Locally ordered representation of 3D space in the entorhinal cortex.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
received:
08
01
2020
accepted:
29
06
2021
pubmed:
13
8
2021
medline:
5
11
2021
entrez:
12
8
2021
Statut:
ppublish
Résumé
As animals navigate on a two-dimensional surface, neurons in the medial entorhinal cortex (MEC) known as grid cells are activated when the animal passes through multiple locations (firing fields) arranged in a hexagonal lattice that tiles the locomotion surface
Identifiants
pubmed: 34381211
doi: 10.1038/s41586-021-03783-x
pii: 10.1038/s41586-021-03783-x
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
404-409Subventions
Organisme : European Research Council
Pays : International
Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Hafting, T., Fyhn, M., Molden, S., Moser, M.-B. & Moser, E. I. Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801–806 (2005).
pubmed: 15965463
doi: 10.1038/nature03721
Finkelstein, A., Las, L. & Ulanovsky, N. 3-D maps and compasses in the brain. Annu. Rev. Neurosci. 39, 171–196 (2016).
pubmed: 27442069
doi: 10.1146/annurev-neuro-070815-013831
Krupic, J., Burgess, N. & O’Keefe, J. Neural representations of location composed of spatially periodic bands. Science 337, 853–857 (2012).
pubmed: 22904012
pmcid: 4576732
doi: 10.1126/science.1222403
Stensola, T., Stensola, H., Moser, M.-B. & Moser, E. I. Shearing-induced asymmetry in entorhinal grid cells. Nature 518, 207–212 (2015).
pubmed: 25673414
doi: 10.1038/nature14151
Hayman, R., Verriotis, M. A., Jovalekic, A., Fenton, A. A. & Jeffery, K. J. Anisotropic encoding of three-dimensional space by place cells and grid cells. Nat. Neurosci. 14, 1182–1188 (2011).
pubmed: 21822271
pmcid: 3166852
doi: 10.1038/nn.2892
Hayman, R. M., Casali, G., Wilson, J. J. & Jeffery, K. J. Grid cells on steeply sloping terrain: evidence for planar rather than volumetric encoding. Front. Psychol. 6, 925 (2015).
pubmed: 26236245
pmcid: 4502341
doi: 10.3389/fpsyg.2015.00925
Casali, G., Bush, D. & Jeffery, K. Altered neural odometry in the vertical dimension. Proc. Natl Acad. Sci. USA 116, 4631–4636 (2019).
pubmed: 30770450
pmcid: 6410878
doi: 10.1073/pnas.1811867116
Yartsev, M. M., Witter, M. P. & Ulanovsky, N. Grid cells without theta oscillations in the entorhinal cortex of bats. Nature 479, 103–107 (2011).
pubmed: 22051680
doi: 10.1038/nature10583
Taube, J. S., Muller, R. U. & Ranck, J. B. Jr Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10, 420–435 (1990).
pubmed: 2303851
pmcid: 6570151
doi: 10.1523/JNEUROSCI.10-02-00420.1990
Sargolini, F. et al. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312, 758–762 (2006).
pubmed: 16675704
doi: 10.1126/science.1125572
Finkelstein, A. et al. Three-dimensional head-direction coding in the bat brain. Nature 517, 159–164 (2015).
pubmed: 25470055
doi: 10.1038/nature14031
Solstad, T., Boccara, C. N., Kropff, E., Moser, M.-B. & Moser, E. I. Representation of geometric borders in the entorhinal cortex. Science 322, 1865–1868 (2008).
pubmed: 19095945
doi: 10.1126/science.1166466
Savelli, F., Yoganarasimha, D. & Knierim, J. J. Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18, 1270–1282 (2008).
pubmed: 19021262
pmcid: 3007674
doi: 10.1002/hipo.20511
Yartsev, M. M. & Ulanovsky, N. Representation of three-dimensional space in the hippocampus of flying bats. Science 340, 367–372 (2013).
pubmed: 23599496
doi: 10.1126/science.1235338
Hales, T. C. A proof of the Kepler conjecture. Ann. Math. 162, 1065–1185 (2005).
doi: 10.4007/annals.2005.162.1065
Stella, F. & Treves, A. The self-organization of grid cells in 3D. eLife 4, e05913 (2015).
pmcid: 4453437
doi: 10.7554/eLife.05913
Mathis, A., Stemmler, M. B. & Herz, A. V. M. Probable nature of higher-dimensional symmetries underlying mammalian grid-cell activity patterns. eLife 4, e05979 (2015).
pmcid: 4454919
doi: 10.7554/eLife.05979
Horiuchi, T. K. & Moss, C. F. Grid cells in 3-D: reconciling data and models. Hippocampus 25, 1489–1500 (2015).
pubmed: 25913890
doi: 10.1002/hipo.22469
Boccara, C. N. et al. Grid cells in pre- and parasubiculum. Nat. Neurosci. 13, 987–994 (2010).
pubmed: 20657591
doi: 10.1038/nn.2602
Krupic, J., Bauza, M., Burton, S. & O’Keefe, J. Local transformations of the hippocampal cognitive map. Science 359, 1143–1146 (2018).
pubmed: 29590044
pmcid: 6331044
doi: 10.1126/science.aao4960
Boccara, C. N., Nardin, M., Stella, F., O’Neill, J. & Csicsvari, J. The entorhinal cognitive map is attracted to goals. Science 363, 1443–1447 (2019).
pubmed: 30923221
doi: 10.1126/science.aav4837
Sanguinetti-Scheck, J. I. & Brecht, M. Home, head direction stability, and grid cell distortion. J. Neurophysiol. 123, 1392–1406 (2020).
pubmed: 32101492
pmcid: 7191526
doi: 10.1152/jn.00518.2019
Krupic, J., Bauza, M., Burton, S., Lever, C. & O’Keefe, J. How environment geometry affects grid cell symmetry and what we can learn from it. Phil. Trans. R. Soc. Lond. B 369, 20130188 (2013).
doi: 10.1098/rstb.2013.0188
Stensola, H. et al. The entorhinal grid map is discretized. Nature 492, 72–78 (2012).
pubmed: 23222610
doi: 10.1038/nature11649
Kropff, E. & Treves, A. The emergence of grid cells: intelligent design or just adaptation? Hippocampus 18, 1256–1269 (2008).
pubmed: 19021261
doi: 10.1002/hipo.20520
Burak, Y. & Fiete, I. R. Accurate path integration in continuous attractor network models of grid cells. PLoS Comput. Biol. 5, e1000291 (2009).
pubmed: 19229307
pmcid: 2632741
doi: 10.1371/journal.pcbi.1000291
McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I. & Moser, M.-B. Path integration and the neural basis of the ‘cognitive map’. Nat. Rev. Neurosci. 7, 663–678 (2006).
pubmed: 16858394
doi: 10.1038/nrn1932
Fiete, I. R., Burak, Y. & Brookings, T. What grid cells convey about rat location. J. Neurosci. 28, 6858–6871 (2008).
pubmed: 18596161
pmcid: 6670990
doi: 10.1523/JNEUROSCI.5684-07.2008
Mathis, A., Herz, A. V. M. & Stemmler, M. B. Resolution of nested neuronal representations can be exponential in the number of neurons. Phys. Rev. Lett. 109, 018103 (2012).
pubmed: 23031134
doi: 10.1103/PhysRevLett.109.018103
Stemmler, M., Mathis, A. & Herz, A. V. M. Connecting multiple spatial scales to decode the population activity of grid cells. Sci. Adv. 1, e1500816 (2015).
pubmed: 26824061
pmcid: 4730856
doi: 10.1126/science.1500816
Sarel, A., Finkelstein, A., Las, L. & Ulanovsky, N. Vectorial representation of spatial goals in the hippocampus of bats. Science 355, 176–180 (2017).
pubmed: 28082589
doi: 10.1126/science.aak9589
Omer, D. B., Maimon, S. R., Las, L. & Ulanovsky, N. Social place-cells in the bat hippocampus. Science 359, 218–224 (2018).
pubmed: 29326274
doi: 10.1126/science.aao3474
Ulanovsky, N. & Moss, C. F. Hippocampal cellular and network activity in freely moving echolocating bats. Nat. Neurosci. 10, 224–233 (2007).
pubmed: 17220886
doi: 10.1038/nn1829
Yovel, Y., Falk, B., Moss, C. F. & Ulanovsky, N. Optimal localization by pointing off axis. Science 327, 701–704 (2010).
pubmed: 20133574
doi: 10.1126/science.1183310
Skaggs, W. E., McNaughton, B. L., Wilson, M. A. & Barnes, C. A. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6, 149–172 (1996).
pubmed: 8797016
doi: 10.1002/(SICI)1098-1063(1996)6:2<149::AID-HIPO6>3.0.CO;2-K
Henriksen, E. J. et al. Spatial representation along the proximodistal axis of CA1. Neuron 68, 127–137 (2010).
pubmed: 20920796
pmcid: 3093538
doi: 10.1016/j.neuron.2010.08.042
Stukowski, A. Visualization and analysis of atomistic simulation data with OVITO—the Open Visualization Tool. Model. Simul. Mater. Sci. Eng. 18, 015012 (2010).
doi: 10.1088/0965-0393/18/1/015012
Larsen, P. M., Schmidt, S. & Schiøtz, J. Robust structural identification via polyhedral template matching. Model. Simul. Mater. Sci. Eng. 24, 055007 (2016).
doi: 10.1088/0965-0393/24/5/055007
Brandon, M. P. et al. Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science 332, 595–599 (2011).
pubmed: 21527714
pmcid: 3252766
doi: 10.1126/science.1201652
Koenig, J., Linder, A. N., Leutgeb, J. K. & Leutgeb, S. The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science 332, 592–595 (2011).
pubmed: 21527713
doi: 10.1126/science.1201685
Hansen, J.-P. & Verlet, L. Phase transitions of the Lennard-Jones system. Phys. Rev. 184, 151–161 (1969).
doi: 10.1103/PhysRev.184.151
Langston, R. F. et al. Development of the spatial representation system in the rat. Science 328, 1576–1580 (2010).
pubmed: 20558721
doi: 10.1126/science.1188210
Wills, T. J., Cacucci, F., Burgess, N. & O’Keefe, J. Development of the hippocampal cognitive map in preweanling rats. Science 328, 1573–1576 (2010).
pubmed: 20558720
pmcid: 3543985
doi: 10.1126/science.1188224
Eliav, T. et al. Nonoscillatory phase coding and synchronization in the bat hippocampal formation. Cell 175, 1119–1130 (2018).
pubmed: 30318145
doi: 10.1016/j.cell.2018.09.017
Derdikman, D. et al. Fragmentation of grid cell maps in a multicompartment environment. Nat. Neurosci. 12, 1325–1332 (2009).
pubmed: 19749749
doi: 10.1038/nn.2396
Torquato, S. & Stillinger, F. H. Jammed hard-particle packings: from Kepler to Bernal and beyond. Rev. Mod. Phys. 82, 2633 (2010).
doi: 10.1103/RevModPhys.82.2633
D’Albis, T. & Kempter, R. A single-cell spiking model for the origin of grid-cell patterns. PLoS Comput. Biol. 13, e1005782 (2017).
pubmed: 28968386
pmcid: 5638623
doi: 10.1371/journal.pcbi.1005782
Monsalve-Mercado, M. M. & Leibold, C. Hippocampal spike-timing correlations lead to hexagonal grid fields. Phys. Rev. Lett. 119, 038101 (2017).
pubmed: 28777606
doi: 10.1103/PhysRevLett.119.038101
Weber, S. N. & Sprekeler, H. Learning place cells, grid cells and invariances with excitatory and inhibitory plasticity. eLife 7, e34560 (2018).
pubmed: 29465399
pmcid: 5927772
doi: 10.7554/eLife.34560
Yoon, K. et al. Specific evidence of low-dimensional continuous attractor dynamics in grid cells. Nat. Neurosci. 16, 1077–1084 (2013).
pubmed: 23852111
pmcid: 3797513
doi: 10.1038/nn.3450
Guanella, A., Kiper, D. & Verschure, P. A model of grid cells based on a twisted torus topology. Int. J. Neural Syst. 17, 231–240 (2007).
pubmed: 17696288
doi: 10.1142/S0129065707001093
Fuhs, M. C. & Touretzky, D. S. A spin glass model of path integration in rat medial entorhinal cortex. J. Neurosci. 26, 4266–4276 (2006).
pubmed: 16624947
pmcid: 6674007
doi: 10.1523/JNEUROSCI.4353-05.2006
Klukas, M., Lewis, M. & Fiete, I. Efficient and flexible representation of higher-dimensional cognitive variables with grid cells. PLoS Comput. Biol. 16, e1007796 (2020).
pubmed: 32343687
pmcid: 7209352
doi: 10.1371/journal.pcbi.1007796
Burak, Y. & Fiete, I. Do we understand the emergent dynamics of grid cell activity? J. Neurosci. 26, 9352–9354 (2006).
pubmed: 16977716
pmcid: 6674593
doi: 10.1523/JNEUROSCI.2857-06.2006
Rowland, D. C., Roudi, Y., Moser, M.-B. & Moser, E. I. Ten years of grid cells. Annu. Rev. Neurosci. 39, 19–40 (2016).
pubmed: 27023731
doi: 10.1146/annurev-neuro-070815-013824