature17144_CR71","doi-asserted-by":"publisher","first-page":"16994","DOI":"10.1073\/pnas.1005362107","volume":"107","author":"SE Lee","year":"2010","unstructured":"Lee, S. E. et al. RGS14 is a natural suppressor of both synaptic plasticity in CA2 neurons and hippocampal-based learning and memory. Proc. Natl Acad. Sci. USA 107, 16994\u201316998 (2010)","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFnature17144_CR72","doi-asserted-by":"publisher","first-page":"348","DOI":"10.1016\/0013-4694(87)90123-4","volume":"67","author":"SS Suzuki","year":"1987","unstructured":"Suzuki, S. S. & Smith, G. K. Spontaneous EEG spikes in the normal hippocampus. I. Behavioral correlates, laminar profiles and bilateral synchrony. Electroencephalogr. Clin. Neurophysiol. 67, 348\u2013359 (1987)","journal-title":"Electroencephalogr. Clin. Neurophysiol."},{"key":"BFnature17144_CR73","doi-asserted-by":"publisher","first-page":"551","DOI":"10.1016\/0306-4522(89)90423-5","volume":"31","author":"G Buzs\u00e1ki","year":"1989","unstructured":"Buzs\u00e1ki, G. Two-stage model of memory trace formation: a role for \u201cnoisy\u201d brain states. Neuroscience 31, 551\u2013570 (1989)","journal-title":"Neuroscience"},{"key":"BFnature17144_CR74","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1016\/S0896-6273(01)00447-0","volume":"32","author":"KD Harris","year":"2001","unstructured":"Harris, K. D., Hirase, H., Leinekugel, X., Henze, D. A. & Buzsaki, G. Temporal interaction between single spikes and complex spike bursts in hippocampal pyramidal cells. Neuron 32, 141\u2013149 (2001)","journal-title":"Neuron"},{"key":"BFnature17144_CR75","doi-asserted-by":"publisher","first-page":"1659","DOI":"10.1002\/hipo.22002","volume":"22","author":"K Mizuseki","year":"2012","unstructured":"Mizuseki, K., Royer, S., Diba, K. & Buzsaki, G. Activity dynamics and behavioral correlates of CA3 and CA1 hippocampal pyramidal neurons. Hippocampus 22, 1659\u20131680 (2012)","journal-title":"Hippocampus"},{"key":"BFnature17144_CR76","doi-asserted-by":"publisher","first-page":"941","DOI":"10.1038\/nature08499","volume":"461","author":"CD Harvey","year":"2009","unstructured":"Harvey, C. D., Collman, F., Dombeck, D. A. & Tank, D. W. Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461, 941\u2013946 (2009)","journal-title":"Nature"},{"key":"BFnature17144_CR77","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1016\/j.neuron.2011.03.006","volume":"70","author":"J Epsztein","year":"2011","unstructured":"Epsztein, J., Brecht, M. & Lee, A. K. Intracellular determinants of hippocampal CA1 place and silent cell activity in a novel environment. Neuron 70, 109\u2013120 (2011)","journal-title":"Neuron"},{"key":"BFnature17144_CR78","doi-asserted-by":"publisher","first-page":"1274","DOI":"10.1016\/j.neuron.2014.01.014","volume":"81","author":"C Grienberger","year":"2014","unstructured":"Grienberger, C., Chen, X. & Konnerth, A. NMDA receptor-dependent multidendrite Ca(2+) spikes required for hippocampal burst firing in vivo. Neuron 81, 1274\u20131281 (2014)","journal-title":"Neuron"},{"key":"BFnature17144_CR79","doi-asserted-by":"publisher","first-page":"1133","DOI":"10.1038\/nn.4062","volume":"18","author":"KC Bittner","year":"2015","unstructured":"Bittner, K. C. et al. Conjunctive input processing drives feature selectivity in hippocampal CA1 neurons. Nature Neurosci. 18, 1133\u20131142 (2015)","journal-title":"Nature Neurosci."},{"key":"BFnature17144_CR80","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1126\/science.1149381","volume":"321","author":"T Klausberger","year":"2008","unstructured":"Klausberger, T. & Somogyi, P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321, 53\u201357 (2008)","journal-title":"Science"},{"key":"BFnature17144_CR81","doi-asserted-by":"publisher","first-page":"14984","DOI":"10.1523\/JNEUROSCI.1091-14.2014","volume":"34","author":"K Diba","year":"2014","unstructured":"Diba, K., Amarasingham, A., Mizuseki, K. & Buzsaki, G. Millisecond timescale synchrony among hippocampal neurons. J. Neurosci. 34, 14984\u201314994 (2014)","journal-title":"J. Neurosci."},{"key":"BFnature17144_CR82","doi-asserted-by":"publisher","first-page":"769","DOI":"10.1038\/nn.3077","volume":"15","author":"S Royer","year":"2012","unstructured":"Royer, S. et al. Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nature Neurosci. 15, 769\u2013775 (2012)","journal-title":"Nature Neurosci."},{"key":"BFnature17144_CR83","unstructured":"Skaggs, W. E., McNaughton, B. L., Gothard, K. & Markus, E. in Advanced in Neural Information Processing Systems (eds Hanson, S., Cowan, J. D. & Giles, C. L. ) 1030\u20131037 (Morgan Kaufmann, 1993)"}],"container-title":["Nature"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.nature.com\/articles\/nature17144.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/nature17144","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/nature17144.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,6,14]],"date-time":"2024-06-14T14:38:45Z","timestamp":1718375925000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/nature17144"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,3]]},"references-count":83,"journal-issue":{"issue":"7593","published-print":{"date-parts":[[2016,3]]}},"alternative-id":["BFnature17144"],"URL":"https:\/\/doi.org\/10.1038\/nature17144","relation":{"has-review":[{"id-type":"doi","id":"10.3410\/f.726189598.793535288","asserted-by":"object"}]},"ISSN":["0028-0836","1476-4687"],"issn-type":[{"value":"0028-0836","type":"print"},{"value":"1476-4687","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,3]]},"assertion":[{"value":"9 June 2015","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"13 January 2016","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 March 2016","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}