How animals find their way in space. Experiments and modeling

Yakov Kazanovich ; Ivan E. Mysin

Matematičeskaâ biologiâ i bioinformatika, Tome 13 (2018) no. 3, pp. t132-t161

Résumé

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.

Bibliographie

[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 | DOI | DOI

[2] O'Keefe J., “Place units in the hippocampus of the freely moving rat”, Exp. Neurol., 51 (1976), 78–109 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[6] Abbott A., “Neuroscience: Brains of Norway”, Nature, 514 (2014), 154–157 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[11] Taube J. S., Bassett J. P., “Persistent neural activity in head direction cells”, Cerebral Cortex, 13 (2003), 1162–1172 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | Zbl | DOI | Zbl

[15] Eichenbaum H., “Time cells in the hippocampus: a new dimension for mapping memories”, Nat. Rev. Neurosci., 15 (2014), 732–744 | DOI | DOI

[16] Kropff E., Carmichael J. E., Moser M. B., Moser E. I., “Speed cells in the medial entorhinal cortex”, Nature, 523 (2015), 419–424 | DOI | DOI

[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 | DOI | DOI

[18] Hoydal O. A., Skytoen E. R., Moser M.-B., Moser E. I., “Object-vector coding in the medial entorhinal cortex”, BioRxiv, 2018 | DOI | DOI

[19] Yartsev M. M., Ulanovsky N., “Representation of three-dimensional space in the hippocampus of flying bats”, Science, 340 (2013), 367–372 | DOI | DOI

[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) http://www.pigeon.psy.tufts.edu/asc/Bingman

[21] Hopfield J. J., “Neural networks and physical systems with emergent collective computational abilities”, PNAS, 79 (1982), 2554–2558 | DOI | MR | Zbl | DOI | MR | Zbl

[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 | DOI | DOI

[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 | DOI | DOI

[24] Damasio A. R., “The brain binds entities and events by multiregional activation from convergence zones”, Neural Comput., 1 (1989), 123–132 | DOI | DOI

[25] Buzsaki G., Moser E. I., “Memory, navigation and theta rhythm in the hippocampalentorhinal system”, Nat. Neurosci., 16 (2013), 130–138 | DOI | DOI

[26] Eichenbaum H., Cohen N. J., Can we reconcile the declarative memory and spatial navigation views on hippocampal function?, Neuron, 83 (2014), 764–770 | DOI | DOI

[27] Witter M. P., Moser E. I., “Spatial representation and the architecture of the entorhinal cortex”, Trends Neurosci., 29 (2006), 671–678 | DOI | DOI

[28] Burgalossi A., Brecht M., “Cellular, columnar and modular organization of spatial representations in medial entorhinal cortex”, Curr. Opin. Neurobiol., 24 (2014), 47–54 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[31] Wilson M. A., McNaughton B. L., “Dynamics of the hippocampal ensemble code for space”, Science, 261 (1993), 1055–1058 | DOI | DOI

[32] Bird C. M., Burgess N., “The hippocampus and memory: insights from spatial processing”, Nat. Rev. Neurosci., 9 (2008), 182–194 | DOI | MR | DOI | MR

[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 | DOI | DOI

[34] Louie K., Wilson M. A., “Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep”, Neuron, 29 (2001), 145–156 | DOI | DOI

[35] O'Keefe J., Recce M. L., “Phase relationship between hippocampal place units and the EEG theta rhythm”, Hippocampus, 3 (1993), 317–330 | DOI | MR | DOI | MR

[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 | 3.0.CO;2-K class='badge bg-secondary rounded-pill ref-badge extid-badge'>DOI | DOI

[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) | DOI | DOI

[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 | DOI | DOI

[39] Fyhn M., Hafting T., Witter M. P., Moser E. I., Moser M. B., “Grid cells in mice”, Hippocampus, 18 (2008), 1230–1238 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[47] Rowland D. C., “Functional properties of stellate cells in medial entorhinal cortex layer II”, eLife, 7 (2018), e36664 | DOI | DOI

[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 | DOI | MR | DOI | MR

[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 | DOI | DOI

[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 | DOI | DOI

[51] Krupic J., Bauza M., Burton S., O'Keefe J., “Local transformations of the hippocampal cognitive map”, Science, 359 (2018), 1143–1146 | DOI | DOI

[52] Buzsáki G., “Theta oscillations in the hippocampus”, Neuron, 33 (2002), 325–340 | DOI | DOI

[53] Vinogradova O. S., “Expression, control, and probable functional significance of the neuronal theta-rhythm”, Prog. Neurobiol., 45 (1995), 523–583 | DOI | DOI

[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 | DOI | DOI

[55] Gonzalez-Sulser A., Nolan M. F., “Grid cells' need for speed”, Nat. Neurosci., 20 (2016), 1–2 | DOI | DOI

[56] Hayman R., Burgess N., “Disrupting the grid cells' need for speed”, Neuron, 91 (2016), 502–503 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[59] Ledberg A., Robbe D., “Locomotion-related oscillatory body movements at 6–12 Hz modulate the hippocampal theta rhythm”, PLoS ONE, 6 (2011), e27575 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[64] Wills T. J., Cacucci F., “The development of the hippocampal neural representation of space”, Curr. Opin. Neurobiol., 24 (2014), 111–119 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[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) http://www.scholarpedia.org/article/Head_direction_cells

[71] Manns J.R., Howard M., Eichenbaum H., “Gradual changes in hippocampal activity support remembering the order of events”, Neuron, 56 (2007), 530–540 | DOI | DOI

[72] Pastalkova E., Itskov V., Amarasingham A., Buzsáki G., “Internally generated cell assembly sequences in the rat hippocampus”, Science, 321 (2008), 1322–1327 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[76] Ponulak F., Hopfield J. J., “Rapid, parallel path planning by propagating wavefronts of spiking neural activity”, Front. Comput. Neurosci., 7 (2013), e98 | DOI | DOI

[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 | DOI | DOI

[78] Roberts P. D., Leen T. K., “Anti-hebbian spike-timing-dependent plasticity and adaptive sensory processing”, Front. Comput. Neurosci., 4 (2010), 1–11 | DOI | DOI

[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 | DOI | DOI

[80] Burak Y., “Spatial coding and attractor dynamics of grid cells in the entorhinal cortex”, Curr. Opin. Neurobiol., 25 (2014), 169–175 | DOI | DOI

[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 | DOI | DOI

[82] Burgess N., “Grid cells and theta as oscillatory interference: Theory and predictions”, Hippocampus, 18 (2008), 1157–1174 | DOI | DOI

[83] Burgess C. P., Burgess N., “Controlling phase noise in oscillatory interference models of grid cell firing”, J. Neurosci., 34 (2014), 6224–6232 | DOI | DOI

[84] Burgess N., Barry C., O'Keefe J., “An oscillatory interference model of grid cell firing”, Hippocampus, 17 (2007), 801–812 | DOI | DOI

[85] Bush D., Burgess N., “A hybrid oscillatory interference/continuous attractor network model of grid cell firing”, J. Neurosci., 34 (2014), 5065–5079 | DOI | DOI

[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 | DOI | DOI

[87] Burak Y., Fiete I. R., “Accurate path integration in continuous attractor network models of grid cells”, PLoS Comput. Biol., 5:2 (2009), e1000291 | DOI | MR | DOI | MR

[88] Fuhs M. C., “A spin glass model of path integration in rat medial entorhinal cortex”, J. Neurosci., 26 (2006), 4266–4276 | DOI | DOI

[89] Si B., Treves A., “A model for the differentiation between grid and conjunctive units in medial entorhinal cortex”, Hippocampus, 23 (2013), 1410–1424 | DOI | DOI

[90] Si B., Kropff E., Treves A., “Grid alignment in entorhinal cortex”, Biol. Cybern., 106 (2012), 483–506 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[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 | DOI | DOI

[94] Waniek N., “Hexagonal grid fields optimally encode transitions in spatiotemporal sequences”, Neural Comput., 30 (2018), 2691–2725 | DOI | MR | DOI | MR

[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 | DOI | DOI

[96] Solstad T., Moser E. I., Einevoll G. T., “From grid cells to place cells: A mathematical model”, Hippocampus, 16 (2006), 1026–1031 | DOI | DOI

[97] Giocomo L. M., Moser M. B., Moser E. I., “Computational models of grid cells”, Neuron, 71 (2011), 589–603 | DOI | DOI

[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 | DOI | DOI

[99] Weber S. N., Sprekeler H., “Learning place cells, grid cells and invariances with excitatory and inhibitory plasticity”, eLife, 7 (2018), e34560 | DOI | DOI

[100] Rowland D. C., Roudi Y., Moser M. B., Moser E. I., “Ten years of grid cells”, Ann. Rev. Neurosci., 39 (2016), 19–40 | DOI | DOI

[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 | DOI | DOI

[102] Bonansco C., Fuenzalida M., “Plasticity of Hippocampal Excitatory-Inhibitory Balance: Missing the Synaptic Control in the Epileptic Brain”, Neural Plast., 2016 (2016), 8607038 | DOI | DOI

[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 | DOI | MR | Zbl | DOI | MR | Zbl

[104] Domínguez U. R., Caplan J. B., “A hexagonal Fourier model of grid cells”, Hippocampus, 2018 | DOI | DOI

[105] Grieves R. M., Jeffery K. J., “The representation of space in the brain”, Behavioural Processes, 135 (2017), 113–131 | DOI | DOI