Integrating time from experience in the lateral entorhinal cortex
Open accessAbstract
The encoding of time and its binding to events are crucial for episodic memory, but how these processes are carried out in hippocampal-entorhinal circuits is unclear. Here we show in freely foraging rats that temporal information is robustly encoded across time scales from seconds to hours within the overall population state of the lateral entorhinal cortex. Similarly pronounced encoding of time was not present in the medial entorhinal cortex or in hippocampal areas CA3-CA1. When animals' experiences were constrained by behavioural tasks to become similar across repeated trials, the encoding of temporal flow across trials was reduced, whereas the encoding of time relative to the start of trials was improved. The findings suggest that populations of lateral entorhinal cortex neurons represent time inherently through the encoding of experience. This representation of episodic time may be integrated with spatial inputs from the medial entorhinal cortex in the hippocampus, allowing the hippocampus to store a unified representation of what, where and when.
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?
Populations of LEC neurons also encode temporal information across different contexts.
“Intriguingly, populations of LEC neurons also encode temporal information across different contexts (Tsao et al., 2018).”
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 Tsao et al., 2018
The LEC is a functional hub for integrating multisensory information, including both spatial and non-spatial characteristics, probably even time.
“This matches the anatomical features of LEC, as being a functional hub for integrating multisensory information (Bota et al., 2015), including both spatial and non-spatial characteristics, probably even time (Tsao et al., 2018).”
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 Tsao et al., 2018
Cites
LIBLINEAR: A Library for Large Linear Classification
Fan, R.-E., Chang, K., Hsieh, C., Xiang-rui, W., & Lin, C. (2008) · doi:10.5555/1390681.1442794 · Cited by 6,680 · see citing works
On the Surprising Behavior of Distance Metrics in High Dimensional Space
Aggarwal, C. C., Hinneburg, A., & Keim, D. A. (2001) · Lecture notes in computer science · doi:10.1007/3-540-44503-x_27 · Cited by 2,179 · see citing works
The importance of mixed selectivity in complex cognitive tasks
Rigotti, M., Barak, O., Warden, M. R., Wang, X.-J., Daw, N. D., Miller, E. K., & Fusi, S. (2013) · Nature · doi:10.1038/nature12160 · Cited by 1,639 · see citing works
Episodic-like memory during cache recovery by scrub jays
Clayton, N. S., & Dickinson, A. (1998) · Nature · doi:10.1038/26216 · Cited by 1,464 · see citing works
Internally Generated Cell Assembly Sequences in the Rat Hippocampus
Pastalkova, E., Itskov, V., Amarasingham, A., & Buzsáki, G. (2008) · Science · doi:10.1126/science.1159775 · Cited by 1,301 · see citing works
Deconstructing episodic memory with construction
Hassabis, D., & Maguire, E. A. (2007) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2007.05.001 · Cited by 1,229 · see citing works
Hippocampal ‘time cells’ bridge the gap in memory for discontiguous events
MacDonald, C. J., Lepage, K. Q., Eden, U. T., & Eichenbaum, H. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.012 · Cited by 1,193 · see citing works
A Distributed Representation of Temporal Context
Howard, M. W., & Kahana, M. J. (2002) · Journal of Mathematical Psychology · doi:10.1006/jmps.2001.1388 · Cited by 1,174 · see citing works
Long-term dynamics of CA1 hippocampal place codes
Ziv, Y., Burns, L. D., Cocker, E. D., Hamel, E. O., Ghosh, K. K., Kitch, L. J., Gamal, A. E., & Schnitzer, M. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3329 · Cited by 1,155 · see citing works
Wood, E. R., Dudchenko, P. A., Robitsek, R. J., & Eichenbaum, H. (2000) · Neuron · doi:10.1016/s0896-6273(00)00071-4 · Cited by 992 · see citing works
The neural basis of temporal processing
Mauk, M. D., & Buonomano, D. V. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144247 · Cited by 976 · see citing works
A shared neural ensemble links distinct contextual memories encoded close in time
Cai, D. J., Aharoni, D. B., Shuman, T., Shobe, J. L., Biane, J. S., Song, W., Wei, B., Veshkini, M., La-Vu, M. Q., Lou, J. J., et al. (2016) · Nature · doi:10.1038/nature17955 · Cited by 947 · see citing works
State-dependent computations: spatiotemporal processing in cortical networks
Buonomano, D. V., & Maass, W. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2558 · Cited by 919 · see citing works
Critical role of the hippocampus in memory for sequences of events
Fortin, N. J., Agster, K. L., & Eichenbaum, H. B. (2002) · Nature Neuroscience · doi:10.1038/nn834 · Cited by 881 · see citing works
Time cells in the hippocampus: a new dimension for mapping memories
Eichenbaum, H. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3827 · Cited by 843 · see citing works
Neural Basis of the Perception and Estimation of Time
Merchant, H., Harrington, D. L., & Meck, W. H. (2013) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062012-170349 · Cited by 710 · see citing works
Major Dissociation Between Medial and Lateral Entorhinal Input to Dorsal Hippocampus
Hargreaves, E. L., Rao, G., Lee, I., & Knierim, J. J. (2005) · Science · doi:10.1126/science.1110449 · Cited by 685 · see citing works
Self-citationSpeed cells in the medial entorhinal cortex
Kropff, E., Carmichael, J. E., Moser, M.-B., & Moser, E. I. (2015) · Nature · doi:10.1038/nature14622 · Cited by 668 · see citing works
Self-citationDevelopment of the Spatial Representation System in the Rat
Langston, R. F., Ainge, J. A., Couey, J. J., Canto, C. B., Bjerknes, T. L., Witter, M. P., Moser, E. I., & Moser, M. (2010) · Science · doi:10.1126/science.1188210 · Cited by 667 · see citing works
Self-citationOn the Integration of Space, Time, and Memory
Eichenbaum, H. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.036 · Cited by 512 · see citing works
Representation of Non-Spatial and Spatial Information in the Lateral Entorhinal Cortex
Deshmukh, S. S., & Knierim, J. J. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00069 · Cited by 454 · see citing works
Self-citationCoordination of entorhinal–hippocampal ensemble activity during associative learning
Igarashi, K. M., Lu, L., Colgin, L. L., Moser, M., & Moser, E. I. (2014) · Nature · doi:10.1038/nature13162 · Cited by 435 · see citing works
Self-citationGradual changes in hippocampal activity support remembering the order of events
Manns, J. R., Howard, M. W., & Eichenbaum, H. (2007) · Neuron · doi:10.1016/j.neuron.2007.08.017 · Cited by 397 · see citing works
Neuronal code for extended time in the hippocampus
Mankin, E. A., Sparks, F. T., Slayyeh, B., Sutherland, R. J., Leutgeb, S., & Leutgeb, J. K. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1214107109 · Cited by 371 · see citing works
Hippocampal Activity Patterns Carry Information about Objects in Temporal Context
Hsieh, L., Gruber, M. J., Jenkins, L. J., & Charan Ranganath, A. (2014) · Neuron · doi:10.1016/j.neuron.2014.01.015 · Cited by 347 · see citing works
Ezzyat, Y., & Davachi, L. (2014) · Neuron · doi:10.1016/j.neuron.2014.01.042 · Cited by 321 · see citing works
The role of the hippocampus in memory for the temporal order of a sequence of odors.
Kesner, R. P., Gilbert, P. E., & Barua, L. A. (2002) · Behavioral Neuroscience · doi:10.1037//0735-7044.116.2.286 · Cited by 309 · see citing works
During Running in Place, Grid Cells Integrate Elapsed Time and Distance Run
Kraus, B. J., Brandon, M. P., Robinson, R. J., Connerney, M. A., Hasselmo, M. E., & Eichenbaum, H. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.031 · Cited by 293 · see citing works
Traces of experience in the lateral entorhinal cortex
Tsao, A., Moser, M.-B., & Moser, E. I. (2013) · Current Biology · doi:10.1016/j.cub.2013.01.036 · Cited by 290 · see citing works
Self-citationHippocampal CA2 activity patterns change over time to a larger extent than between spatial contexts
Mankin, E. A., Diehl, G. W., Sparks, F. T., Leutgeb, S., & Leutgeb, J. K. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.001 · Cited by 279 · see citing works
Entorhinal cortex of the rat: Organization of intrinsic connections
Dolorfo, C. L., & Amaral, D. G. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980817)398:1 · Cited by 268 · see citing works
Hippocampal ensemble dynamics timestamp events in long-term memory
Rubin, A., Geva, N., Sheintuch, L., & Ziv, Y. (2015) · eLife · doi:10.7554/elife.12247 · Cited by 266 · see citing works
The role of the hippocampus in memory for the temporal order of a sequence of odors.
Kesner, R. P., Gilbert, P. E., & Barua, L. A. (2002) · Behavioral Neuroscience · doi:10.1037/0735-7044.116.2.286 · Cited by 261 · see citing works
Integrating what and when across the primate medial temporal lobe
Naya, Y., & Suzuki, W. A. (2011) · Science · doi:10.1126/science.1206773 · Cited by 257 · see citing works
Neural representation of time in cortico-basal ganglia circuits
Jin, D. Z., Fujii, N., & Graybiel, A. M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909881106 · Cited by 246 · see citing works
Architecture of the cerebral cortical association connectome underlying cognition
Bota, M., Sporns, O., & Swanson, L. W. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1504394112 · Cited by 231 · see citing works
Contextual encoding by ensembles of medial prefrontal cortex neurons
Hyman, J. M., Ma, L., Balaguer‐Ballester, E., Durstewitz, D., & Seamans, J. K. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114415109 · Cited by 222 · see citing works
Rowland, D. C., Roudi, Y., Moser, M., & Moser, E. I. (2016) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070815-013824 · Cited by 219 · see citing works
Self-citationA Unified Mathematical Framework for Coding Time, Space, and Sequences in the Hippocampal Region
Howard, M. W., MacDonald, C. J., Tiganj, Z., Shankar, K. H., Du, Q., Hasselmo, M. E., & Eichenbaum, H. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.5808-12.2014 · Cited by 195 · see citing works
Mau, W., Sullivan, D. W., Kinsky, N. R., Hasselmo, M. E., Howard, M. W., & Eichenbaum, H. (2018) · Current Biology · doi:10.1016/j.cub.2018.03.051 · Cited by 186 · see citing works
A Specific Role of the Human Hippocampus in Recall of Temporal Sequences
Lehn, H., Steffenach, H.-A., van Strien, N. M., Veltman, D. J., Witter, M. P., & Haberg, A. K. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5370-08.2009 · Cited by 177 · see citing works
Buzsáki, G., & Llinás, R. (2017) · Science · doi:10.1126/science.aan8869 · Cited by 175 · see citing works
Topography of Place Maps along the CA3-to-CA2 Axis of the Hippocampus
Lu, L., Igarashi, K. M., Witter, M. P., Moser, E. I., & Moser, M. (2015) · Neuron · doi:10.1016/j.neuron.2015.07.007 · Cited by 149 · see citing works
Self-citationEkstrom, A. D., & Bookheimer, S. Y. (2007) · Learning & Memory · doi:10.1101/lm.575107 · Cited by 139 · see citing works
McEchron, M. D., Tseng, W., & Disterhoft, J. F. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-04-01535.2003 · Cited by 136 · see citing works
Keene, C. S., Bladon, J. H., McKenzie, S., Liu, C. D., O'Keefe, J., & Eichenbaum, H. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.4368-15.2016 · Cited by 131 · see citing works
Impaired hippocampal rate coding after lesions of the lateral entorhinal cortex
Lu, L., Leutgeb, J. K., Tsao, A., Henriksen, E. J., Leutgeb, S., Barnes, C. A., Witter, M. P., Moser, M., & Moser, E. I. (2013) · Nature Neuroscience · doi:10.1038/nn.3462 · Cited by 108 · see citing works
Self-citationFinnerty, G. T., Shadlen, M. N., Jazayeri, M., Nobre, A. C., & Buonomano, D. V. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2654-15.2015 · Cited by 100 · see citing works
Learning and remembering real-world events after medial temporal lobe damage
Dede, A. J. O., Frascino, J. C., Wixted, J. T., & Squire, L. R. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1617025113 · Cited by 99 · see citing works
Human Episodic Memory Retrieval Is Accompanied by a Neural Contiguity Effect
Folkerts, S., Rutishauser, U., & Howard, M. W. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2312-17.2018 · Cited by 97 · see citing works
Episodic memory—From brain to mind
Ferbinteanu, J., Kennedy, P., & Shapiro, M. L. (2006) · Hippocampus · doi:10.1002/hipo.20204 · Cited by 92 · see citing works
Pilkiw, M., Insel, N., Cui, Y., Finney, C. A., Morrissey, M. D., & Takehara‐Nishiuchi, K. (2017) · eLife · doi:10.7554/elife.28611 · Cited by 35 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Whittington, J. C. R., Muller, T. H., Mark, S., Chen, G., Barry, C., Burgess, N., & Behrens, T. E. J. (2020) · Cell · doi:10.1016/j.cell.2020.10.024 · Cited by 660 · see citing works
Navigating cognition: Spatial codes for human thinking
Bellmund, J. L. S., Gärdenfors, P., Moser, E. I., & Doeller, C. F. (2018) · Science · doi:10.1126/science.aat6766 · Cited by 643 · see citing works
Self-citationDentate gyrus circuits for encoding, retrieval and discrimination of episodic memories
Hainmueller, T., & Bartos, M. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0260-z · Cited by 474 · see citing works
Thirst regulates motivated behavior through modulation of brainwide neural population dynamics
Allen, W. E., Chen, M. Z., Pichamoorthy, N., Tien, R. H., Pachitariu, M., Luo, L., & Deisseroth, K. A. (2019) · Science · doi:10.1126/science.aav3932 · Cited by 362 · see citing works
Time cells in the human hippocampus and entorhinal cortex support episodic memory
Umbach, G. S., Kantak, P. A., Jacobs, J., Kahana, M. J., Pfeiffer, B. E., Sperling, M. R., & Lega, B. C. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2013250117 · Cited by 236 · see citing works
Transcending time in the brain: How event memories are constructed from experience
Clewett, D., DuBrow, S., & Davachi, L. (2019) · Hippocampus · doi:10.1002/hipo.23074 · Cited by 233 · see citing works
Gamma rhythm communication between entorhinal cortex and dentate gyrus neuronal assemblies
Fernández‐Ruiz, A., Oliva, A., Soula, M., Rocha-Almeida, F., Nagy, G. A., Martín-Vázquez, G., & Buzsáki, G. (2021) · Science · doi:10.1126/science.abf3119 · Cited by 228 · see citing works
Representational drift in the mouse visual cortex
Deitch, D., Rubin, A., & Ziv, Y. (2021) · Current Biology · doi:10.1016/j.cub.2021.07.062 · Cited by 227 · see citing works
Mesolimbic dopamine release conveys causal associations
Jeong, H., Taylor, A., Floeder, J. R., Lohmann, M., Mihalaş, Ş., Wu, B., Zhou, M., Burke, D. A., & Namboodiri, V. M. K. (2022) · Science · doi:10.1126/science.abq6740 · Cited by 226 · see citing works
Re-evaluating Circuit Mechanisms Underlying Pattern Separation
Cayco-Gajic, N. A., & Silver, R. A. (2019) · Neuron · doi:10.1016/j.neuron.2019.01.044 · Cited by 220 · see citing works
Ährlund‐Richter, S., Xuan, Y., van Lunteren, J. A., Kim, H., Ortiz, C., Dorocic, I. P., Meletis, K., & Carlén, M. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0354-y · Cited by 212 · see citing works
Behavioral state coding by molecularly defined paraventricular hypothalamic cell type ensembles
Xu, S., Yang, H., Menon, V., Lemire, A. L., Wang, L., Henry, F. E., Turaga, S. C., & Sternson, S. M. (2020) · Science · doi:10.1126/science.abb2494 · Cited by 197 · see citing works
Episodic memory: Neuronal codes for what, where, and when
Sugar, J., & Moser, M. (2019) · Hippocampus · doi:10.1002/hipo.23132 · Cited by 196 · see citing works
Self-citationNilssen, E. S., Doan, T. P., Nigro, M. J., Ohara, S., & Witter, M. P. (2019) · Hippocampus · doi:10.1002/hipo.23145 · Cited by 178 · 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
Neuronal circuitry for recognition memory of object and place in rodent models
Chao, O. Y.-H., Nikolaus, S., Yang, Y., & Huston, J. P. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104855 · Cited by 157 · see citing works
Werning, M. (2020) · Review of Philosophy and Psychology · doi:10.1007/s13164-020-00471-z · Cited by 151 · see citing works
The hippocampus, ventromedial prefrontal cortex, and episodic and semantic memory
Rolls, E. T. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102334 · Cited by 144 · see citing works
Sosa, M., & Giocomo, L. M. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00479-z · Cited by 142 · see citing works
Precise temporal memories are supported by the lateral entorhinal cortex in humans
Montchal, M. E., Reagh, Z. M., & Yassa, M. A. (2019) · Nature Neuroscience · doi:10.1038/s41593-018-0303-1 · Cited by 142 · see citing works
The brain in motion: How ensemble fluidity drives memory-updating and flexibility
Mau, W., Hasselmo, M. E., & Cai, D. J. (2020) · eLife · doi:10.7554/elife.63550 · Cited by 139 · see citing works
Assessments of dentate gyrus function: discoveries and debates
Borzello, M., Ramirez, S., Treves, A., Lee, I., Scharfman, H. E., Stark, C. E. L., Knierim, J. J., & Rangel, L. M. (2023) · Nature reviews. Neuroscience · doi:10.1038/s41583-023-00710-z · Cited by 138 · see citing works
Self-citationTaxidis, J., Pnevmatikakis, E. A., Dorian, C. C., Mylavarapu, A. L., Arora, J. S., Samadian, K. D., Hoffberg, E. A., & Golshani, P. (2020) · Neuron · doi:10.1016/j.neuron.2020.08.028 · Cited by 136 · see citing works
Hippocampal neurons represent events as transferable units of experience
Sun, C., Yang, W., Martin, J., & Tonegawa, S. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0614-x · Cited by 135 · see citing works
Lopez‐Rojas, J., de Solis, C. A., Leroy, F., Kandel, E. R., & Siegelbaum, S. A. (2022) · Neuron · doi:10.1016/j.neuron.2022.01.028 · Cited by 122 · see citing works
Chen, Y., Chen, X., Başerdem, B., Zhan, H., Li, Y., Davis, M. B., Kebschull, J. M., Zador, A. M., Koulakov, A. A., & Albeanu, D. F. (2022) · Cell · doi:10.1016/j.cell.2022.09.038 · Cited by 119 · see citing works
Kobro-Flatmoen, A., Lagartos-Donate, M. J., Aman, Y., Edison, P., Witter, M. P., & Fang, E. F. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101307 · Cited by 112 · see citing works
Selection of experience for memory by hippocampal sharp wave ripples
Yang, W., Sun, C., Huszár, R., Hainmueller, T., Kiselev, K., & Buzsáki, G. (2024) · Science · doi:10.1126/science.adk8261 · Cited by 116 · see citing works
The neural bases for timing of durations
Tsao, A., Yousefzadeh, S. A., Meck, W. H., Moser, M., & Moser, E. I. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00623-3 · Cited by 109 · see citing works
Self-citationHuang, C., Rolls, E. T., Hsu, C. H., Feng, J., & Lin, C. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab113 · Cited by 107 · see citing works
A generative model of memory construction and consolidation
Spens, E., & Burgess, N. (2024) · Nature Human Behaviour · doi:10.1038/s41562-023-01799-z · Cited by 101 · see citing works
A temporal record of the past with a spectrum of time constants in the monkey entorhinal cortex
Bright, I. M., Meister, M. L. R., Cruzado, N. A., Tiganj, Z., Buffalo, E. A., & Howard, M. W. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1917197117 · Cited by 99 · see citing works
Neural Sequences as an Optimal Dynamical Regime for the Readout of Time
Zhou, S., Masmanidis, S. C., & Buonomano, D. V. (2020) · Neuron · doi:10.1016/j.neuron.2020.08.020 · Cited by 99 · see citing works
Do hippocampal pyramidal cells respond to nonspatial stimuli?
O’Keefe, J., & Krupic, J. (2021) · Physiological Reviews · doi:10.1152/physrev.00014.2020 · Cited by 93 · see citing works
Mapping sequence structure in the human lateral entorhinal cortex
Bellmund, J. L. S., Deuker, L., & Doeller, C. F. (2019) · eLife · doi:10.7554/elife.45333 · Cited by 93 · see citing works
The representation of context in mouse hippocampus is preserved despite neural drift
Keinath, A. T., Mosser, C., & Brandon, M. P. (2022) · Nature Communications · doi:10.1038/s41467-022-30198-7 · Cited by 92 · see citing works
Doan, T. P., Lagartos-Donate, M. J., Nilssen, E. S., Ohara, S., & Witter, M. P. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.09.005 · Cited by 91 · see citing works
Scalable representation of time in the hippocampus
Shimbo, A., Izawa, E., & Fujisawa, S. (2021) · Science Advances · doi:10.1126/sciadv.abd7013 · Cited by 91 · see citing works
Rolls, E. T., Wirth, S., Deco, G., Huang, C., & Feng, J. (2022) · Human Brain Mapping · doi:10.1002/hbm.26089 · Cited by 90 · see citing works
Brain-inspired multimodal hybrid neural network for robot place recognition
Yu, F., Wu, Y., Ma, S., Xu, M., Li, H., Qu, H., Song, C., Wang, T., Zhao, R. J., & Shi, L. (2023) · Science Robotics · doi:10.1126/scirobotics.abm6996 · Cited by 87 · see citing works
Human Hippocampal Neurons Track Moments in a Sequence of Events
Reddy, L., Zoefel, B., Possel, J. K., Peters, J. C., Dijksterhuis, D. E., Poncet, M., van Straaten, E. C. W., Baayen, J. C., Idema, S., & Self, M. W. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.3157-20.2021 · Cited by 84 · see citing works
Billig, A. J., Lad, M., Sedley, W., & Griffiths, T. D. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102326 · Cited by 84 · see citing works
Anatomy and Function of the Primate Entorhinal Cortex
Garcia, A. D., & Buffalo, E. A. (2020) · Annual Review of Vision Science · doi:10.1146/annurev-vision-030320-041115 · Cited by 83 · see citing works
Rolls, E. T. (2022) · Hippocampus · doi:10.1002/hipo.23467 · Cited by 82 · see citing works
Spike frequency adaptation supports network computations on temporally dispersed information
Salaj, D., Subramoney, A., Kraišniković, C., Bellec, G., Legenstein, R. A., & Maass, W. (2021) · eLife · doi:10.7554/elife.65459 · Cited by 80 · see citing works
Fan Cells in Layer 2 of the Lateral Entorhinal Cortex Are Critical for Episodic-like Memory
Vandrey, B., Garden, D. L. F., Ambrozova, V., McClure, C., Nolan, M. F., & Ainge, J. A. (2019) · Current Biology · doi:10.1016/j.cub.2019.11.027 · Cited by 78 · see citing works
The effective connectivity of the human hippocampal memory system
Rolls, E. T., Deco, G., Huang, C., & Feng, J. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab442 · Cited by 78 · see citing works
Single-Neuron Representations of Spatial Targets in Humans
Tsitsiklis, M., Miller, J. F., Qasim, S. E., Inman, C. S., Gross, R. E., Willie, J. T., Smith, E. H., Sheth, S. A., Schevon, C. A., Sperling, M. R., et al. (2020) · Current Biology · doi:10.1016/j.cub.2019.11.048 · Cited by 74 · see citing works
Mesoscopic Neural Representations in Spatial Navigation
Kunz, L., Maidenbaum, S., Chen, D., Wang, L., Jacobs, J., & Axmacher, N. (2019) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2019.04.011 · Cited by 67 · see citing works
Densities and numbers of calbindin and parvalbumin positive neurons across the rat and mouse brain
Bjerke, I. E., Yates, S. C., Laja, A., Witter, M. P., Puchades, M. A., Bjaalie, J. G., & Leergaard, T. B. (2020) · iScience · doi:10.1016/j.isci.2020.101906 · Cited by 66 · see citing works
GoodSmith, D., Lee, H., Neunuebel, J. P., Song, H., & Knierim, J. J. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0940-19.2019 · Cited by 65 · see citing works
Self-citationThe Generation of Time in the Hippocampal Memory System
Rolls, E. T., & Mills, P. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.07.042 · Cited by 62 · see citing works
A Predictive Processing Model of Episodic Memory and Time Perception
Fountas, Z., Sylaidi, A., Nikiforou, K., Seth, A. K., Shanahan, M., & Roseboom, W. (2022) · Neural Computation · doi:10.1162/neco_a_01514 · Cited by 61 · see citing works
Exercise-induced enhancement of synaptic function triggered by the inverse BAR protein, Mtss1L
Chatzi, C. A., Zhang, Y., Hendricks, W. D., Chen, Y., Schnell, E., Goodman, R. H., & Westbrook, G. L. (2019) · eLife · doi:10.7554/elife.45920 · Cited by 60 · see citing works
Self-agency and self-ownership in cognitive mapping
Arzy, S., & Schacter, D. (2019) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2019.04.003 · Cited by 48 · see citing works
Sleep restores an optimal computational regime in cortical networks
Xu, Y., Schneider, A. M., Weßel, R., & Hengen, K. B. (2024) · Nature Neuroscience · doi:10.1038/s41593-023-01536-9 · Cited by 59 · see citing works
Predicting the Future with Multi-scale Successor RepresentationsPreprint
Momennejad, I., & Howard, M. W. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/449470 · Cited by 59 · see citing works
Thavabalasingam, S., O’Neil, E. B., Tay, J., Nestor, A., & Lee, A. C. H. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1819993116 · Cited by 58 · see citing works
The tie that binds: temporal coding and adaptive emotion
Wang, J., Tambini, A., & Lapate, R. C. (2022) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2022.09.005 · Cited by 58 · see citing works
Bowler, J. C., & Losonczy, A. (2023) · Neuron · doi:10.1016/j.neuron.2023.09.013 · Cited by 55 · see citing works
Sequence Memory in the Hippocampal–Entorhinal Region
Bellmund, J. L. S., Polti, I., & Doeller, C. F. (2020) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01592 · Cited by 55 · see citing works
Lost in time: Relocating the perception of duration outside the brain
Robbe, D. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105312 · Cited by 53 · see citing works
Minute-scale oscillatory sequences in medial entorhinal cortex
Cogno, S. G., Obenhaus, H. A., Lautrup, A., Jacobsen, R. I., Claudia Clopath, A., Andersson, S. O., Donato, F., Moser, M., & Moser, E. I. (2023) · Nature · doi:10.1038/s41586-023-06864-1 · Cited by 53 · see citing works
Self-citationA theory of hippocampal function: New developments
Rolls, E. T., & Treves, A. (2024) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2024.102636 · Cited by 52 · see citing works
A neural microcircuit model for a scalable scale‐invariant representation of time
Liu, Y., Tiganj, Z., Hasselmo, M. E., & Howard, M. W. (2018) · Hippocampus · doi:10.1002/hipo.22994 · Cited by 52 · see citing works
Crucial role for CA2 inputs in the sequential organization of CA1 time cells supporting memory
MacDonald, C. J., & Tonegawa, S. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2020698118 · Cited by 52 · see citing works
Liu, C., Ye, Z., Chen, C., Axmacher, N., & Xue, G. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab304 · Cited by 51 · see citing works
Mnemonic construction and representation of temporal structure in the hippocampal formation
Bellmund, J. L. S., Deuker, L., Montijn, N. D., & Doeller, C. F. (2022) · Nature Communications · doi:10.1038/s41467-022-30984-3 · Cited by 50 · see citing works
Bilash, O. M., Chavlis, S., Johnson, C. D., Poirazi, P., & Basu, J. (2023) · Cell Reports · doi:10.1016/j.celrep.2022.111962 · Cited by 50 · see citing works
Temporal context and latent state inference in the hippocampal splitter signal
Duvelle, É., Grieves, R. M., & van der Meer, M. A. A. (2022) · eLife · doi:10.7554/elife.82357 · Cited by 50 · see citing works
Extensive cortical functional connectivity of the human hippocampal memory system
Ma, Q., Rolls, E. T., Huang, C., Cheng, W., & Feng, J. (2021) · Cortex · doi:10.1016/j.cortex.2021.11.014 · Cited by 50 · see citing works
Shahbaba, B., Li, L., Agostinelli, F., Saraf, M., Cooper, K. W., Haghverdian, D., Elias, G. A., Baldi, P., & Fortin, N. J. (2022) · Nature Communications · doi:10.1038/s41467-022-28057-6 · Cited by 50 · see citing works
The Hippocampal Horizon: Constructing and Segmenting Experience for Episodic Memory
Ross, T. W., & Easton, A. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.11.038 · Cited by 49 · see citing works
Path integration maintains spatial periodicity of grid cell firing in a 1D circular track
Jacob, P.-Y., Capitano, F., Poucet, B., Save, É., & Sargolini, F. (2019) · Nature Communications · doi:10.1038/s41467-019-08795-w · Cited by 48 · see citing works
The Entorhinal Cortex as a Gateway for Amygdala Influences on Memory Consolidation
Roesler, R., & McGaugh, J. L. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.01.023 · Cited by 46 · see citing works
Anxiety-related activity of ventral hippocampal interneurons
Forro, T., Volitaki, E., Malagon‐Vina, H., Klausberger, T., Nevian, T., & Ciocchi, S. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102368 · Cited by 46 · see citing works
Inhibitory Connectivity Dominates the Fan Cell Network in Layer II of Lateral Entorhinal Cortex
Nilssen, E. S., Jacobsen, B., Fjeld, G., Nair, R. R., Blankvoort, S., Kentros, C. G., & Witter, M. P. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1290-18.2018 · Cited by 46 · see citing works
Navigating Through Time: A Spatial Navigation Perspective on How the Brain May Encode Time
Issa, J. B., Tocker, G., Hasselmo, M. E., Heys, J. G., & Dombeck, D. A. (2020) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-101419-011117 · Cited by 46 · see citing works
Ben‐Zion, Z., Zeevi, Y., Keynan, J. N., Admon, R., Kozlovski, T., Sharon, H., Halpern, P., Liberzon, I., Shalev, A. Y., Benjamini, Y., et al. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-00898-z · Cited by 46 · see citing works
Dimensions and mechanisms of memory organization
de Sousa, A. F., Chowdhury, A., & Silva, A. J. (2021) · Neuron · doi:10.1016/j.neuron.2021.06.014 · Cited by 46 · see citing works
Complementary representations of time in the prefrontal cortex and hippocampus
Ning, W., Bladon, J. H., & Hasselmo, M. E. (2022) · Hippocampus · doi:10.1002/hipo.23451 · Cited by 45 · see citing works
Lateral entorhinal cortex subpopulations represent experiential epochs surrounding reward
Issa, J. B., Radvansky, B. A., Xuan, F., & Dombeck, D. A. (2024) · Nature Neuroscience · doi:10.1038/s41593-023-01557-4 · Cited by 44 · see citing works
Alexander, A. S., Robinson, J. C., Dannenberg, H., Kinsky, N. R., Levy, S. J., Mau, W., Chapman, G. W., Sullivan, D. W., & Hasselmo, M. E. (2020) · Brain and Neuroscience Advances · doi:10.1177/2398212820972871 · Cited by 43 · see citing works
The Entorhinal Cortex and Adult Neurogenesis in Major Depression
Kim, I. B., & Park, S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111725 · Cited by 43 · see citing works
Ohara, S., Gianatti, M., Itou, K., Berndtsson, C. H., Doan, T. P., Kitanishi, T., Mizuseki, K., Iijima, T., Tsutsui, K., & Witter, M. P. (2019) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2019.00054 · Cited by 42 · see citing works
Rozov, A. V., Rannap, M., Lorenz, F., Nasretdinov, A., Draguhn, A., & Egorov, A. V. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0586-20.2020 · Cited by 42 · see citing works
Flexible Working Memory Through Selective Gating and Attentional Tagging
Kruijne, W., Bohté, S. M., Roelfsema, P. R., & Olivers, C. N. L. (2020) · Neural Computation · doi:10.1162/neco_a_01339 · Cited by 40 · see citing works
Changing temporal context in human temporal lobe promotes memory of distinct episodes
El-Kalliny, M. M., Wittig, J. H., Sheehan, T. C., Sreekumar, V., Inati, S. K., & Zaghloul, K. A. (2019) · Nature Communications · doi:10.1038/s41467-018-08189-4 · Cited by 38 · see citing works
FMTP: A unifying computational framework of temporal preparation across time scales.
Salet, J. M., Kruijne, W., van Rijn, H., Los, S. A., & Meeter, M. (2022) · Psychological Review · doi:10.1037/rev0000356 · Cited by 38 · see citing works
Time coding in rat dorsolateral striatum
Toso, A., Reinartz, S., Pulecchi, F., & Diamond, M. E. (2021) · Neuron · doi:10.1016/j.neuron.2021.08.020 · Cited by 38 · see citing works
Internally generated time in the rodent hippocampus is logarithmically compressed
Cao, R., Bladon, J. H., Charczynski, S. J., Hasselmo, M. E., & Howard, M. W. (2022) · eLife · doi:10.7554/elife.75353 · Cited by 37 · see citing works
Divergent recruitment of developmentally defined neuronal ensembles supports memory dynamics
Kveim, V. A., Salm, L., Ulmer, T., Lahr, M., Kandler, S., Imhof, F., & Donato, F. (2024) · Science · doi:10.1126/science.adk0997 · Cited by 37 · see citing works
Time to put the mammillothalamic pathway into context
Dillingham, C. M., Milczarek, M. M., Perry, J. C., & Vann, S. D. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.11.031 · Cited by 37 · see citing works
Terada, S.-I., Kobayashi, K., & Matsuzaki, M. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111494 · Cited by 37 · see citing works
Generalisation of structural knowledge in the hippocampal-entorhinal system
Whittington, J. C. R., Muller, T. H., Mark, S., Barry, C., & Behrens, T. E. J. (2018) · arXiv · doi:10.48550/arxiv.1805.09042 · Cited by 36 · see citing works
Buonomano, D. V., Buzsáki, G., Davachi, L., & Nobre, A. C. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.1430-23.2023 · Cited by 36 · see citing works
The effects of developmental alcohol exposure on the neurobiology of spatial processing
Harvey, R. E., Berkowitz, L. E., Hamilton, D. A., & Clark, B. J. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.018 · Cited by 37 · see citing works
Neural Circuitry–Neurogenesis Coupling Model of Depression
Kim, I. B., & Park, S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052468 · Cited by 36 · see citing works
Neuronal chemo‐architecture of the entorhinal cortex: A comparative review
Kobro‐Flatmoen, A., & Witter, M. P. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14511 · Cited by 35 · see citing works
Lee, A. C. H., Thavabalasingam, S., Alushaj, D., Çavdaroğlu, B., & Ito, R. (2019) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2019.107300 · Cited by 35 · see citing works
- Authors
- Tsao, A., Sugar, J., Lu, L., Wang, C., Knierim, J. J., Moser, M.-B., & Moser, E. I.
- Affiliations
- Norwegian University of Science and Technology (NO)
- Baylor College of Medicine (US)
- Johns Hopkins University (US)
- Corresponding author
- Tsao, Albert
- Moser, Edvard I.
- Venue
- Nature
- Published
- 2018-08-29
- Volume
- 561
- Issue
- 7721
- Pages
- 57-62
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2889422159
- Cited by
- 490
- References
- 51
- Citations by year
- 2026: 35 · 2025: 69 · 2024: 74 · 2023: 51 · 2022: 78 · 2021: 66 · 2020: 56 · 2019: 51 · 2018: 10
- FWCI
- 27.26
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- other-oa
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- NORA - Norwegian Open Research Archives (submittedVersion, other-oa)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- time encoding, lateral entorhinal cortex, medial entorhinal cortex, hippocampus, episodic memory, temporal binding, population coding, temporal flow, rats
- MeSH terms
- Animals, Behavior, Animal, Male, Time Factors, Entorhinal 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