How animals find their way in space. Experiments and modeling
Matematičeskaâ biologiâ i bioinformatika, Tome 13 (2018), pp. t132-t161.

Voir la notice de l'article provenant de la source Math-Net.Ru

We describe different components of brain's space representation system, such as place cells, grid cells, time cells, and head-direction cells and review the models that suggest and test neural mechanisms on how this system can be used by an animal during navigation.
@article{MBB_2018_13_a8,
     author = {Yakov Kazanovich and Ivan E. Mysin},
     title = {How animals find their way in space. {Experiments} and modeling},
     journal = {Matemati\v{c}eska\^a biologi\^a i bioinformatika},
     pages = {t132--t161},
     publisher = {mathdoc},
     volume = {13},
     year = {2018},
     language = {en},
     url = {http://geodesic.mathdoc.fr/item/MBB_2018_13_a8/}
}
TY  - JOUR
AU  - Yakov Kazanovich
AU  - Ivan E. Mysin
TI  - How animals find their way in space. Experiments and modeling
JO  - Matematičeskaâ biologiâ i bioinformatika
PY  - 2018
SP  - t132
EP  - t161
VL  - 13
PB  - mathdoc
UR  - http://geodesic.mathdoc.fr/item/MBB_2018_13_a8/
LA  - en
ID  - MBB_2018_13_a8
ER  - 
%0 Journal Article
%A Yakov Kazanovich
%A Ivan E. Mysin
%T How animals find their way in space. Experiments and modeling
%J Matematičeskaâ biologiâ i bioinformatika
%D 2018
%P t132-t161
%V 13
%I mathdoc
%U http://geodesic.mathdoc.fr/item/MBB_2018_13_a8/
%G en
%F MBB_2018_13_a8
Yakov Kazanovich; Ivan E. Mysin. How animals find their way in space. Experiments and modeling. Matematičeskaâ biologiâ i bioinformatika, Tome 13 (2018), pp. t132-t161. http://geodesic.mathdoc.fr/item/MBB_2018_13_a8/

[1] O'Keefe J., Dostrovsky J., “The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat”, Brain Res., 34 (1971), 171–175 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/0006-8993(71)90358-1'>10.1016/0006-8993(71)90358-1</ext-link>

[2] O'Keefe J., “Place units in the hippocampus of the freely moving rat”, Exp. Neurol., 51 (1976), 78–109 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/0014-4886(76)90055-8'>10.1016/0014-4886(76)90055-8</ext-link>

[3] Keefe J. O., Nadel L., The hippocampus as a cognitive map, Clarendon Press, Oxford, 1978

[4] Tolman E. C., “Cognitive maps in rats and men”, Psychol. Rev., 55 (1948), 189–208 <ext-link ext-link-type='doi' href='https://doi.org/10.1037/h0061626'>10.1037/h0061626</ext-link>

[5] Hafting T., Fyhn M., Molden S., Moser M. B., Moser E. I., “Microstructure of a spatial map in the entorhinal cortex”, Nature, 436 (2005), 801–806 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nature03721'>10.1038/nature03721</ext-link>

[6] Abbott A., “Neuroscience: Brains of Norway”, Nature, 514 (2014), 154–157 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/514154a'>10.1038/514154a</ext-link>

[7] Moser E. I., Roudi Y., Witter M. P., Kentros C., Bonhoeffer T., Moser M. B., “Grid cells and cortical representation”, Nat. Rev. Neurosci., 15 (2014), 466–481 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nrn3766'>10.1038/nrn3766</ext-link>

[8] Taube J. S., Muller R. U., Ranck J. B., “Head-direction cells recorded from the postsubiculum in freely moving rats. I: Description and quantitative analysis”, J. Neurosci., 10 (1990), 420–435 <ext-link ext-link-type='doi' href='https://doi.org/10.1523/JNEUROSCI.10-02-00420.1990'>10.1523/JNEUROSCI.10-02-00420.1990</ext-link>

[9] Taube J. S., Muller R. U., Ranck J. B., “Head-direction cells recorded from the postsubiculum in freely moving rats. II: Effects of environmental manipulations”, J. Neurosci., 10 (1990), 436–447 <ext-link ext-link-type='doi' href='https://doi.org/10.1523/JNEUROSCI.10-02-00436.1990'>10.1523/JNEUROSCI.10-02-00436.1990</ext-link>

[10] Taube J. S., Burton H. L., “Head direction cell activity monitored in a novel environment and during a cue conflict situation”, J. Neurophysiol., 74 (1995), 1953–1971 <ext-link ext-link-type='doi' href='https://doi.org/10.1152/jn.1995.74.5.1953'>10.1152/jn.1995.74.5.1953</ext-link>

[11] Taube J. S., Bassett J. P., “Persistent neural activity in head direction cells”, Cerebral Cortex, 13 (2003), 1162–1172 <ext-link ext-link-type='doi' href='http://dx.doi.org/10.1093/cercor/bhg102'>http://dx.doi.org/10.1093/cercor/bhg102</ext-link>

[12] Yoganarasimha D., Yu X., Knierim J. J., “Head direction cell representations maintain internal coherence during conflicting proximal and distal cue rotations: comparison with hippocampal place cells”, J. Neurosci., 26 (2006), 622–631 <ext-link ext-link-type='doi' href='https://doi.org/10.1523/JNEUROSCI.3885-05.2006'>10.1523/JNEUROSCI.3885-05.2006</ext-link>

[13] Solstad T., Boccara C. N., Kropff E., Moser M. B., Moser E. I., “Representation of geometric borders in the entorhinal cortex”, Science, 322 (2008), 1865–1868 <ext-link ext-link-type='doi' href='https://doi.org/10.1126/science.1166466'>10.1126/science.1166466</ext-link>

[14] Rolls E. T., Stringer S. M., “Spatial view cells in the hippocampus, and their idiothetic update based on place and head direction”, Neural Netw., 18 (2005), 1229–1241 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.neunet.2005.08.006'>10.1016/j.neunet.2005.08.006</ext-link><ext-link ext-link-type='zbl-item-id' href='https://zbmath.org/?q=an:1086.92009'>1086.92009</ext-link>

[15] Eichenbaum H., “Time cells in the hippocampus: a new dimension for mapping memories”, Nat. Rev. Neurosci., 15 (2014), 732–744 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nrn3827'>10.1038/nrn3827</ext-link>

[16] Kropff E., Carmichael J. E., Moser M. B., Moser E. I., “Speed cells in the medial entorhinal cortex”, Nature, 523 (2015), 419–424 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nature14622'>10.1038/nature14622</ext-link>

[17] Ye J., Witter M. P., Moser M.-B., Moser E. I., “Entorhinal fast-spiking speed cells project to the hippocampus”, Proc. Natl. Acad. Sci. (USA), 115 (2018), E1627–E1636 <ext-link ext-link-type='doi' href='https://doi.org/10.1073/pnas.1720855115'>10.1073/pnas.1720855115</ext-link>

[18] Hoydal O. A., Skytoen E. R., Moser M.-B., Moser E. I., “Object-vector coding in the medial entorhinal cortex”, BioRxiv, 2018 <ext-link ext-link-type='doi' href='https://doi.org/10.1101/286286'>10.1101/286286</ext-link>

[19] Yartsev M. M., Ulanovsky N., “Representation of three-dimensional space in the hippocampus of flying bats”, Science, 340 (2013), 367–372 <ext-link ext-link-type='doi' href='https://doi.org/10.1126/science.1235338'>10.1126/science.1235338</ext-link>

[20] Bingman V., Jechura T., Kahn M. C., “Behavioral and neural mechanisms of homing and migration in birds”, Animal Spatial Cognition: Comparative, Neural and Computational Approaches, 2006 (accessed 20.01.2015) <ext-link ext-link-type='uri' href='http://www.pigeon.psy.tufts.edu/asc/Bingman'>http://www.pigeon.psy.tufts.edu/asc/Bingman</ext-link>

[21] Hopfield J. J., “Neural networks and physical systems with emergent collective computational abilities”, PNAS, 79 (1982), 2554–2558 <ext-link ext-link-type='doi' href='https://doi.org/10.1073/pnas.79.8.2554'>10.1073/pnas.79.8.2554</ext-link><ext-link ext-link-type='mr-item-id' href='http://mathscinet.ams.org/mathscinet-getitem?mr=652033'>652033</ext-link><ext-link ext-link-type='zbl-item-id' href='https://zbmath.org/?q=an:1369.92007'>1369.92007</ext-link>

[22] Devanand D. P., Pradhaban G., Liu X., Khandji A., De Santi S., Segal S., Rusinek H., Pelton G. H., Honig L. S., Mayeux R. et al., “Hippocampal and entorhinal atrophy in mild cognitive impairment: prediction of Alzheimer disease”, Neurology, 68 (2007), 828–836 <ext-link ext-link-type='doi' href='https://doi.org/10.1212/01.wnl.0000256697.20968.d7'>10.1212/01.wnl.0000256697.20968.d7</ext-link>

[23] Vinogradova O. S., “Hippocampus as comparator: Role of the two input and two output systems of the hippocampus in selection and registration of information”, Hippocampus, 11 (2001), 578–598 <ext-link ext-link-type='doi' href='https://doi.org/10.1002/hipo.1073.abs'>10.1002/hipo.1073.abs</ext-link>

[24] Damasio A. R., “The brain binds entities and events by multiregional activation from convergence zones”, Neural Comput., 1 (1989), 123–132 <ext-link ext-link-type='doi' href='https://doi.org/10.1162/neco.1989.1.1.123'>10.1162/neco.1989.1.1.123</ext-link>

[25] Buzsaki G., Moser E. I., “Memory, navigation and theta rhythm in the hippocampalentorhinal system”, Nat. Neurosci., 16 (2013), 130–138 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nn.3304'>10.1038/nn.3304</ext-link>

[26] Eichenbaum H., Cohen N. J., Can we reconcile the declarative memory and spatial navigation views on hippocampal function?, Neuron, 83 (2014), 764–770 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.neuron.2014.07.032'>10.1016/j.neuron.2014.07.032</ext-link>

[27] Witter M. P., Moser E. I., “Spatial representation and the architecture of the entorhinal cortex”, Trends Neurosci., 29 (2006), 671–678 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.tins.2006.10.003'>10.1016/j.tins.2006.10.003</ext-link>

[28] Burgalossi A., Brecht M., “Cellular, columnar and modular organization of spatial representations in medial entorhinal cortex”, Curr. Opin. Neurobiol., 24 (2014), 47–54 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.conb.2013.08.011'>10.1016/j.conb.2013.08.011</ext-link>

[29] Ray S., Naumann R., Burgalossi A., Tang Q., Schmidt H., Brecht M., “Grid-layout and theta-modulation of layer 2 pyramidal neurons in medial entorhinal cortex”, Science, 343 (2014), 891–896 <ext-link ext-link-type='doi' href='https://doi.org/10.1126/science.1243028'>10.1126/science.1243028</ext-link>

[30] Nakazawa K., McHugh T. J., Wilson M. A., Tonegawa S., “NMDA receptors, place cells and hippocampal spatial memory”, Nat. Rev. Neurosci., 5 (2004), 361–372 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nrn1385'>10.1038/nrn1385</ext-link>

[31] Wilson M. A., McNaughton B. L., “Dynamics of the hippocampal ensemble code for space”, Science, 261 (1993), 1055–1058 <ext-link ext-link-type='doi' href='https://doi.org/10.1126/science.8351520'>10.1126/science.8351520</ext-link>

[32] Bird C. M., Burgess N., “The hippocampus and memory: insights from spatial processing”, Nat. Rev. Neurosci., 9 (2008), 182–194 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nrn2335'>10.1038/nrn2335</ext-link><ext-link ext-link-type='mr-item-id' href='http://mathscinet.ams.org/mathscinet-getitem?mr=2394759'>2394759</ext-link>

[33] Foster D. J., Wilson M. A., “Reverse replay of behavioural sequences in hippocampal place cells during the awake state”, Nature, 440 (2006), 680–683 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nature04587'>10.1038/nature04587</ext-link>

[34] Louie K., Wilson M. A., “Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep”, Neuron, 29 (2001), 145–156 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/S0896-6273(01)00186-6'>10.1016/S0896-6273(01)00186-6</ext-link>

[35] O'Keefe J., Recce M. L., “Phase relationship between hippocampal place units and the EEG theta rhythm”, Hippocampus, 3 (1993), 317–330 <ext-link ext-link-type='doi' href='https://doi.org/10.1002/hipo.450030307'>10.1002/hipo.450030307</ext-link><ext-link ext-link-type='mr-item-id' href='http://mathscinet.ams.org/mathscinet-getitem?mr=1228541'>1228541</ext-link>

[36] Skaggs W. E., McNaughton B. L., “Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences”, Hippocampus, 6 (1996), 149–172 <ext-link ext-link-type='doi' href='https://doi.org/10.1002/(SICI)1098-1063(1996)6:2&lt;149::AID-HIPO6&gt;3.0.CO;2-K'>10.1002/(SICI)1098-1063(1996)6:2&lt;149::AID-HIPO6&gt;3.0.CO;2-K</ext-link>

[37] Sadowski J. H., Jones M. W., Mellor J. R., “Ripples make waves: binding structured activity and plasticity in hippocampal networks”, Neural Plast., 2011 (2011) <ext-link ext-link-type='doi' href='https://doi.org/10.1155/2011/960389'>10.1155/2011/960389</ext-link>

[38] Borisyuk R., Chik D., Kazanovich Y., da Silva Gomes J., “Spiking neural network model for memorizing sequences with forward and backward recall”, BioSystems, 112 (2013), 214–223 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.biosystems.2013.03.018'>10.1016/j.biosystems.2013.03.018</ext-link>

[39] Fyhn M., Hafting T., Witter M. P., Moser E. I., Moser M. B., “Grid cells in mice”, Hippocampus, 18 (2008), 1230–1238 <ext-link ext-link-type='doi' href='https://doi.org/10.1002/hipo.20472'>10.1002/hipo.20472</ext-link>

[40] Yartsev M. M., Witter M. P., Ulanovsky N., “Grid cells without theta oscillations in the entorhinal cortex of bats”, Nature, 479 (2011), 103–107 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nature10583'>10.1038/nature10583</ext-link>

[41] Killian N. J., Jutras M. J., Buffalo E. A., “A map of visual space in the primate entorhinal cortex”, Nature, 491 (2012), 761–764 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nature11587'>10.1038/nature11587</ext-link>

[42] Jacobs J., Weidemann C. T., Miller J. F., Solway A., Burke J. F., Wei X. X., Suthana N., Sperling M. R., Sharan A. D., Fried I., Kahana M. J., “Direct recordings of grid-like neuronal activity in human spatial navigation”, Nat. Neurosci., 16 (2013), 1188–1190 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nn.3466'>10.1038/nn.3466</ext-link>

[43] Sargolini F., Fyhn M., Hafting T., McNaughton B. L., Witter M. P., Moser M-B., Moser E. I., “Conjunctive representation of position, direction, and velocity in entorhinal cortex”, Science, 312 (2006), 758–762 <ext-link ext-link-type='doi' href='https://doi.org/10.1126/science.1125572'>10.1126/science.1125572</ext-link>

[44] Zhang S. J., Ye J., Miao C., Tsao A., Cerniauskas I., Ledergerber D., Moser M. B., Moser E. I., “Optogenetic dissection of entorhinal-hippocampal functional connectivity”, Science, 340 (2013), 1232627 <ext-link ext-link-type='doi' href='https://doi.org/10.1126/science.1232627'>10.1126/science.1232627</ext-link>

[45] Diehl G. W., Hon O. J., Leutgeb S., Leutgeb J. K., “Grid and nongrid cells in medial entorhinal cortex represent spatial location and environmental features with complementary coding schemes”, Neuron, 94 (2017), 83–92 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.neuron.2017.03.004'>10.1016/j.neuron.2017.03.004</ext-link>

[46] Boccara C. N., Sargolini F., Thoresen V. H., Solstad T., Witter M. P., Moser E. I., Moser M. B., “Grid cells in pre- and parasubiculum”, Nat. Neurosci., 13 (2010), 987–994 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nn.2602'>10.1038/nn.2602</ext-link>

[47] Rowland D. C., “Functional properties of stellate cells in medial entorhinal cortex layer II”, eLife, 7 (2018), e36664 <ext-link ext-link-type='doi' href='https://doi.org/10.7554/eLife.36664'>10.7554/eLife.36664</ext-link>

[48] Brun V. H., Solstad T., Kjelstrup K. B., Fyhn M., Witter M. P., Moser E. I., Moser M. B., “Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex”, Hippocampus, 18 (2008), 1200–1212 <ext-link ext-link-type='doi' href='https://doi.org/10.1002/hipo.20504'>10.1002/hipo.20504</ext-link><ext-link ext-link-type='mr-item-id' href='http://mathscinet.ams.org/mathscinet-getitem?mr=2392136'>2392136</ext-link>

[49] Stensola H., Stensola T., Solstad T., Froland K., Moser M. B., Moser E. I., “The entorhinal grid map is discretized”, Nature, 492 (2012), 72–78 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nature11649'>10.1038/nature11649</ext-link>

[50] Heys J. G., Rangarajan K. V., Dombeck D. A., “The functional micro-organization of grid cells revealed by cellular-resolution imaging neuron”, Neuron, 84 (2014), 1079–1090 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.neuron.2014.10.048'>10.1016/j.neuron.2014.10.048</ext-link>

[51] Krupic J., Bauza M., Burton S., O'Keefe J., “Local transformations of the hippocampal cognitive map”, Science, 359 (2018), 1143–1146 <ext-link ext-link-type='doi' href='https://doi.org/10.1126/science.aao4960'>10.1126/science.aao4960</ext-link>

[52] Buzsáki G., “Theta oscillations in the hippocampus”, Neuron, 33 (2002), 325–340 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/S0896-6273(02)00586-X'>10.1016/S0896-6273(02)00586-X</ext-link>

[53] Vinogradova O. S., “Expression, control, and probable functional significance of the neuronal theta-rhythm”, Prog. Neurobiol., 45 (1995), 523–583 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/0301-0082(94)00051-I'>10.1016/0301-0082(94)00051-I</ext-link>

[54] Gonzalez-Sulser A., Parthier D., Candela A., McClure Ch., Pastoll H., Garden D., Sürmeli G., Nolan M.F., “GABAergic projections from the medial septum selectively inhibit interneurons in the medial entorhinal cortex”, J. Neurosci., 34 (2014), 16739–16743 <ext-link ext-link-type='doi' href='https://doi.org/10.1523/JNEUROSCI.1612-14.2014'>10.1523/JNEUROSCI.1612-14.2014</ext-link>

[55] Gonzalez-Sulser A., Nolan M. F., “Grid cells' need for speed”, Nat. Neurosci., 20 (2016), 1–2 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nn.4460'>10.1038/nn.4460</ext-link>

[56] Hayman R., Burgess N., “Disrupting the grid cells' need for speed”, Neuron, 91 (2016), 502–503 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.neuron.2016.07.028'>10.1016/j.neuron.2016.07.028</ext-link>

[57] Justus D., Dalügge D., Bothe S., Fuhrmann F., Hannes C., Kaneko H., Friedrichs D., Sosulina L., Schwarz I., Elliott D.A., Schoch S., Bradke F., Schwarz M.K., Remy S., “Glutamatergic synaptic integration of locomotion speed via septoentorhinal projections”, Nat. Neurosci., 20 (2017), 16–19 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nn.4447'>10.1038/nn.4447</ext-link>

[58] Robinson J., Manseau F., Ducharme G., Amilhon B., Vigneault E., El Mestikawy S., Williams S., “Optogenetic activation of septal glutamatergic neurons drive hippocampal theta rhythms”, J. Neurosci., 36 (2016), 3016–3023 <ext-link ext-link-type='doi' href='https://doi.org/10.1523/JNEUROSCI.2141-15.2016'>10.1523/JNEUROSCI.2141-15.2016</ext-link>

[59] Ledberg A., Robbe D., “Locomotion-related oscillatory body movements at 6–12 Hz modulate the hippocampal theta rhythm”, PLoS ONE, 6 (2011), e27575 <ext-link ext-link-type='doi' href='https://doi.org/10.1371/journal.pone.0027575'>10.1371/journal.pone.0027575</ext-link>

[60] Hinman J.R., Penley S.C., Long L.L., Escabí M.A., Chrobak J.J., “Septotemporal variation in dynamics of theta: speed and habituation”, J. Neurophysiol., 10 (2011), 2675–2686 <ext-link ext-link-type='doi' href='https://doi.org/10.1152/jn.00837.2010'>10.1152/jn.00837.2010</ext-link>

[61] Jeewajee A., Barry C., Douchamps V., Manson D., Lever C., Burgess N., “Theta phase precession of grid and place cell firing in open environments”, Philos. Trans. R. Soc. Lond. B Biol. Sci., 369 (2015), 20120532 <ext-link ext-link-type='doi' href='https://doi.org/10.1098/rstb.2012.0532'>10.1098/rstb.2012.0532</ext-link>

[62] Brandon M. P., Bogaard A. R., Libby C. P., Connerney M. A., Gupta K., Hasselmo M. E., “Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning”, Science, 332 (2011), 595–599 <ext-link ext-link-type='doi' href='https://doi.org/10.1126/science.1201652'>10.1126/science.1201652</ext-link>

[63] Newman E. L., Climer J. R., Hasselmo M. E., “Grid cell spatial tuning reduced following systemic muscarinic receptor blockade”, Hippocampus, 24 (2014), 643–655 <ext-link ext-link-type='doi' href='https://doi.org/10.1002/hipo.22253'>10.1002/hipo.22253</ext-link>

[64] Wills T. J., Cacucci F., “The development of the hippocampal neural representation of space”, Curr. Opin. Neurobiol., 24 (2014), 111–119 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.conb.2013.09.006'>10.1016/j.conb.2013.09.006</ext-link>

[65] Bonnevie T., Dunn B., Fyhn M., Hafting T., Derdikman D., Kubie J. L., Roudi Y., Moser E. I., Moser M. B., “Grid cells require excitatory drive from the hippocampus”, Nat. Neurosci., 16 (2013), 309–317 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nn.3311'>10.1038/nn.3311</ext-link>

[66] Schlesiger M.I., Boublil B.L., Hales J.B., Leutgeb J.K., Leutgeb S., “Hippocampal global remapping can occur without input from the medial entorhinal cortex”, Cell Rep., 22 (2018), 3152–3159 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.celrep.2018.02.082'>10.1016/j.celrep.2018.02.082</ext-link>

[67] Deshmukh S.S., Knierim J.J., “Representation of non-spatial and spatial information in the lateral entorhinal cortex”, Front. Behav. Neurosci., 5 (2011), 69 <ext-link ext-link-type='doi' href='https://doi.org/10.3389/fnbeh.2011.00069'>10.3389/fnbeh.2011.00069</ext-link>

[68] Jacob P.-Y., Casalil G., Spieser L., Page H., Overington D., Jeffery K., “An independent, landmark-dominated head direction signal in dysgranular retrosplenial cortex”, Nat. Neurosci., 20 (2017), 173–175 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nn.4465'>10.1038/nn.4465</ext-link>

[69] Sharp P.E., Blair H.T., Cho J., “The anatomical and computational basis of the rat headdirection cell signal”, Trends Neurosci., 2001, 289–294

[70] Taube J., Head direction cells, Scholarpedia, (accessed 19 September 2018) <ext-link ext-link-type='uri' href='http://www.scholarpedia.org/article/Head_direction_cells'>http://www.scholarpedia.org/article/Head_direction_cells</ext-link>

[71] Manns J.R., Howard M., Eichenbaum H., “Gradual changes in hippocampal activity support remembering the order of events”, Neuron, 56 (2007), 530–540 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.neuron.2007.08.017'>10.1016/j.neuron.2007.08.017</ext-link>

[72] Pastalkova E., Itskov V., Amarasingham A., Buzsáki G., “Internally generated cell assembly sequences in the rat hippocampus”, Science, 321 (2008), 1322–1327 <ext-link ext-link-type='doi' href='https://doi.org/10.1126/science.1159775'>10.1126/science.1159775</ext-link>

[73] Kraus B.J., Robinson R.J., White J.A., Eichenbaum H., Hasselmo M.E., “Hippocampal ‘time cells’: time versus path integration”, Neuron, 78 (2013), 1090–1101 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.neuron.2013.04.015'>10.1016/j.neuron.2013.04.015</ext-link>

[74] D'Hooge R., De Deyn P. P., “Applications of the Morris water maze in the study of learning and memory”, Brain Res. Rev., 36 (2001), 60–90 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/S0165-0173(01)00067-4'>10.1016/S0165-0173(01)00067-4</ext-link>

[75] Krichmar J. L., Seth A. K., Nitz D. A., Fleischer J. G., Edelman G. M., “Spatial navigation and causal analysis in a brain-based device modeling cortical-hippocampal interactions”, Neuroinformatics, 3 (2005), 197–221 <ext-link ext-link-type='doi' href='https://doi.org/10.1385/NI:3:3:197'>10.1385/NI:3:3:197</ext-link>

[76] Ponulak F., Hopfield J. J., “Rapid, parallel path planning by propagating wavefronts of spiking neural activity”, Front. Comput. Neurosci., 7 (2013), e98 <ext-link ext-link-type='doi' href='https://doi.org/10.3389/fncom.2013.00098'>10.3389/fncom.2013.00098</ext-link>

[77] Han V. Z., Grant K., Bell C. C., “Reversible associative depression and nonassociative potentiation at a parallel fiber synapse”, Neuron, 27 (2000), 611–622 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/S0896-6273(00)00070-2'>10.1016/S0896-6273(00)00070-2</ext-link>

[78] Roberts P. D., Leen T. K., “Anti-hebbian spike-timing-dependent plasticity and adaptive sensory processing”, Front. Comput. Neurosci., 4 (2010), 1–11 <ext-link ext-link-type='doi' href='https://doi.org/10.3389/fncom.2010.00156'>10.3389/fncom.2010.00156</ext-link>

[79] Miller J. F., Neufang M., Solway A., Brandt A., Trippel M., Mader I., Hefft S., Merkow M., Polyn S. M., Jacobs J., Kahana M. J., Schulze-Bonhage A., “Neural activity in human hippocampal formation reveals the spatial context of retrieved memories”, Science, 342 (2013), 1111–1114 <ext-link ext-link-type='doi' href='https://doi.org/10.1126/science.1244056'>10.1126/science.1244056</ext-link>

[80] Burak Y., “Spatial coding and attractor dynamics of grid cells in the entorhinal cortex”, Curr. Opin. Neurobiol., 25 (2014), 169–175 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.conb.2014.01.013'>10.1016/j.conb.2014.01.013</ext-link>

[81] Grossberg S., Pilly P. K., “Coordinated learning of grid cell and place cell spatial and temporal properties: multiple scales, attention and oscillations”, Philos. Trans. R. Soc. Lond. B Biol. Sci., 369 (2014), 20120524 <ext-link ext-link-type='doi' href='https://doi.org/10.1098/rstb.2012.0524'>10.1098/rstb.2012.0524</ext-link>

[82] Burgess N., “Grid cells and theta as oscillatory interference: Theory and predictions”, Hippocampus, 18 (2008), 1157–1174 <ext-link ext-link-type='doi' href='https://doi.org/10.1002/hipo.20518'>10.1002/hipo.20518</ext-link>

[83] Burgess C. P., Burgess N., “Controlling phase noise in oscillatory interference models of grid cell firing”, J. Neurosci., 34 (2014), 6224–6232 <ext-link ext-link-type='doi' href='https://doi.org/10.1523/JNEUROSCI.2540-12.2014'>10.1523/JNEUROSCI.2540-12.2014</ext-link>

[84] Burgess N., Barry C., O'Keefe J., “An oscillatory interference model of grid cell firing”, Hippocampus, 17 (2007), 801–812 <ext-link ext-link-type='doi' href='https://doi.org/10.1002/hipo.20327'>10.1002/hipo.20327</ext-link>

[85] Bush D., Burgess N., “A hybrid oscillatory interference/continuous attractor network model of grid cell firing”, J. Neurosci., 34 (2014), 5065–5079 <ext-link ext-link-type='doi' href='https://doi.org/10.1523/JNEUROSCI.4017-13.2014'>10.1523/JNEUROSCI.4017-13.2014</ext-link>

[86] Pilly P. K., Grossberg S., “How do spatial learning and memory occur in the brain? Coordinated learning of entorhinal grid cells and hippocampal place cells”, J. Cogn. Neurosci., 24 (2012), 1031–1054 <ext-link ext-link-type='doi' href='https://doi.org/10.1162/jocn_a_00200'>10.1162/jocn_a_00200</ext-link>

[87] Burak Y., Fiete I. R., “Accurate path integration in continuous attractor network models of grid cells”, PLoS Comput. Biol., 5:2 (2009), e1000291 <ext-link ext-link-type='doi' href='https://doi.org/10.1371/journal.pcbi.1000291'>10.1371/journal.pcbi.1000291</ext-link><ext-link ext-link-type='mr-item-id' href='http://mathscinet.ams.org/mathscinet-getitem?mr=2496586'>2496586</ext-link>

[88] Fuhs M. C., “A spin glass model of path integration in rat medial entorhinal cortex”, J. Neurosci., 26 (2006), 4266–4276 <ext-link ext-link-type='doi' href='https://doi.org/10.1523/JNEUROSCI.4353-05.2006'>10.1523/JNEUROSCI.4353-05.2006</ext-link>

[89] Si B., Treves A., “A model for the differentiation between grid and conjunctive units in medial entorhinal cortex”, Hippocampus, 23 (2013), 1410–1424 <ext-link ext-link-type='doi' href='https://doi.org/10.1002/hipo.22194'>10.1002/hipo.22194</ext-link>

[90] Si B., Kropff E., Treves A., “Grid alignment in entorhinal cortex”, Biol. Cybern., 106 (2012), 483–506 <ext-link ext-link-type='doi' href='https://doi.org/10.1007/s00422-012-0513-7'>10.1007/s00422-012-0513-7</ext-link>

[91] 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 (2006), 663–678 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nrn1932'>10.1038/nrn1932</ext-link>

[92] Navratilova Z., Giocomo L. M., Fellous J. M., Hasselmo M. E., McNaughton B. L., “Phase precession and variable spatial scaling in a periodic attractor map model of medial entorhinal grid cells with realistic after-spike dynamics”, Hippocampus, 22 (2012), 772–789 <ext-link ext-link-type='doi' href='https://doi.org/10.1002/hipo.20939'>10.1002/hipo.20939</ext-link>

[93] Widloski J., Fiete I. R., “A model of grid cell development through spatial exploration and spike time-dependent plasticity”, Neuron, 83 (2014), 481–495 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.neuron.2014.06.018'>10.1016/j.neuron.2014.06.018</ext-link>

[94] Waniek N., “Hexagonal grid fields optimally encode transitions in spatiotemporal sequences”, Neural Comput., 30 (2018), 2691–2725 <ext-link ext-link-type='doi' href='https://doi.org/10.1162/neco_a_01122'>10.1162/neco_a_01122</ext-link><ext-link ext-link-type='mr-item-id' href='http://mathscinet.ams.org/mathscinet-getitem?mr=3865579'>3865579</ext-link>

[95] Banino A., Barry C., Uria B., Blundell Ch., Lillicrap T., Mirowski P., Pritzel A., Chadwick M. J., Degris T., Modayil J. et al., “Vector-based navigation using grid-like representations in artificial agents”, Nature, 557 (2018), 429–433 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/s41586-018-0102-6'>10.1038/s41586-018-0102-6</ext-link>

[96] Solstad T., Moser E. I., Einevoll G. T., “From grid cells to place cells: A mathematical model”, Hippocampus, 16 (2006), 1026–1031 <ext-link ext-link-type='doi' href='https://doi.org/10.1002/hipo.20244'>10.1002/hipo.20244</ext-link>

[97] Giocomo L. M., Moser M. B., Moser E. I., “Computational models of grid cells”, Neuron, 71 (2011), 589–603 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.neuron.2011.07.023'>10.1016/j.neuron.2011.07.023</ext-link>

[98] Rennó-Costa C., Tort A. B. L., “Place and grid cells in a loop: implications for memory function and spatial coding”, J. Neurosci., 37 (2017), 8062–8076 <ext-link ext-link-type='doi' href='https://doi.org/10.1523/JNEUROSCI.3490-16.2017'>10.1523/JNEUROSCI.3490-16.2017</ext-link>

[99] Weber S. N., Sprekeler H., “Learning place cells, grid cells and invariances with excitatory and inhibitory plasticity”, eLife, 7 (2018), e34560 <ext-link ext-link-type='doi' href='https://doi.org/10.7554/eLife.34560'>10.7554/eLife.34560</ext-link>

[100] Rowland D. C., Roudi Y., Moser M. B., Moser E. I., “Ten years of grid cells”, Ann. Rev. Neurosci., 39 (2016), 19–40 <ext-link ext-link-type='doi' href='https://doi.org/10.1146/annurev-neuro-070815-013824'>10.1146/annurev-neuro-070815-013824</ext-link>

[101] Dombeck D. A., Harvey C. D., Tian L., Looger L. L., Tank D. W., “Functional imaging of hippocampal place cells at cellular resolution during virtual navigation”, Nat. Neurosci., 13 (2010), 1433–1440 <ext-link ext-link-type='doi' href='https://doi.org/10.1038/nn.2648'>10.1038/nn.2648</ext-link>

[102] Bonansco C., Fuenzalida M., “Plasticity of Hippocampal Excitatory-Inhibitory Balance: Missing the Synaptic Control in the Epileptic Brain”, Neural Plast., 2016 (2016), 8607038 <ext-link ext-link-type='doi' href='https://doi.org/10.1155/2016/8607038'>10.1155/2016/8607038</ext-link>

[103] Turing A. M., “The chemical basis of morphogenesis”, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 237:641 (1952), 37–72 <ext-link ext-link-type='doi' href='https://doi.org/10.1098/rstb.1952.0012'>10.1098/rstb.1952.0012</ext-link><ext-link ext-link-type='mr-item-id' href='http://mathscinet.ams.org/mathscinet-getitem?mr=3363444'>3363444</ext-link><ext-link ext-link-type='zbl-item-id' href='https://zbmath.org/?q=an:1403.92034'>1403.92034</ext-link>

[104] Domínguez U. R., Caplan J. B., “A hexagonal Fourier model of grid cells”, Hippocampus, 2018 <ext-link ext-link-type='doi' href='https://doi.org/10.1002/hipo.23028'>10.1002/hipo.23028</ext-link>

[105] Grieves R. M., Jeffery K. J., “The representation of space in the brain”, Behavioural Processes, 135 (2017), 113–131 <ext-link ext-link-type='doi' href='https://doi.org/10.1016/j.beproc.2016.12.012'>10.1016/j.beproc.2016.12.012</ext-link>