Ten Years of Grid Cells

Annual Review of Neuroscience

Volumn 39, Issue , 2016, Pages 19-40

  Rowland, David C ^a   Roudi, Yasser ^a   Moser, May Britt ^a   Moser, Edvard I ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

Association cortex; Attractor networks; Entorhinal cortex; Hippocampus; Memory; Spatial navigation

Indexed keywords

ARTICLE; CELL FUNCTION; CELL INTERACTION; CELL POPULATION; CELL SURFACE; CELLS BY BODY ANATOMY; ENVIRONMENTAL FACTOR; FIRING RATE; GEOMETRY; GRID CELL; HIPPOCAMPUS; HUMAN; MEDIAL ENTORHINAL CORTEX; NONHUMAN; PRIORITY JOURNAL; SPIKE WAVE; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; ENTORHINAL CORTEX; NERVE CELL; NERVE CELL NETWORK; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; ENTORHINAL CORTEX; GRID CELLS; HUMANS; MODELS, NEUROLOGICAL; NERVE NET; NEURONS;

EID: 84979502944     PISSN: 0147006X     EISSN: 15454126     Source Type: Book Series    
DOI: 10.1146/annurev-neuro-070815-013824     Document Type: Article

References (155)

1. Abrikosov AA. 1957. On the magnetic properties of superconductors of the second group. Sov. Phys. JETP 5: 1174-82
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
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
4. Alonso A, Llinas RR. 1989. Subthreshold Na+-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342: 175-77
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
6. Barry C, Ginzberg LL, O'Keefe J, Burgess N. 2012. Grid cell firing patterns signal environmental novelty by expansion. PNAS 109: 17687-92
7. Barry C, Hayman R, Burgess N, Jeffery KJ. 2007. Experience-dependent rescaling of entorhinal grids. Nat. Neurosci. 10: 682-84
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
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
10. Bjerknes TL, Moser EI, Moser MB. 2014. Representation of geometric borders in the developing rat. Neuron 82: 71-78
11. Boccara CN, Sargolini F, Thoresen VH, Solstad T, WitterMP, et al. 2010. Grid cells in pre-and parasubiculum. Nat. Neurosci. 13: 987-94
12. Bonnevie T, Dunn B, FyhnM, Hafting T, Derdikman D, et al. 2013. Grid cells require excitatory drive from the hippocampus. Nat. Neurosci. 16: 309-17
13. Bostock E, Muller RU, Kubie JL. 1991. Experience-dependent modifications of hippocampal place cell firing. Hippocampus 1: 193-205
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
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
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
17. Burak Y, Fiete IR. 2009. Accurate path integration in continuous attractor network models of grid cells. PLOS Comput. Biol. 5: e1000291
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
19. Buzsáki G, Moser EI. 2013. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 16: 130-38
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
21. Canto CB, Wouterlood FG, Witter MP. 2008. What does the anatomical organization of the entorhinal cortex tell us Neural Plast. 2008: 381243
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
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
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
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
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
28. Cheng J, Ji D. 2013. Rigid firing sequences undermine spatial memory codes in a neurodegenerative mouse model. eLife 2: e00647
29. Cheng K. 1986. A purely geometric module in the rat's spatial representation. Cognition 23: 149-78
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
31. de Almeida L, IdiartM, Lisman JE. 2009. The input-output transformation of the hippocampal granule cells: from grid cells to place fields. J. Neurosci. 29: 7504-12
32. Dehaene S, Cohen L. 2007. Cultural recycling of cortical maps. Neuron 56: 384-98
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
34. Deshmukh SS, Knierim JJ. 2011. Representation of non-spatial and spatial information in the lateral entorhinal cortex. Front. Behav. Neurosci. 5: 69
35. Dhillon A, Jones RS. 2000. Laminar differences in recurrent excitatory transmission in the rat entorhinal cortex in vitro. Neuroscience 99: 413-22
36. DoellerCF, Barry C, BurgessN. 2010. Evidence for grid cells in a human memory network. Nature 463: 657-61
37. DomnisoruC, Kinkhabwala AA, TankDW. 2013. Membrane potential dynamics of grid cells. Nature 495: 199-204
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, MørreaunetM, Roudi Y. 2015. Correlations and functional connections in a population of grid cells. PLOS Comput. Biol. 11: e1004052
40. Fiete IR, Burak Y, Brookings T. 2008. What grid cells convey about rat location. J. Neurosci. 28: 6858-71
41. Finkelstein A, Derdikman D, Rubin A, Foerster JN, Las L, Ulanovsky N. 2015. Three-dimensional headdirection coding in the bat brain. Nature 517: 159-64
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
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
44. Fyhn M, Hafting T, Treves A, Moser MB, Moser EI. 2007. Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446: 190-94
45. Fyhn M, Hafting T, Witter MP, Moser EI, Moser MB. 2008. Grid cells in mice. Hippocampus 18: 1230-38
46. Fyhn M, Molden S, Witter MP, Moser EI, Moser MB. 2004. Spatial representation in the entorhinal cortex. Science 305: 1258-64
47. Gierer A, Meinhardt H. 1972. A theory of biological pattern formation. Kybernetik 12: 30-39
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
50. Guanella A, Kiper D, Verschure P. 2007. Amodel of grid cells based on a twisted torus topology. Int. J. Neural Syst. 17: 231-40
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
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
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
54. Hayman RMA, Verriotis MA, Jovalekic A, Fenton AA, Jeffery KJ. 2011. Anisotropic encoding of threedimensional space by place cells and grid cells. Nat. Neurosci. 14: 1182-88
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
56. Heys JG, Rangarajan KV, Dombeck DA. 2014. The functional micro-organization of grid cells revealed by cellular-resolution imaging. Neuron 84: 1079-90
57. HubelDH, Wiesel TN. 1959. Receptive fields of single neurones in the cat's striate cortex. J. Physiol. 148: 574-91
58. Hubel DH, Wiesel TN. 1962. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. 160: 106-54
59. Hubel DH, Wiesel TN. 1977. Ferrier lecture: functional architecture of macaque monkey visual cortex. Proc. R. Soc. B 198: 1-59
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
61. Jeffery KJ, Wilson JJ, Casali G, Hayman RM. 2015. Neural encoding of large-scale three-dimensional spaceproperties and constraints. Front. Psychol. 6: 927
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
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
64. Killian NJ, Jutras MJ, Buffalo EA. 2012. A map of visual space in the primate entorhinal cortex. Nature 491: 761-64
65. Kitamura T, Pignatelli M, Suh J, Kohara K, Yoshiki A, et al. 2014. Island cells control temporal association memory. Science 343: 896-901
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
67. Klink R, Alonso A. 1997. Ionicmechanisms of muscarinic depolarization in entorhinal cortex layer II neurons. J. Neurophysiol. 77: 1829-43
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
69. Kondo S, Miura T. 2010. Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329: 1616-20
70. Konishi M. 2003. Coding of auditory space. Annu. Rev. Neurosci. 26: 31-55
71. Kropff E, Carmichael JE, Moser MB, Moser EI. 2015. Speed cells in the medial entorhinal cortex. Nature 523: 419-24
72. Kropff E, Treves A. 2008. The emergence of grid cells: intelligent design or just adaptation? Hippocampus 18: 1256-69
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
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
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
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
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
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
79. Mathis A, Herz AVM, Stemmler MB. 2012. Optimal population codes for space: Grid cells outperform place cells. Neural Comput. 24: 2280-317
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
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
82. Miao C, Cao Q, ItoHT, YamahachiH, WitterMP, 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
84. Monaco JD, Abbott LF. 2011. Modular realignment of entorhinal grid cell activity as a basis for hippocampal remapping. J. Neurosci. 31: 9414-25
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
86. Mountcastle VB. 1957. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J. Neurophysiol. 20: 408-34
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
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
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
90. Nakao H, Mikhailov AS. 2010. Turing patterns in network-organized activator-inhibitor systems. Nat. Phys. 6: 544-50
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. 115: 992-1002
92. O'Keefe J. 1976. Place units in the hippocampus of the freely moving rat. Exp. Neurol. 51: 78-109
93. O'Keefe J, Burgess N. 1996. Geometric determinants of the place fields of hippocampal neurons. Nature 381: 425-28
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
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
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
98. Ouyang Q, Swinney HL. 1991. Transition from a uniform state to hexagonal and striped Turing patterns. Nature 352: 610-12
99. Pastalkova E, Itskov V, Amarasingham A, Buzsáki G. 2008. Internally generated cell assembly sequences in the rat hippocampus. Science 321: 1322-27
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
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
102. Ranck J. 1985. Head direction cells in the deep cell layer of the dorsal presubiculum in freely moving rats. In Electrical Activity of the Archicortex, ed. G Buzsáki, CH Vanderwolf, pp. 217-20. Budapest, Hung.
103. Akadémiai Kiadó 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
104. Ravassard P, Kees A, Willers B, Ho D, Aharoni D, et al. 2013. Multisensory control of hippocampal spatiotemporal selectivity. Science 340: 1342-46
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
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
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
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
109. Roudi Y, Moser EI. 2014. Grid cells in an inhibitory network. Nat. Neurosci. 17: 639-41
110. Rowland DC, Moser MB. 2014. From cortical modules to memories. Curr. Opin. Neurobiol. 24: 22-27
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
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
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
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
115. Schmidt-Hieber C, Hausser M. 2013. Cellular mechanisms of spatial navigation in the medial entorhinal cortex. Nat. Neurosci. 16: 325-31
116. Seelig JD, Jayaraman V. 2015. Neural dynamics for landmark orientation and angular path integration. Nature 521: 186-91
117. Si B, Kropff E, Treves A. 2012. Grid alignment in entorhinal cortex. Biol. Cybern. 106: 483-506
118. Si B, Treves A. 2013. A model for the differentiation between grid and conjunctive units in medial entorhinal cortex. Hippocampus 23: 1410-24
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
120. Smith SL, Smith IT, Branco T, Hausser M. 2013. Dendritic spikes enhance stimulus selectivity in cortical neurons in vivo. Nature 503: 115-20
121. Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI. 2008. Representation of geometric borders in the entorhinal cortex. Science 322: 1865-68
122. Solstad T, Moser EI, Einevoll GT. 2006. From grid cells to place cells: A mathematical model. Hippocampus 16: 1026-31
123. Sreenivasan S, Fiete I. 2011. Grid cells generate an analog error-correcting code for singularly precise neural computation. Nat. Neurosci. 14: 1330-37
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
125. Stella F, Treves A. 2015. The self-organization of grid cells in 3D. eLife 4: e05913
126. Stemmler M, Mathis A, Herz AV. 2015. Connecting multiple spatial scales to decode the population activity of grid cells. Sci. Adv. 1: e1500816
127. Stensola H, Stensola T, Solstad T, Froland K, Moser MB, Moser EI. 2012. The entorhinal grid map is discretized. Nature 492: 72-78
128. Stensola T, Stensola H, Moser MB, Moser EI. 2015. Shearing-induced asymmetry in entorhinal grid cells. Nature 518: 207-12
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
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
131. Tang Q, Burgalossi A, Ebbesen CL, Sanguinetti-Scheck JI, Schmidt H, et al. 2016. Functional architecture of the rat parasubiculum. J. Neurosci. 36(7): 2289-301
132. Taube JS, Muller RU, Ranck JB Jr. 1990. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10: 420-35
133. Taube JS, Muller RU, Ranck JB Jr. 1990. Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J. Neurosci. 10: 436-47
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
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
136. Tsao A, Moser MB, Moser EI. 2013. Traces of experience in the lateral entorhinal cortex. Curr. Biol. 23: 399-405
137. Turing AM. 1952. The chemical basis of morphogenesis. Philos. Trans. R. Soc. 237: 37-72
138. UlanovskyN. 2011. Neuroscience: How is three-dimensional space encoded in the brain? Curr. Biol. 21: R886-88
139. Urdapilleta E, Troiani F, Stella F, Treves A. 2015. Can rodents conceive hyperbolic spaces J. R. Soc. Interface 12: 20141214
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
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
142. Wei XX, Prentice J, Balasubramanian V. 2015. A principle of economy predicts the functional architecture of grid cells. eLife 4: e08362
143. Wernle T, MørreaunetM, 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
145. Wills TJ, Cacucci F, BurgessN, O'Keefe J. 2010. Development of the hippocampal cognitive map in preweanling rats. Science 328: 1573-76
146. Wilson MA, McNaughton BL. 1993. Dynamics of the hippocampal ensemble code for space. Science 261: 1055-58
147. Yartsev MM, Ulanovsky N. 2013. Representation of three-dimensional space in the hippocampus of flying bats. Science 340: 367-72
148. Yartsev MM, WitterMP, Ulanovsky N. 2011. Grid cells without theta oscillations in the entorhinal cortex of bats. Nature 479: 103-7
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
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
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
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
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
155. Zhang SJ, Ye J, Miao C, Tsao A, Cerniauskas I, et al. 2013. Optogenetic dissection of entorhinal-hippocampal functional connectivity. Science 340: 1232627