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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.
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“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
In the citing paper
“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
Citations
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 6,684
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
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
Episodic-like memory during cache recovery by scrub jays
Clayton, N. S., & Dickinson, A. (1998) · Nature · doi:10.1038/26216 · Cited by 1,464
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
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
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
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
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
Wood, E. R., Dudchenko, P. A., Robitsek, R. J., & Eichenbaum, H. (2000) · Neuron · doi:10.1016/s0896-6273(00)00071-4 · Cited by 992
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 981
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
State-dependent computations: spatiotemporal processing in cortical networks
Buonomano, D. V., & Maass, W. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2558 · Cited by 950
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
Time cells in the hippocampus: a new dimension for mapping memories
Eichenbaum, H. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3827 · Cited by 843
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
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
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 680
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
Self-citationOn the Integration of Space, Time, and Memory
Eichenbaum, H. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.036 · Cited by 548
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 475
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 457
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
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
Hippocampal Activity Patterns Carry Information about Objects in Temporal Context
Hsieh, L., Gruber, M. J., Jenkins, L. J., & Ranganath, C. (2014) · Neuron · doi:10.1016/j.neuron.2014.01.015 · Cited by 363
Ezzyat, Y., & Davachi, L. (2014) · Neuron · doi:10.1016/j.neuron.2014.01.042 · Cited by 321
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
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 294
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
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
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 275
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
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
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
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 240
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
Rowland, D. C., Roudi, Y., Moser, M., & Moser, E. I. (2016) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070815-013824 · Cited by 227
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 203
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 191
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 187
Buzsáki, G., & Llinás, R. (2017) · Science · doi:10.1126/science.aan8869 · Cited by 175
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 163
Self-citationKeene, 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 140
Ekstrom, A. D., & Bookheimer, S. Y. (2007) · Learning & Memory · doi:10.1101/lm.575107 · Cited by 139
McEchron, M. D., Tseng, W., & Disterhoft, J. F. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-04-01535.2003 · Cited by 137
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
Self-citationLearning 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 106
Finnerty, 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 102
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 102
Episodic memory—From brain to mind
Ferbinteanu, J., Kennedy, P., & Shapiro, M. L. (2006) · Hippocampus · doi:10.1002/hipo.20204 · Cited by 99
Guinard, D., Usson, Y., Guillermet, C., & Saxod, R. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980817)398:1 · Cited by 41
Pilkiw, M., Insel, N., Cui, Y., Finney, C. A., Morrissey, M. D., & Takehara‐Nishiuchi, K. (2017) · eLife · doi:10.7554/elife.28611 · Cited by 37
Research works printed but not linked: 2
- Tulving, E. Elements of Episodic Memory (Oxford Univ. Press, Oxford, 1985).
- Skaggs, W. E., McNaughton, B. L. & Gothard, K. M. in Advances in Neural Information Processing Systems 5 (NIPS 1992) 1030–1037 (Morgan Kaufmann Publishers Inc., 1993).
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
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
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 506
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 371
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 247
Metadata
- 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
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