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Abstract

The medial entorhinal cortex (MEC) creates a neural representation of space through a set of functionally dedicated cell types: grid cells, border cells, head direction cells, and speed cells. Grid cells, the most abundant functional cell type in the MEC, have hexagonally arranged firing fields that tile the surface of the environment. These cells were discovered only in 2005, but after 10 years of investigation, we are beginning to understand how they are organized in the MEC network, how their periodic firing fields might be generated, how they are shaped by properties of the environment, and how they interact with the rest of the MEC network. The aim of this review is to summarize what we know about grid cells and point out where our knowledge is still incomplete.

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2016-07-08
2024-04-18
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Literature Cited

  1. Abrikosov AA. 1957. On the magnetic properties of superconductors of the second group. Sov. Phys. JETP 5:1174–82 [Google Scholar]
  2. Aghajan ZM, Acharya L, Moore JJ, Cushman JD, Vuong C, Mehta MR. 2015. Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality. Nat. Neurosci. 18:121–28 [Google Scholar]
  3. Alme CB, Miao C, Jezek K, Treves A, Moser EI, Moser MB. 2014. Place cells in the hippocampus: eleven maps for eleven rooms. PNAS 111:18428–35 [Google Scholar]
  4. Alonso A, Llinas RR. 1989. Subthreshold Na+-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342:175–77 [Google Scholar]
  5. Andermann ML, Gilfoy NB, Goldey GJ, Sachdev RN, Wolfel M. et al. 2013. Chronic cellular imaging of entire cortical columns in awake mice using microprisms. Neuron 80:900–13 [Google Scholar]
  6. Barry C, Ginzberg LL, O'Keefe J, Burgess N. 2012. Grid cell firing patterns signal environmental novelty by expansion. PNAS 109:17687–92 [Google Scholar]
  7. Barry C, Hayman R, Burgess N, Jeffery KJ. 2007. Experience-dependent rescaling of entorhinal grids. Nat. Neurosci. 10:682–84 [Google Scholar]
  8. Beed P, Bendels MH, Wiegand HF, Leibold C, Johenning FW, Schmitz D. 2010. Analysis of excitatory microcircuitry in the medial entorhinal cortex reveals cell-type-specific differences. Neuron 68:1059–66 [Google Scholar]
  9. Bjerknes TL, Langston RF, Kruge IU, Moser EI, Moser MB. 2015. Coherence among head direction cells before eye opening in rat pups. Curr. Biol. 25:103–8 [Google Scholar]
  10. Bjerknes TL, Moser EI, Moser MB. 2014. Representation of geometric borders in the developing rat. Neuron 82:71–78 [Google Scholar]
  11. Boccara CN, Sargolini F, Thoresen VH, Solstad T, Witter MP. et al. 2010. Grid cells in pre- and parasubiculum. Nat. Neurosci. 13:987–94 [Google Scholar]
  12. Bonnevie T, Dunn B, Fyhn M, Hafting T, Derdikman D. et al. 2013. Grid cells require excitatory drive from the hippocampus. Nat. Neurosci. 16:309–17 [Google Scholar]
  13. Bostock E, Muller RU, Kubie JL. 1991. Experience-dependent modifications of hippocampal place cell firing. Hippocampus 1:193–205 [Google Scholar]
  14. Brun VH, Otnæss MK, Molden S, Steffenach HA, Witter MP. et al. 2002. Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296:2243–46 [Google Scholar]
  15. Brun VH, Solstad T, Kjelstrup KB, Fyhn M, Witter MP. et al. 2008. Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex. Hippocampus 18:1200–12 [Google Scholar]
  16. Buetfering C, Allen K, Monyer H. 2014. Parvalbumin interneurons provide grid cell–driven recurrent inhibition in the medial entorhinal cortex. Nat. Neurosci. 17:710–18 [Google Scholar]
  17. Burak Y, Fiete IR. 2009. Accurate path integration in continuous attractor network models of grid cells. PLOS Comput. Biol. 5:e1000291 [Google Scholar]
  18. Burgalossi A, Herfst L, von Heimendahl M, Forste H, Haskic K. et al. 2011. Microcircuits of functionally identified neurons in the rat medial entorhinal cortex. Neuron 70:773–86 [Google Scholar]
  19. Buzsáki G, Moser EI. 2013. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 16:130–38 [Google Scholar]
  20. Canto CB, Witter MP. 2012. Cellular properties of principal neurons in the rat entorhinal cortex. II. The medial entorhinal cortex. Hippocampus 22:1277–99 [Google Scholar]
  21. Canto CB, Wouterlood FG, Witter MP. 2008. What does the anatomical organization of the entorhinal cortex tell us?. Neural Plast. 2008:381243 [Google Scholar]
  22. Cao Q, Miao C, Moser EI, Moser MB. 2015. Spatially periodic firing in grid cells requires local inhibition through parvalbumin interneurons Presented at Soc. Neurosci., Oct. 17, Chicago
  23. Carandini M, Ferster D. 2000. Membrane potential and firing rate in cat primary visual cortex. J. Neurosci. 20:470–84 [Google Scholar]
  24. Carpenter F, Manson D, Jeffery K, Burgess N, Barry C. 2015. Grid cells form a global representation of connected environments. Curr. Biol. 25:1176–82 [Google Scholar]
  25. Chen G, King JA, Burgess N, O'Keefe J. 2013. How vision and movement combine in the hippocampal place code. PNAS 110:378–83 [Google Scholar]
  26. Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL. et al. 2013. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499:295–300 [Google Scholar]
  27. Chen X, He Q, Kelly JW, Fiete IR, McNamara TP. 2015. Bias in human path integration is predicted by properties of grid cells. Curr. Biol. 25:1771–76 [Google Scholar]
  28. Cheng J, Ji D. 2013. Rigid firing sequences undermine spatial memory codes in a neurodegenerative mouse model. eLife 2:e00647 [Google Scholar]
  29. Cheng K. 1986. A purely geometric module in the rat's spatial representation. Cognition 23:149–78 [Google Scholar]
  30. Couey JJ, Witoelar A, Zhang SJ, Zheng K, Ye J. et al. 2013. Recurrent inhibitory circuitry as a mechanism for grid formation. Nat. Neurosci. 16:318–24 [Google Scholar]
  31. de Almeida L, Idiart M, Lisman JE. 2009. The input-output transformation of the hippocampal granule cells: from grid cells to place fields. J. Neurosci. 29:7504–12 [Google Scholar]
  32. Dehaene S, Cohen L. 2007. Cultural recycling of cortical maps. Neuron 56:384–98 [Google Scholar]
  33. Derdikman D, Whitlock JR, Tsao A, Fyhn M, Hafting T. et al. 2009. Fragmentation of grid cell maps in a multicompartment environment. Nat. Neurosci. 12:1325–32 [Google Scholar]
  34. Deshmukh SS, Knierim JJ. 2011. Representation of non-spatial and spatial information in the lateral entorhinal cortex. Front. Behav. Neurosci. 5:69 [Google Scholar]
  35. Dhillon A, Jones RS. 2000. Laminar differences in recurrent excitatory transmission in the rat entorhinal cortex in vitro. Neuroscience 99:413–22 [Google Scholar]
  36. Doeller CF, Barry C, Burgess N. 2010. Evidence for grid cells in a human memory network. Nature 463:657–61 [Google Scholar]
  37. Domnisoru C, Kinkhabwala AA, Tank DW. 2013. Membrane potential dynamics of grid cells. Nature 495:199–204 [Google Scholar]
  38. Donato F, Tsao A, Moser MB, Moser EI, Bonhoeffer T. 2014. 2-photon imaging of the medial entorhinal cortex in mice performing a virtual reality navigation task. Presented at Soc. Neurosci., Nov. 15, Washington, DC
  39. Dunn B, Mørreaunet M, Roudi Y. 2015. Correlations and functional connections in a population of grid cells. PLOS Comput. Biol. 11:e1004052 [Google Scholar]
  40. Fiete IR, Burak Y, Brookings T. 2008. What grid cells convey about rat location. J. Neurosci. 28:6858–71 [Google Scholar]
  41. Finkelstein A, Derdikman D, Rubin A, Foerster JN, Las L, Ulanovsky N. 2015. Three-dimensional head-direction coding in the bat brain. Nature 517:159–64 [Google Scholar]
  42. Flusberg BA, Nimmerjahn A, Cocker ED, Mukamel EA, Barretto RP. et al. 2008. High-speed, miniaturized fluorescence microscopy in freely moving mice. Nat. Methods 5:935–38 [Google Scholar]
  43. Fuhs MC, Vanrhoads SR, Casale AE, McNaughton B, Touretzky DS. 2005. Influence of path integration versus environmental orientation on place cell remapping between visually identical environments. J. Neurophysiol. 94:2603–16 [Google Scholar]
  44. Fyhn M, Hafting T, Treves A, Moser MB, Moser EI. 2007. Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446:190–94 [Google Scholar]
  45. Fyhn M, Hafting T, Witter MP, Moser EI, Moser MB. 2008. Grid cells in mice. Hippocampus 18:1230–38 [Google Scholar]
  46. Fyhn M, Molden S, Witter MP, Moser EI, Moser MB. 2004. Spatial representation in the entorhinal cortex. Science 305:1258–64 [Google Scholar]
  47. Gierer A, Meinhardt H. 1972. A theory of biological pattern formation. Kybernetik 12:30–39 [Google Scholar]
  48. Ginosar G, Finkelstein A, Rubin A, Las L, Ulanovsky N. 2015. 3D grid cells and border cells in flying bats Presented at Soc. Neurosci., Oct. 20, Chicago
  49. Gothard KM, Skaggs WE, Moore KM, McNaughton BL. 1996. Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J. Neurosci. 16:823–35 [Google Scholar]
  50. Guanella A, Kiper D, Verschure P. 2007. A model of grid cells based on a twisted torus topology. Int. J. Neural Syst. 17:231–40 [Google Scholar]
  51. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. 2005. Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–6 [Google Scholar]
  52. Hales JB, Schlesiger MI, Leutgeb JK, Squire LR, Leutgeb S, Clark RE. 2014. Medial entorhinal cortex lesions only partially disrupt hippocampal place cells and hippocampus-dependent place memory. Cell Rep. 9:893–901 [Google Scholar]
  53. Hargreaves EL, Rao G, Lee I, Knierim JJ. 2005. Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 308:1792–94 [Google Scholar]
  54. Hayman RMA, Verriotis MA, Jovalekic A, Fenton AA, Jeffery KJ. 2011. Anisotropic encoding of three-dimensional space by place cells and grid cells. Nat. Neurosci. 14:1182–88 [Google Scholar]
  55. Hayman RMA, Casali G, Wilson JJ, Jeffery KJ. 2015. Grid cells on steeply sloping terrain: evidence for planar rather than volumetric encoding. Front. Psychol. 6:925 [Google Scholar]
  56. Heys JG, Rangarajan KV, Dombeck DA. 2014. The functional micro-organization of grid cells revealed by cellular-resolution imaging. Neuron 84:1079–90 [Google Scholar]
  57. Hubel DH, Wiesel TN. 1959. Receptive fields of single neurones in the cat's striate cortex. J. Physiol. 148:574–91 [Google Scholar]
  58. Hubel DH, Wiesel TN. 1962. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. 160:106–54 [Google Scholar]
  59. Hubel DH, Wiesel TN. 1977. Ferrier lecture: functional architecture of macaque monkey visual cortex. Proc. R. Soc. B 198:1–59 [Google Scholar]
  60. Jacobs J, Weidemann CT, Miller JF, Solway A, Burke JF. et al. 2013. Direct recordings of grid-like neuronal activity in human spatial navigation. Nat. Neurosci. 16:1188–90 [Google Scholar]
  61. Jeffery KJ, Wilson JJ, Casali G, Hayman RM. 2015. Neural encoding of large-scale three-dimensional space-properties and constraints. Front. Psychol. 6:927 [Google Scholar]
  62. Jia H, Rochefort NL, Chen X, Konnerth A. 2011. In vivo two-photon imaging of sensory-evoked dendritic calcium signals in cortical neurons. Nat. Protoc. 6:28–35 [Google Scholar]
  63. Jung MW, Wiener SI, McNaughton BL. 1994. Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J. Neurosci. 14:7347–56 [Google Scholar]
  64. Killian NJ, Jutras MJ, Buffalo EA. 2012. A map of visual space in the primate entorhinal cortex. Nature 491:761–64 [Google Scholar]
  65. Kitamura T, Pignatelli M, Suh J, Kohara K, Yoshiki A. et al. 2014. Island cells control temporal association memory. Science 343:896–901 [Google Scholar]
  66. Kjelstrup KB, Solstad T, Brun VH, Hafting T, Leutgeb S. et al. 2008. Finite scale of spatial representation in the hippocampus. Science 321:140–43 [Google Scholar]
  67. Klink R, Alonso A. 1997. Ionic mechanisms of muscarinic depolarization in entorhinal cortex layer II neurons. J. Neurophysiol. 77:1829–43 [Google Scholar]
  68. Ko H, Hofer SB, Pichler B, Buchanan KA, Sjöström PJ, Mrsic-Flogel TD. 2011. Functional specificity of local synaptic connections in neocortical networks. Nature 473:87–91 [Google Scholar]
  69. Kondo S, Miura T. 2010. Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329:1616–20 [Google Scholar]
  70. Konishi M. 2003. Coding of auditory space. Annu. Rev. Neurosci. 26:31–55 [Google Scholar]
  71. Kropff E, Carmichael JE, Moser MB, Moser EI. 2015. Speed cells in the medial entorhinal cortex. Nature 523:419–24 [Google Scholar]
  72. Kropff E, Treves A. 2008. The emergence of grid cells: intelligent design or just adaptation?. Hippocampus 18:1256–69 [Google Scholar]
  73. Krupic J, Bauza M, Burton S, Barry C, O'Keefe J. 2015. Grid cell symmetry is shaped by environmental geometry. Nature 518:232–35 [Google Scholar]
  74. Kunz L, Schroder TN, Lee H, Montag C, Lachmann B. et al. 2015. Reduced grid-cell-like representations in adults at genetic risk for Alzheimer's disease. Science 350:430–33 [Google Scholar]
  75. Langston RF, Ainge JA, Couey JJ, Canto CB, Bjerknes TL. et al. 2010. Development of the spatial representation system in the rat. Science 328:1576–80 [Google Scholar]
  76. Li Y, Lu H, Cheng PL, Ge S, Xu H. et al. 2012. Clonally related visual cortical neurons show similar stimulus feature selectivity. Nature 486:118–21 [Google Scholar]
  77. Low RJ, Gu Y, Tank DW. 2014. Cellular resolution optical access to brain regions in fissures: imaging medial prefrontal cortex and grid cells in entorhinal cortex. PNAS 111:18739–44 [Google Scholar]
  78. Marshel JH, Mori T, Nielsen KJ, Callaway EM. 2010. Targeting single neuronal networks for gene expression and cell labeling in vivo. Neuron 67:562–74 [Google Scholar]
  79. Mathis A, Herz AVM, Stemmler MB. 2012. Optimal population codes for space: Grid cells outperform place cells. Neural Comput. 24:2280–317 [Google Scholar]
  80. Mathis A, Herz AVM, Stemmler MB. 2013. Multiscale codes in the nervous system: the problem of noise correlations and the ambiguity of periodic scales. Phys. Rev. E 88:022713 [Google Scholar]
  81. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB. 2006. Path integration and the neural basis of the ‘cognitive map.’. Nat. Rev. Neurosci. 7:663–78 [Google Scholar]
  82. Miao C, Cao Q, Ito HT, Yamahachi H, Witter MP. et al. 2015. Hippocampal remapping after partial inactivation of the medial entorhinal cortex. Presented at Soc. Neurosci., Oct. 17, Chicago
  83. Miller VM, Best PJ. 1980. Spatial correlates of hippocampal unit activity are altered by lesions of the fornix and endorhinal cortex. Brain Res. 194:311–23 [Google Scholar]
  84. Monaco JD, Abbott LF. 2011. Modular realignment of entorhinal grid cell activity as a basis for hippocampal remapping. J. Neurosci. 31:9414–25 [Google Scholar]
  85. Moser EI, Roudi Y, Witter MP, Kentros C, Bonhoeffer T, Moser MB. 2014. Grid cells and cortical representation. Nat. Rev. Neurosci. 15:466–81 [Google Scholar]
  86. Mountcastle VB. 1957. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J. Neurophysiol. 20:408–34 [Google Scholar]
  87. Muessig L, Hauser J, Wills TJ, Cacucci F. 2015. A developmental switch in place cell accuracy coincides with grid cell maturation. Neuron 86:1167–73 [Google Scholar]
  88. Muller RU, Kubie JL. 1987. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 7:1951–68 [Google Scholar]
  89. Naber PA, Lopes da Silva FH, Witter MP. 2001. Reciprocal connections between the entorhinal cortex and hippocampal fields CA1 and the subiculum are in register with the projections from CA1 to the subiculum. Hippocampus 11:99–104 [Google Scholar]
  90. Nakao H, Mikhailov AS. 2010. Turing patterns in network-organized activator-inhibitor systems. Nat. Phys. 6:544–50 [Google Scholar]
  91. Navratilova Z, Godfrey KB, McNaughton BL. 2016. Grids from bands, or bands from grids? An examination of the effects of single unit contamination on grid cell firing fields. J. Neurophysiol. 115992–1002
  92. O'Keefe J. 1976. Place units in the hippocampus of the freely moving rat. Exp. Neurol. 51:78–109 [Google Scholar]
  93. O'Keefe J, Burgess N. 1996. Geometric determinants of the place fields of hippocampal neurons. Nature 381:425–28 [Google Scholar]
  94. O'Keefe J, Conway DH. 1978. Hippocampal place units in the freely moving rat: Why they fire where they fire. Exp. Brain Res. 31:573–90 [Google Scholar]
  95. O'Keefe J, Dostrovsky J. 1971. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34:171–75 [Google Scholar]
  96. O'Keefe J, Nadel L. 1978. The Hippocampus as a Cognitive Map Oxford, UK: Clarendon
  97. Ormond J, McNaughton BL. 2015. Place field expansion after focal MEC inactivations is consistent with loss of Fourier components and path integrator gain reduction. PNAS 112:4116–21 [Google Scholar]
  98. Ouyang Q, Swinney HL. 1991. Transition from a uniform state to hexagonal and striped Turing patterns. Nature 352:610–12 [Google Scholar]
  99. Pastalkova E, Itskov V, Amarasingham A, Buzsáki G. 2008. Internally generated cell assembly sequences in the rat hippocampus. Science 321:1322–27 [Google Scholar]
  100. Quirk GJ, Muller RU, Kubie JL. 1990. The firing of hippocampal place cells in the dark depends on the rat's recent experience. J. Neurosci. 10:2008–17 [Google Scholar]
  101. Quirk GJ, Muller RU, Kubie JL, Ranck JB Jr. 1992. The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells. J. Neurosci. 12:1945–63 [Google Scholar]
  102. Ranck J. 1985. Head direction cells in the deep cell layer of the dorsal presubiculum in freely moving rats. Electrical Activity of the Archicortex G Buzsáki, CH Vanderwolf, 217–20 Budapest, Hung: Akadémiai Kiadó [Google Scholar]
  103. Rancz EA, Franks KM, Schwarz MK, Pichler B, Schaefer AT, Margrie TW. 2011. Transfection via whole-cell recording in vivo: bridging single-cell physiology, genetics and connectomics. Nat. Neurosci. 14:527–32 [Google Scholar]
  104. Ravassard P, Kees A, Willers B, Ho D, Aharoni D. et al. 2013. Multisensory control of hippocampal spatiotemporal selectivity. Science 340:1342–46 [Google Scholar]
  105. Ray S, Naumann R, Burgalossi A, Tang Q, Schmidt H, Brecht M. 2014. Grid-layout and theta-modulation of layer 2 pyramidal neurons in medial entorhinal cortex. Science 343:891–96 [Google Scholar]
  106. Rigotti M, Barak O, Warden MR, Wang XJ, Daw ND. et al. 2013. The importance of mixed selectivity in complex cognitive tasks. Nature 497:585–90 [Google Scholar]
  107. Rigotti M, Ben Dayan Rubin D, Wang XJ, Fusi S. 2010. Internal representation of task rules by recurrent dynamics: the importance of the diversity of neural responses. Front. Comput. Neurosci. 4:24 [Google Scholar]
  108. Rolls ET, Stringer SM, Elliot T. 2006. Entorhinal cortex grid cells can map to hippocampal place cells by competitive learning. Network 17:447–65 [Google Scholar]
  109. Roudi Y, Moser EI. 2014. Grid cells in an inhibitory network. Nat. Neurosci. 17:639–41 [Google Scholar]
  110. Rowland DC, Moser MB. 2014. From cortical modules to memories. Curr. Opin. Neurobiol. 24:22–27 [Google Scholar]
  111. Rowland DC, Weible AP, Wickersham IR, Wu H, Mayford M. et al. 2013. Transgenically targeted rabies virus demonstrates a major monosynaptic projection from hippocampal area CA2 to medial entorhinal layer II neurons. J. Neurosci. 33:14889–98 [Google Scholar]
  112. Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP. et al. 2006. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312:758–62 [Google Scholar]
  113. Savelli F, Knierim JJ. 2010. Hebbian analysis of the transformation of medial entorhinal grid-cell inputs to hippocampal place fields. J. Neurophysiol. 103:3167–83 [Google Scholar]
  114. Schlesiger MI, Cannova CC, Boublil BL, Hales JB, Mankin EA. et al. 2015. The medial entorhinal cortex is necessary for temporal organization of hippocampal neuronal activity. Nat. Neurosci. 18:1123–32 [Google Scholar]
  115. Schmidt-Hieber C, Hausser M. 2013. Cellular mechanisms of spatial navigation in the medial entorhinal cortex. Nat. Neurosci. 16:325–31 [Google Scholar]
  116. Seelig JD, Jayaraman V. 2015. Neural dynamics for landmark orientation and angular path integration. Nature 521:186–91 [Google Scholar]
  117. Si B, Kropff E, Treves A. 2012. Grid alignment in entorhinal cortex. Biol. Cybern. 106:483–506 [Google Scholar]
  118. Si B, Treves A. 2013. A model for the differentiation between grid and conjunctive units in medial entorhinal cortex. Hippocampus 23:1410–24 [Google Scholar]
  119. Skaggs WE, Knierim JJ, Kudrimoti HS, McNaughton BL. 1995. A model of the neural basis of the rat's sense of direction. Adv. Neural Inf. Process. Syst. 7:173–80 [Google Scholar]
  120. Smith SL, Smith IT, Branco T, Hausser M. 2013. Dendritic spikes enhance stimulus selectivity in cortical neurons in vivo. Nature 503:115–20 [Google Scholar]
  121. Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI. 2008. Representation of geometric borders in the entorhinal cortex. Science 322:1865–68 [Google Scholar]
  122. Solstad T, Moser EI, Einevoll GT. 2006. From grid cells to place cells: a mathematical model. Hippocampus 16:1026–31 [Google Scholar]
  123. Sreenivasan S, Fiete I. 2011. Grid cells generate an analog error-correcting code for singularly precise neural computation. Nat. Neurosci. 14:1330–37 [Google Scholar]
  124. Stella F, Si B, Kropff E, Treves A. 2013. Grid maps for spaceflight, anyone? They are for free!. Behav. Brain Sci. 36:566–67 [Google Scholar]
  125. Stella F, Treves A. 2015. The self-organization of grid cells in 3D. eLife 4:e05913 [Google Scholar]
  126. Stemmler M, Mathis A, Herz AV. 2015. Connecting multiple spatial scales to decode the population activity of grid cells. Sci. Adv. 1:e1500816 [Google Scholar]
  127. Stensola H, Stensola T, Solstad T, Froland K, Moser MB, Moser EI. 2012. The entorhinal grid map is discretized. Nature 492:72–78 [Google Scholar]
  128. Stensola T, Stensola H, Moser MB, Moser EI. 2015. Shearing-induced asymmetry in entorhinal grid cells. Nature 518:207–12 [Google Scholar]
  129. Sun C, Kitamura T, Yamamoto J, Martin J, Pignatelli M. et al. 2015. Distinct speed dependence of entorhinal island and ocean cells, including respective grid cells. PNAS 112:9466–71 [Google Scholar]
  130. Tan HM, Bassett JP, O'Keefe J, Cacucci F, Wills TJ. 2015. The development of the head direction system before eye opening in the rat. Curr. Biol. 25:479–83 [Google Scholar]
  131. Tang Q, Burgalossi A, Ebbesen CL, Sanguinetti-Scheck JI, Schmidt H. et al. 2016. Functional architecture of the rat parasubiculum. J. Neurosci. 36:72289–301 [Google Scholar]
  132. Taube JS, Muller RU, Ranck JB Jr. 1990a. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10:420–35 [Google Scholar]
  133. Taube JS, Muller RU, Ranck JB Jr. 1990b. Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J. Neurosci. 10:436–47 [Google Scholar]
  134. Terrazas A, Krause M, Lipa P, Gothard KM, Barnes CA, McNaughton BL. 2005. Self-motion and the hippocampal spatial metric. J. Neurosci. 25:8085–96 [Google Scholar]
  135. Tocker G, Barak O, Derdikman D. 2015. Grid cells correlation structure suggests organized feedforward projections into superficial layers of the medial entorhinal cortex. Hippocampus 25:1599–613 [Google Scholar]
  136. Tsao A, Moser MB, Moser EI. 2013. Traces of experience in the lateral entorhinal cortex. Curr. Biol. 23:399–405 [Google Scholar]
  137. Turing AM. 1952. The chemical basis of morphogenesis. Philos. Trans. R. Soc. 237:37–72 [Google Scholar]
  138. Ulanovsky N. 2011. Neuroscience: How is three-dimensional space encoded in the brain?. Curr. Biol. 21:R886–88 [Google Scholar]
  139. Urdapilleta E, Troiani F, Stella F, Treves A. 2015. Can rodents conceive hyperbolic spaces?. J. R. Soc. Interface 12:20141214 [Google Scholar]
  140. Van Cauter T, Poucet B, Save E. 2008. Unstable CA1 place cell representation in rats with entorhinal cortex lesions. Eur. J. Neurosci. 27:1933–46 [Google Scholar]
  141. Villette V, Malvache A, Tressard T, Dupuy N, Cossart R. 2015. Internally recurring hippocampal sequences as a population template of spatiotemporal information. Neuron 88:357–66 [Google Scholar]
  142. Wei XX, Prentice J, Balasubramanian V. 2015. A principle of economy predicts the functional architecture of grid cells. eLife 4:e08362 [Google Scholar]
  143. Wernle T, Mørreaunet M, Moser EI, Moser MB. 2015. Grid synchronization in merged space. Presented at Soc. Neurosci., Oct. 17, Chicago
  144. Wertz A, Trenholm S, Yonehara K, Hillier D, Raics Z. et al. 2015. Single-cell-initiated monosynaptic tracing reveals layer-specific cortical network modules. Science 349:70–74 [Google Scholar]
  145. Wills TJ, Cacucci F, Burgess N, O'Keefe J. 2010. Development of the hippocampal cognitive map in preweanling rats. Science 328:1573–76 [Google Scholar]
  146. Wilson MA, McNaughton BL. 1993. Dynamics of the hippocampal ensemble code for space. Science 261:1055–58 [Google Scholar]
  147. Yartsev MM, Ulanovsky N. 2013. Representation of three-dimensional space in the hippocampus of flying bats. Science 340:367–72 [Google Scholar]
  148. Yartsev MM, Witter MP, Ulanovsky N. 2011. Grid cells without theta oscillations in the entorhinal cortex of bats. Nature 479:103–7 [Google Scholar]
  149. Ye J, Zhang S-J, Kropff E, Moser MB, Moser EI. 2015. Entorhinal speed cells project to the hippocampus. Presented at Soc. Neurosci., Oct. 17, Chicago
  150. Yoganarasimha D, Yu X, Knierim JJ. 2006. Head direction cell representations maintain internal coherence during conflicting proximal and distal cue rotations: comparison with hippocampal place cells. J. Neurosci. 26:622–31 [Google Scholar]
  151. Yoon K, Buice MA, Barry C, Hayman R, Burgess N, Fiete IR. 2013. Specific evidence of low-dimensional continuous attractor dynamics in grid cells. Nat. Neurosci. 16:1077–84 [Google Scholar]
  152. Yoshida M, Jochems A, Hasselmo ME. 2013. Comparison of properties of medial entorhinal cortex layer II neurons in two anatomical dimensions with and without cholinergic activation. PLOS ONE 8:e73904 [Google Scholar]
  153. Yu YC, Bultje RS, Wang X, Shi SH. 2009. Specific synapses develop preferentially among sister excitatory neurons in the neocortex. Nature 458:501–4 [Google Scholar]
  154. Zhang K. 1996. Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J. Neurosci. 16:2112–26 [Google Scholar]
  155. Zhang SJ, Ye J, Miao C, Tsao A, Cerniauskas I. et al. 2013. Optogenetic dissection of entorhinal-hippocampal functional connectivity. Science 340:1232627 [Google Scholar]
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