Space in the brain: How the hippocampal formation supports spatial cognition

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1635, 2014, Pages

  Hartley, Tom ^a   Lever, Colin ^b   Burgess, Neil ^c   O'Keefe, John ^d  

^a UNIVERSITY OF YORK   (United Kingdom)

^b DURHAM UNIVERSITY   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Boundary cells; Entorhinal cortex; Grid cells; Head direction cells; Hippocampus; Place cells

Indexed keywords

ANIMAL; BRAIN; GENETIC ENGINEERING; NUMERICAL MODEL; PARAMETERIZATION; SPATIAL COGNITION;

ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; BOUNDARY CELLS; COGNITION; COMPUTER SIMULATION; CYTOLOGY; DEPTH PERCEPTION; ENTORHINAL CORTEX; GRID CELLS; HEAD DIRECTION CELLS; HIPPOCAMPUS; HISTOLOGY; HUMAN; MOUSE; NERVE CELL; PHYSIOLOGY; PLACE CELLS; RAT; REVIEW; THETA RHYTHM;

BOUNDARY CELLS; ENTORHINAL CORTEX; GRID CELLS; HEAD DIRECTION CELLS; HIPPOCAMPUS; PLACE CELLS;

ACTION POTENTIALS; ANIMALS; COGNITION; COMPUTER SIMULATION; HIPPOCAMPUS; HUMANS; MICE; MODELS, NEUROLOGICAL; NEURONS; RATS; SPACE PERCEPTION; THETA RHYTHM;

EID: 84897370672     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0510     Document Type: Review

References (216)

1. Hubel DH, Wiesel TN. 1962 Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. 160, 106-154.
2. Kaas JH, Nelson RJ, Sur M, Lin C-S, Merzenich MM. 1979 Multiple representations of the body within the primary somatosensory cortex of primates. Science 204, 521-523. (doi:10.1126/science. 107591)
3. Georgopoulos AP, Schwartz AB, Kettner RE. 1986 Neuronal population coding of movement direction. Science 233, 1416-1419. (doi:10.1126/science. 3749885)
4. Colby CL. 1998 Action-oriented spatial reference frames in cortex. Neuron 20, 15-24. (doi:10.1016/ S0896-6273(00)80429-8)
5. Andersen RA. 1997 Multimodal integration for the representation of space in the posterior parietal cortex. Phil. Trans. R. Soc. Lond. B 352, 1421-1428. (doi:10.1098/rstb.1997.0128)
6. Burgess N, Jeffery KJ, O'Keefe J. 1999 Intergrating hippocampal and parietal functions: a spatial point of view. In The hippocampal and parietal foundations of spatial cognition (eds N Burgess, KJ Jeffery, J O'Keefe), pp. 3-29. Oxford, UK: Oxford University Press.
7. Milner AD, Goodale MA. 1995 The visual brain in action. New York, NY: Oxford University Press.
8. Salinas E, Abbott L. 1996 A model of multiplicative neural responses in parietal cortex. Proc. Natl Acad. Sci. USA 93, 11 956-11 961. (doi:10.1073/pnas.93. 21.11956)
9. Pouget A, Deneve S, Duhamel J-R. 2002 A computational perspective on the neural basis of multisensory spatial representations. Nat. Rev. Neurosci. 3, 741-747. (doi:10.1038/nrn914)
10. Tolman EC. 1948 Cognitive maps in rats and men. Psychol. Rev. 55, 189-208. (doi:10.1037/h0061626)
11. O'Keefe J, Nadel L. 1978 The hippocampus as a cognitive map. Oxford, UK: Oxford University Press.
12. Burgess N, Becker S, King JA, O'Keefe J. 2001 Memory for events and their spatial context: models and experiments. Phil. Trans. R. Soc. Lond. B 356, 1493-1503. (doi:10.1098/rstb.2001.0948)
13. Milner AD, Dijkerman HC, Carey DP. 1999 Visuospatial processing in a case of visual form agnosia. In The hippocampal and parietal foundations of spatial cognition (eds N Burgess, KJ Jeffery, J O'Keefe), pp. 443-466. Oxford, UK: Oxford University Press.
14. Marr D. 1971 Simple memory: a theory for archicortex. Phil. Trans. R. Soc. Lond. B 262, 23-81. (doi:10.1098/rstb.1971.0078)
15. Doherty A. 1999 MRC Centre for Synaptic Plasticity, University of Bristol available at http://www.bristol. ac.uk/synaptic/pathways/ (accessed 27 August 2013).
16. Cajal SRY. 1955 Histologie du systeme nerveux de l'homme & des vertebres. Consejo Superior de Investigaciones Cientificas, Instituto Ramon y Cajal.
17. Bliss TV, Lomo T. 1973 Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232, 331-356.
18. Gardner-Medwin AR. 1976 The recall of events through the learning of associations between their parts. Proc. R. Soc. Lond. B 194, 375-402. (doi:10.1098/rspb.1976.0084)
19. Andersen P, Morris R, Amaral D, Bliss T, O'Keefe J. 2006 The hippocampus book. Oxford, UK: Oxford University Press.
20. Witter MP, Canto CB, Couey JJ, Koganezawa N, O'Reilly KC. 2014 Architecture of spatial circuits in the hippocampal region. Phil. Trans. R. Soc. B 369, 20120515. (doi:10.1098/rstb.2012.0515)
21. Taube JS. 1998 Head direction cells and the neuropsychological basis for a sense of direction. Prog. Neurobiol. 55, 225-256. (doi:10.1016/S0301-0082(98)00004-5)
22. Luo AH, Tahsili-Fahadan P, Wise RA, Lupica CR, Aston-Jones G. 2013 Linking context with reward: a functional circuit from hippocampal CA3 to ventral tegmental area. Science 333, 353-357. (doi:10. 1126/science.1204622)
23. Vanderwolf CH. 1969 Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26, 407-418. (doi:10.1016/0013-4694(69)90092-3)
24. Jeewajee A, Lever C, Burton S, O'Keefe J, Burgess N. 2008 Environmental novelty is signaled by reduction of the hippocampal theta frequency. Hippocampus 18, 340-348. (doi:10.1002/hipo.20394)
25. Hasselmo ME, Bodelon C, Wyble BP. 2002 A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput. 14, 793-817. (doi:10.1162/089976602317318965)
26. Easton A, Douchamps V, Eacott M, Lever C. 2012 A specific role for septohippocampal acetylcholine in memory? Neuropsychologia 50, 3156-3168. (doi:10.1016/j.neuropsychologia.2012.07.022)
27. Douchamps V, Jeewajee A, Blundell P, Burgess N, Lever C. 2013 Evidence for encoding versus retrieval scheduling in the hippocampus by theta phase and acetylcholine. J. Neurosci. 33, 8689-8704. (doi:10. 1523/JNEUROSCI.4483-12.2013)
28. O'Keefe J, Recce ML. 1993 Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317-330. (doi:10.1002/hipo.450030307)
29. Burgess N, O'Keefe J. 2011 Models of place and grid cell firing and theta rhythmicity. Curr. Opin. Neurobiol. 21, 734-744. (doi:10.1016/j.conb.2011. 07.002)
30. Rivas J, Gaztelu J, Garcia-Austt E. 1996 Changes in hippocampal cell discharge patterns and theta rhythm spectral properties as a function of walking velocity in the guinea pig. Exp. Brain Res. 108, 113-118. (doi:10.1007/ BF00242908)
31. Slawinska U, Kasicki S. 1998 The frequency of rat's hippocampal theta rhythm is related to the speed of locomotion. Brain Res. 796, 327-331. (doi:10. 1016/S0006-8993(98)00390-4)
32. Lever C, Jeewajee A, Burton S, O'Keefe J, Burgess N. 2009 Hippocampal theta frequency, novelty, and behavior. Hippocampus 19, 409-410. (doi:10.1002/ hipo.20557)
33. Hinman JR, Penley SC, Long LL, Escabi MA, Chrobak JJ. 2011 Septotemporal variation in dynamics of theta: speed and habituation. J. Neurophysiol. 105, 2675-2686. (doi:10.1152/jn.00837.2010)
34. Wells CE, Amos DP, Jeewajee A, Douchamps V, Rodgers J, O'Keefe J, Burgess N, Lever C. 2013 Novelty and anxiolytic drugs dissociate two components of hippocampal theta in behaving rats. J. Neurosci. 33, 8650-8667. (doi:10.1523/ JNEUROSCI.5040-12.2013)
35. McNaughton BL, Barnes CA, O'Keefe J. 1983 The contributions of position, direction, and velocity to single unit activity in the hippocampus of freelymoving rats. Exp. Brain. Res 52, 41-49. (doi:10. 1007/BF00237147)
36. Jeewajee A, Barry C, Douchamps V, Manson D, Lever C, Burgess N. 2014 Theta phase precession of grid and place cell firing in open environments. Phil. Trans. R. Soc. B 369, 20120532. (doi:10.1098/rstb. 2012.0532)
37. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser M-B. 2006 Path integration and the neural basis of the 'cognitive map'. Nat. Rev. Neurosci. 7, 663-678. (doi:10.1038/nrn1932)
38. Burgess N, Barry C, O'Keefe J. 2007 An oscillatory interference model of grid cell firing. Hippocampus 17, 801-812. (doi:10.1002/hipo.20327)
39. Welday AC, Shlifer IG, Bloom ML, Zhang K, Blair HT. 2011 Cosine directional tuning of theta cell burst frequencies: evidence for spatial coding by oscillatory interference. J. Neurosci. 31, 16 157-16 176. (doi:10.1523/JNEUROSCI.0712-11.2011)
40. Burgess N. 2008 Grid cells and theta as oscillatory interference: theory and predictions. Hippocampus 18, 1157-1174. (doi:10.1002/hipo.20518)
41. Blair HT, Wu A, Cong J. 2014 Oscillatory neurocomputing with ring attractors: a network architecture for mapping locations in space onto patterns of neural synchrony. Phil. Trans. R. Soc. B 369, 20120526. (doi:10.1098/ rstb.2012.0526)
42. Hasselmo ME. 2014 Neuronal rebound spiking, resonance frequency and theta cycle skipping may contribute to grid cell firing in medial entorhinal cortex. Phil. Trans. R. Soc. B 369, 20120523. (doi:10.1098/rstb.2012.0523)
43. Moser EI, Moser M-B, Roudi Y. 2014 Network mechanisms of grid cells. Phil. Trans. R. Soc. B 369, 20120511. (doi:10.1098/rstb.2012.0511)
44. Jacobs J. 2014 Hippocampal theta oscillations are slower in humans than in rodents: implications for models of spatial navigation and memory. Phil. Trans. R. Soc. B 369, 20130304. (doi:10.1098/rstb. 2013.0304)
45. Heys JG, MacLeod KM, Moss CF, Hasselmo ME. 2013 Bat and rat neurons differ in theta-frequency resonance despite similar coding of space. Science 340, 363-367. (doi:10.1126/science.1233831)
46. Barry C, Doeller CF. 2013 3D mapping in the brain. Science 340, 279-280. (doi:10.1126/science. 1237569)
47. Buzsaki G. 2002 Theta oscillations in the hippocampus. Neuron 33, 325-340. (doi:10.1016/ S0896-6273(02)00586-X)
48. Buzsaki G. 2009 Rhythms of the brain. Oxford, UK: Oxford University Press.
49. Somogyi P, Katona L, Klausberger T, Lasztóczi B, Viney TJ. 2014 Temporal redistribution of inhibition over neuronal subcellular domains underlies statedependent rhythmic change of excitability in the hippocampus. Phil. Trans. R. Soc. B 369, 20120518. (doi:10.1098/rstb.2012.0518)
50. Mizuseki K, Buzsaki G. 2014 Theta oscillations decrease spike synchrony in the hippocampus and entorhinal cortex. Phil. Trans. R. Soc. B 369, 20120530. (doi:10.1098/rstb.2012.0530)
51. Manns JR, Zilli EA, Ong KC, Hasselmo ME, Eichenbaum H. 2007 Hippocampal CA1 spiking during encoding and retrieval: relation to theta phase. Neurobiol. Learn. Mem. 87, 9-20. (doi:10.1016/j.nlm.2006.05.007)
52. Jezek K, Henriksen EJ, Treves A, Moser EI, Moser M-B. 2011 Theta-paced flickering between place-cell maps in the hippocampus. Nature 478, 246-249. (doi:10.1038/nature10439)
53. Hartley T, Burgess N, Lever C, Cacucci F, O'Keefe J. 2000 Modeling place fields in terms of the cortical inputs to the hippocampus. Hippocampus 10, 369-379. (doi:10.1002/1098-1063(2000)10: 4,369::AID-HIPO3.3.0.CO;2-0)
54. 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, 171-175. (doi:10.1016/0006-8993(71)90358-1)
55. 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, 7347-7356.
56. Kjelstrup KB, Solstad T, Brun VH, Hafting T, Leutgeb S, Witter MP, Moser EI, Moser M-B. 2008 Finite scale of spatial representation in the hippocampus. Science 321, 140-143. (doi:10.1126/science. 1157086)
57. Muller RU, Kubie JL. 1987 The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 7, 1951-1968.
58. Bostock E, Muller RU, Kubie JL. 1991 Experiencedependent modifications of hippocampal place cell firing. Hippocampus 1, 193-205. (doi:10.1002/hipo. 450010207)
59. Sharp PE. 1997 Subicular cells generate similar spatial firing patterns in two geometrically and visually distinctive environments: comparison with hippocampal place cells. Behav. Brain Res. 85, 71-92. (doi:10.1016/S0166-4328(96) 00165-9)
60. Kentros C, Hargreaves E, Hawkins RD, Kandel ER, Shapiro M, Muller RV. 1998 Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science 280, 2121-2126. (doi:10.1126/science.280.5372.2121)
61. Lever C, Wills T, Cacucci F, Burgess N, O'Keefe J. 2002 Long-term plasticity in the hippocampal place cell representation of environmental geometry. Nature 416, 90-94. (doi:10.1038/416090a)
62. Knierim JJ. 2002 Dynamic interactions between local surface cues, distal landmarks, and intrinsic circuitry in hippocampal place cells. J. Neurosci. 22, 6254-6264.
63. Leutgeb S, Leutgeb JK, Treves A, Moser MB, Moser EI. 2004 Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305, 1295-1298. (doi:10.1126/science.1100265)
64. Wilson MA, McNaughton BL. 1993 Dynamics of the hippocampal ensemble code for space. Science 261, 1055-1058. (doi:10.1126/science.8351520)
65. Zhang K, Ginzburg I, McNaughton BL, Sejnowski TJ. 1998 Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. J. Neurophysiol. 79, 1017-1044.
66. O'Keefe J, Conway DH. 1978 Hippocampal place units in the freely moving rat: why they fire where they fire. Exp. Brain Res. 31, 573-590. (doi:10. 1007/BF00239813)
67. Muller RU, Bostock E, Taube JS, Kubie JL. 1994 On the directional firing properties of hippocampal place cells. J. Neurosci. 14, 7235-7251.
68. Anderson MI, Jeffery KJ. 2003 Heterogeneous modulation of place cell firing by changes in context. J. Neurosci. 23, 8827-8835.
69. Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, Moser M-B. 2005 Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309, 619-623. (doi:10.1126/science.1114037)
70. Huxter J, Burgess N, O'Keefe J. 2003 Nature 425, 828-832.
71. Hafting T, Fyhn M, Bonnevie T, Moser M-B, Moser EI. 2008 Hippocampus-independent phase precession in entorhinal grid cells. Nature 453, 1248-1252. (doi:10.1038/nature06957)
72. Dragoi G, Buzsaki G. 2006 Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 50, 145-157. (doi:10.1016/j.neuron.2006. 02.023)
73. Burgess N, Recce M, O'Keefe J. 1994 A model of hippocampal function. Neural Netw. 7, 1065-1081. (doi:10.1016/S0893-6080(05)80159-5)
74. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA. 1996 Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6, 149-172. (doi:10.1002/(SICI)1098-1063(1996)6:2,149::AIDHIPO6.3.0. CO;2-K)
75. Taube JS, Muller RU, Ranck Jr JB. 1990 Headdirection cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10, 420-435.
76. Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser M-B, Moser EI. 2006 Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312, 758-762. (doi:10. 1126/science.1125572)
77. Taube JS. 2007 The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 30, 181-207. (doi:10.1146/annurev.neuro.29. 051605.112854)
78. Zhang K. 1996 Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J. Neurosci. 16, 2112-2126.
79. Johnson A, Seeland K, Redish AD. 2005 Reconstruction of the postsubiculum head direction signal from neural ensembles. Hippocampus 15, 86-96. (doi:10.1002/hipo.20033)
80. Calton JL, Stackman RW, Goodridge JP, Archey WB, Dudchenko PA, Taube JS. 2003 Hippocampal place cell instability after lesions of the head direction cell network. J. Neurosci. 23, 9719-9731.
81. Burgess N, Cacucci F, Lever C, O'Keefe J. 2004 Characterizing multiple independent behavioral correlates of cell firing in freely moving animals. Hippocampus 15, 149-153. (doi:10.1002/ hipo.20058)
82. Knierim JJ, Kudrimoti HS, McNaughton BL. 1998 Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. J. Neurophysiol. 80, 425-446.
83. Jeffery KJ. 1998 Learning of landmark stability and instability by hippocampal place cells. Neuropharmacology 37, 677-687. (doi:10.1016/ S0028-3908(98)00053-7)
84. Zugaro MLB, Arleo A, Berthoz A, Wiener SI. 2003 Rapid spatial reorientation and head direction cells. J. Neurosci. 23, 3478-3482.
85. McNaughton BL et al. 1996 Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J. Exp. Biol. 199, 173-185.
86. Cressant A, Muller RU, Poucet B. 1997 Failure of centrally placed objects to control the firing fields of hippocampal place cells. J. Neurosci. 17, 2531-2542.
87. Jeffery KJ, Donnett JG, Burgess N, O'Keefe J. 1997 Directional control of hippocampal place fields. Exp. Brain Res. 117, 131-142. (doi:10.1007/ s002210050206)
88. Knight R, Piette CE, Page H, Walters D, Marozzi E, Nardini M, Stringer S, Jeffery KJ. 2014 Weighted cue integration in the rodent head direction system. Phil. Trans. R. Soc. B 369, 20120512. (doi:10.1098/ rstb.2012.0512)
89. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. 2005 Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801-806. (doi:10. 1038/nature03721)
90. Boccara CN, Sargolini F, Thoresen VH, Solstad T, Witter MP, Moser EI, Moser M-B. 2010 Grid cells in pre-and parasubiculum. Nat. Neurosci. 13, 987-994. (doi:10.1038/nn.2602)
91. Fyhn M, Hafting T, Witter MP, Moser EI, Moser MB. 2008 Grid cells in mice. Hippocampus 18, 1230-1238. (doi:10.1002/hipo.20472)
92. Giocomo LM, Hasselmo ME. 2008 Time constants of h current in layer II stellate cells differ along the dorsal to ventral axis of medial entorhinal cortex. J. Neurosci. 28, 9414-9425. (doi:10.1523/ JNEUROSCI.3196-08.2008)
93. Giocomo LM, Hussaini SA, Zheng F, Kandel ER, Moser M-B, Moser EI. 2011 Grid cells use HCN1 channels for spatial scaling. Cell 147, 1159-1170. (doi:10.1016/j.cell.2011.08.051)
94. Barry C, Hayman R, Burgess N, Jeffery K. 2007 Experience-dependent rescaling of entorhinal grids. Nat. Neurosci. 10, 682-684. (doi:10.1038/nn1905)
95. Fiete IR, Burak Y, Brookings T. 2008 What grid cells convey about rat location. J. Neurosci. 28, 6858-6871. (doi:10.1523/JNEUROSCI.5684-07.2008)
96. Gorchetchnikov A, Grossberg S. 2007 Space, time and learning in the hippocampus: how fine spatial and temporal scales are expanded into population codes for behavioral control. Neural Netw. 20, 182-193. (doi:10.1016/j.neunet.2006.11.007)
97. Towse BW, Barry C, Bush D, Burgess N. 2014 Optimal configurations of spatial scale for grid cell firing under noise and uncertainty. Phil. Trans. R. Soc. B 369, 20130290. (doi:10.1098/ rstb.2013.0290)
98. Stensola H, Stensola T, Solstad T, Froland K, Moser M-B, Moser EI. 2012 The entorhinal grid map is discretized. Nature 492, 72-78. (doi:10.1038/ nature11649)
99. Schmidt-Hieber C, Häusser M. 2014 How to build a grid cell. Phil. Trans. R. Soc. B 369, 20120520. (doi:10.1098/rstb.2012.0520)
100. Barry C, Ginzberg LL, O'Keefe J, Burgess N. 2012 Grid cell firing patterns signal environmental novelty by expansion. Proc. Natl Acad. Sci. USA 109, 17 687-17 692. (doi:10.1073/pnas.1209918109)
101. Poucet B, Sargolini F, Song EY, Hangya B, Fox S, Muller RU. 2014 Independence of landmark and self-motion-guided navigation: a different role for grid cells. Phil. Trans. R. Soc. B 369, 20130370. (doi:10.1098/rstb.2013.0370)
102. O'Keefe J, Burgess N. 1996 Geometric determinants of the place fields of hippocampal neurons. Nature 381, 425-428. (doi:10.1038/381425a0)
103. Muller RU, Kubie JL, Ranck Jr JB. 1987 Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J. Neurosci. 7, 1935-1950.
104. Burgess N, Jackson A, Hartley T, O'Keefe J. 2000 Predictions derived from modelling the hippocampal role in navigation. Biol. Cybern. 83, 301-312. (doi:10.1007/s004220000172)
105. Lever C, Burgess N, Cacucci F, Hartley T, O'Keefe J. 2002 What can the hippocampal representation of environmental geometry tell us about Hebbian learning? Biol. Cybern. 87, 356-372. (doi:10.1007/ s00422-002-0360-z)
106. Barry C, Lever C, Hayman R, Hartley T, Burton S, O'Keefe J, Jeffery K, Burgess N. 2006 The boundary vector cell model of place cell firing and spatial memory. Rev. Neurosci. 17, 71-97. (doi:10.1515/ REVNEURO.2006.17.1-2.71)
107. Lever C, Burton S, Jeewajee A, O'Keefe J, Burgess N. 2009 Boundary vector cells in the subiculum of the hippocampal formation. J. Neurosci. 29, 9771-9777. (doi:10.1523/JNEUROSCI. 1319-09.2009)
108. Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI. 2008 Representation of geometric borders in the entorhinal cortex. Science 322, 1865-1868. (doi:10.1126/science.1166466)
109. Savelli F, Yoganarasimha D, Knierim JJ. 2008 Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18, 1270-1282. (doi:10.1002/ hipo.20511)
110. Stewart S, Jeewajee A, Wills TJ, Burgess N, Lever C. 2014 Boundary coding in the rat subiculum. Phil. Trans. R. Soc. B 369, 20120514. (doi:10.1098/ rstb.2012.0514)
111. Krupic J, Bauza M, Burton S, Lever C, O'Keefe J. 2014 How environment geometry affects grid cell symmetry and what we can learn from it. Phil. Trans. R. Soc. B 369, 20130188. (doi:10.1098/ rstb.2013.0188)
112. Derdikman D, Whitlock JR, Tsao A, Fyhn M, Hafting T, Moser M-B, Moser EI. 2009 Fragmentation of grid cell maps in a multicompartment environment. Nat. Neurosci. 12, 1325-1332. (doi:10.1038/nn.2396)
113. Doeller CF, Burgess N. 2008 Distinct error-correcting and incidental learning of location relative to landmarks and boundaries. Proc. Natl Acad. Sci. USA 105, 5909-5914. (doi:10.1073/pnas.0711433105)
114. Doeller CF, King JA, Burgess N. 2008 Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory. Proc. Natl Acad. Sci. USA 105, 5915-5920. (doi:10.1073/pnas. 0801489105)
115. Bird CM, Capponi C, King JA, Doeller CF, Burgess N. 2010 Establishing the boundaries: the hippocampal contribution to imagining scenes. J. Neurosci. 30, 11 688-11 695. (doi:10.1523/JNEUROSCI.0723-10. 2010)
116. Horne MR, Iordanova MD, Pearce JM. 2010 Spatial learning based on boundaries in rats is hippocampus-dependent and prone to overshadowing. Behav. Neurosci. 124, 623-632. (doi:10.1037/a0020824)
117. Lee SA, Spelke ES. 2010 Two systems of spatial representation underlying navigation. Exp. Brain Res. 206, 179-188. (doi:10.1007/s00221-010-2349-5)
118. Cheng K, Newcombe NS. 2005 Is there a geometric module for spatial orientation? Squaring theory and evidence. Psychon. Bull. Rev. 12, 1-23. (doi:10. 3758/BF03196346)
119. Mhatre H, Gorchetchnikov A, Grossberg S. 2012 Grid cell hexagonal patterns formed by fast selforganized learning within entorhinal cortex. Hippocampus 22, 320-334. (doi:10.1002/ hipo.20901)
120. Hasselmo ME, Brandon MP. 2012 A model combining oscillations and attractor dynamics for generation of grid cell firing. Front. Neural Circuits 6, 30. (doi:10.3389/fncir.2012.00030)
121. Krupic J, Burgess N, O'Keefe J. 2012 Neural representations of location composed of spatially periodic bands. Science 337, 853-857. (doi:10. 1126/science.1222403)
122. Cacucci F, Lever C, Burgess N, O'Keefe J. 2000 Topodirectional cells in the hippocampal formation of the rat. Eur. J. Neurosci. 12, 86.
123. MacDonald CJ, Lepage KQ, Eden UT, Eichenbaum H. 2011 Hippocampal 'time cells' bridge the gap in memory for discontiguous events. Neuron 71, 737-749. (doi:10.1016/j.neuron.2011.07.012)
124. Kraus BJ, Robinson II RJ, White JA, Eichenbaum H, Hasselmo ME. 2013 Hippocampal 'time cells': time versus path integration. Neuron 78, 1090-1101. (doi:10.1016/j.neuron.2013.04.015)
125. Knierim JJ, Neunuebel JP, Deshmukh SS. 2014 Functional correlates of the lateral and medial entorhinal cortex: objects, path integration and local-global reference frames. Phil. Trans. R. Soc. B 369, 20130369. (doi:10.1098/rstb.2013.0369)
126. Tsao A, Moser M-B, Moser EI. 2013 Traces of experience in the lateral entorhinal cortex. Curr. Biol. 23, 399-405. (doi:10.1016/j.cub.2013.01.036)
127. Deshmukh SS, Knierim JJ. 2011 Representation of non-spatial and spatial information in the lateral entorhinal cortex. Front. Behav. Neurosci. 5, 69. (doi:10.3389/fnbeh.2011.00069)
128. Wilson MA, McNaughton BL. 1994 Reactivation of hippocampal ensemble memories during sleep. Science 265, 676-679. (doi:10.1126/science. 8036517)
129. Skaggs WE, McNaughton BL. 1996 Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271, 1870-1873. (doi:10.1126/science.271. 5257.1870)
130. Nadasdy Z, Hirase H, Czurko A, Csicsvari J, Buzsaki G. 1999 Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci. 19, 9497-9507.
131. Lee AK, Wilson MA. 2002 Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36, 1183-1194. (doi:10.1016/S0896-6273(02)01096-6)
132. Foster DJ, Wilson MA. 2006 Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440, 680-683. (doi:10.1038/nature04587)
133. O'Neill J, Pleydell-Bouverie B, Dupret D, Csicsvari J. 2010 Play it again: reactivation of waking experience and memory. Trends Neurosci. 33, 220-229. (doi:10.1016/j.tins.2010.01.006)
134. Girardeau G, Zugaro M. 2011 Hippocampal ripples and memory consolidation. Curr. Opin. Neurobiol. 21, 452-459. (doi:10.1016/j.conb.2011.02.005)
135. Csicsvari J, Dupret D. 2014 Sharp wave/ripple network oscillations and learning-associated hippocampal maps. Phil. Trans. R. Soc. B 369, 20120528. (doi:10.1098/rstb.2012.0528)
136. Pfeiffer BE, Foster DJ. 2013 Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497, 74-79. (doi:10. 1038/nature12112)
137. Dragoi G, Tonegawa S. 2014 Selection of preconfigured cell assemblies for representation of novel spatial experiences. Phil. Trans. R. Soc. B 369, 20120522. (doi:10.1098/rstb.2012.0522)
138. Dragoi G, Tonegawa S. 2011 Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 469, 397-401. (doi:10.1038/ nature09633)
139. Dragoi G, Tonegawa S. 2013 Distinct preplay of multiple novel spatial experiences in the rat. Proc. Natl Acad. Sci. USA 110, 9100-9105. (doi:10.1073/ pnas.1306031110)
140. Diba K, Buzsaki G. 2007 Forward and reverse hippocampal place-cell sequences during ripples. Nat. Neurosci. 10, 1241-1242. (doi:10.1038/ nn1961)
141. Buckner RL. 2010 The role of the hippocampus in prediction and imagination. Annu Rev. Psychol. 61, 27-34. (doi:10.1146/annurev.psych.60.110707. 163508)
142. Solstad T, Moser EI, Einevoll GT. 2006 From grid cells to place cells: a mathematical model. Hippocampus 16, 1026-1031. (doi:10.1002/ hipo.20244)
143. Rolls ET, Stringer SM, Elliot T. 2006 Entorhinal cortex grid cells can map to hippocampal place cells by competitive learning. Netw. Comput. Neural Syst. 17, 447-465. (doi:10.1080/0954898060 1064846)
144. Zhang S-J, Ye J, Couey JJ, Witter M, Moser EI, Moser M-B. 2014 Functional connectivity of the entorhinal-hippocampal space circuit. Phil. Trans. R. Soc. B 369, 20120516. (doi:10.1098/ rstb.2012.0516)
145. Zhang S-J, Ye J, Miao C, Tsao A, Cerniauskas I, Ledergerber D, Moser M-B, Moser EI. 2013 Optogenetic dissection of entorhinal-hippocampal functional connectivity. Science 340, 1232627. (doi:10.1126/science.1232627)
146. Langston RF, Ainge JA, Couey JJ, Canto CB, Bjerknes TL, Witter MP, Moser EI, Moser M-B. 2010 Development of the spatial representation system in the rat. Science 328, 1576-1580. (doi:10.1126/ science.1188210)
147. Wills TJ, Cacucci F, Burgess N, O'Keefe J. 2010 Development of the hippocampal cognitive map in preweanling rats. Science 328, 1573-1576. (doi:10. 1126/science.1188224)
148. Wills TJ, Muessig L, Cacucci F. 2014 The development of spatial behaviour and the hippocampal neural representation of space. Phil. Trans. R. Soc. B 369, 20130409. (doi:10.1098/rstb. 2013.0409)
149. Koenig J, Linder AN, Leutgeb JK, Leutgeb S. 2011 The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science 332, 592-595. (doi:10.1126/science.1201685)
150. Bonnevie T, Dunn B, Fyhn M, Hafting T, Derdikman D, Kubie JL, Roudi Y, Moser EI, Moser M-B. 2013 Grid cells require excitatory drive from the hippocampus. Nat. Neurosci. 16, 309-317. (doi:10.1038/nn.3311)
151. O'Keefe J, Burgess N. 2005 Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells. Hippocampus 15, 853-866. (doi:10.1002/ hipo.20115)
152. Zilli EA. 2012 Models of grid cell spatial firing published 2005-2011. Front. Neural Circuits 6, 16. (doi:10.3389/fncir.2012.00016)
153. Page HJI, Walters DM, Knight R, Piette CE, Jeffery KJ, Stringer SM. 2014 A theoretical account of cue averaging in the rodent head direction system. Phil. Trans. R. Soc. B 369, 20130283. (doi:10.1098/rstb.2013.0283)
154. Rotenberg A, Muller RU. 1997 Variable place-cell coupling to a continuously viewed stimulus: evidence that the hippocampus acts as a perceptual system. Phil. Trans. R. Soc. Lond. B 352, 1505-1513. (doi:10.1098/rstb.1997.0137)
155. Samsonovich A, McNaughton BL. 1997 Path integration and cognitive mapping in a continuous attractor neural network model. J. Neurosci. 17, 5900-5920.
156. Conklin J, Eliasmith C. 2005 A controlled attractor network model of path integration in the rat. J. Comput. Neurosci. 18, 183-203. (doi:10.1007/ s10827-005-6558-z)
157. Fuhs MC, Touretzky DS. 2006 A spin glass model of path integration in rat medial entorhinal cortex. J. Neurosci. 26, 4266-4276. (doi:10.1523/ JNEUROSCI.4353-05.2006)
158. Guanella A, Verschure PF. 2006 A model of grid cells based on a path integration mechanism. In Artificial Neural Networks-ICANN 2006, Part I, LNCS4131 (eds S Kollias, A Stafylopatis, W Duch, E Oja), pp. 740-749. Berlin, Germany: Springer.
159. Turing AM. 1990 The chemical basis of morphogenesis. Bull. Math. Biol. 52, 153-197. (doi:10.1007/BF02459572)
160. Fenton AA, Kao H-Y, Neymotin SA, Olypher A, Vayntrub Y, Lytton WW, Ludvig N. 2008 Unmasking the CA1 ensemble place code by exposures to small and large environments: more place cells and multiple, irregularly arranged, and expanded place fields in the larger space. J. Neurosci. 28, 11 250-11 262. (doi:10.1523/JNEUROSCI.2862-08.2008)
161. Harvey CD, Collman F, Dombeck DA, Tank DW. 2009 Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461, 941-946. (doi:10.1038/nature08499)
162. Chorev E, Epsztein J, Houweling AR, Lee AK, Brecht M. 2009 Electrophysiological recordings from behaving animals-going beyond spikes. Curr. Opin. Neurobiol. 19, 513-519. (doi:10.1016/j.conb. 2009.08.005)
163. Domnisoru C, Kinkhabwala AA, Tank DW. 2013 Membrane potential dynamics of grid cells. Nature 495, 199-204. (doi:10.1038/nature11973)
164. Schmidt-Hieber C, Hausser M. 2013 Cellular mechanisms of spatial navigation in the medial entorhinal cortex. Nat. Neurosci. 16, 325-331. (doi:10.1038/nn.3340)
165. Jacobs J et al. 2013 Direct recordings of grid-like neuronal activity in human spatial navigation. Nat. Neurosci. 16, 1188-1190. (doi:10.1038/nn.3466)
166. Watrous AJ, Lee DJ, Izadi A, Gurkoff GG, Shahlaie K, Ekstrom AD. 2013 A comparative study of human and rat hippocampal low-frequency oscillations during spatial navigation. Hippocampus 23, 656-661. (doi:10.1002/hipo.22124)
167. Grossberg S, Pilly PK. 2014 Coordinated learning of grid cell and place cell spatial and temporal properties: multiple scales, attention and oscillations. Phil. Trans. R. Soc. B 369, 20120524. (doi:10.1098/rstb.2012.0524)
168. Brecht M, Ray S, Burgalossi A, Tang Q, Schmidt H, Naumann R. 2014 An isomorphic mapping hypothesis of the grid representation. Phil. Trans. R. Soc. B 369, 20120521. (doi:10.1098/rstb. 2012.0521)
169. Burak Y, Fiete IR. 2009 Accurate path integration in continuous attractor network models of grid cells. PLoS Comput. Biol. 5, e1000291. (doi:10.1371/ journal.pcbi.1000291)
170. Lapray D et al. 2012 Behavior-dependent specialization of identified hippocampal interneurons. Nat. Neurosci. 15, 1265-1271. (doi:10.1038/nn.3176)
171. Epsztein J, Brecht M, Lee AK. 2011 Intracellular determinants of hippocampal CA1 place and silent cell activity in a novel environment. Neuron 70, 109-120. (doi:10.1016/j.neuron.2011.03.006)
172. Holscher C, Schnee A, Dahmen H, Setia L, Mallot HA. 2005 Rats are able to navigate in virtual environments. J. Exp. Biol. 208, 561-569. (doi:10. 1242/jeb.01371)
173. Chen G, King JA, Burgess N, O'Keefe J. 2013 How vision and movement combine in the hippocampal place code. Proc. Natl Acad. Sci. USA 110, 378-383. (doi:10.1073/pnas.1215834110)
174. Dombeck DA, Harvey CD, Tian L, Looger LL, Tank DW. 2010 Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nat. Neurosci. 13, 1433-1440. (doi:10.1038/ nn.2648)
175. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. 2005 Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263-1268. (doi:10.1038/ nn1525)
176. Ramirez S, Liu X, Lin P-A, Suh J, Pignatelli M, Redondo RL, Ryan TJ, Tonegawa S. 2013 Creating a false memory in the hippocampus. Science 341, 387-391. (doi:10.1126/science.1239073)
177. Eacott MJ, Easton A. 2010 Episodic memory in animals: remembering which occasion. Neuropsychologia 48, 2273-2280. (doi:10.1016/j. neuropsychologia.2009.11.002)
178. Hori E, Tabuchi E, Matsumura N, Tamura R, Eifuku S, Endo S, Nishijo H, Ono T. 2003 Representation of place by monkey hippocampal neurons in real and virtual translocation. Hippocampus 13, 190-196. (doi:10.1002/hipo.10062)
179. Robertson RG, Rolls ET, Georges-Francois P, Panzeri S. 1999 Head direction cells in the primate presubiculum. Hippocampus 9, 206-219. (doi:10.1002/ (SICI)1098-1063(1999)9:3,206::AID-HIPO2.3.0. CO;2-H)
180. Killian NJ, Jutras MJ, Buffalo EA. 2012 A map of visual space in the primate entorhinal cortex. Nature 491, 761-764. (doi:10.1038/nature11587)
181. Rolls ET, Robertson RG, Georges-Francois P. 1997 Spatial view cells in the primate hippocampus. Eur. J. Neurosci. 9, 1789-1794. (doi:10.1111/j. 1460-9568.1997.tb01538.x)
182. Yartsev MM, Witter MP, Ulanovsky N. 2011 Grid cells without theta oscillations in the entorhinal cortex of bats. Nature 479, 103-107. (doi:10.1038/ nature10583)
183. Barry C, Bush D, O'Keefe J, Burgess N. 2012 Models of grid cells and theta oscillations. Nature 488, E1. (doi:10.1038/nature11276)
184. Kaplan R, Doeller CF, Barnes GR, Litvak V, Duzel E, Bandettini PA, Burgess N. 2012 Movement-related theta rhythm in humans: coordinating self-directed hippocampal learning. PLoS Biol. 10, e1001267. (doi:10.1371/journal.pbio.1001267)
185. Fox NC, Warrington EK, Stevens JM, Rossor MN. 1996 Atrophy of the hippocampal formation in early familial Alzheimer's disease. A longitudinal MRI study of at-risk members of a family with an amyloid precursor protein 717Val-Gly mutation. Ann. NY Acad. Sci. 777, 226-232. (doi:10.1111/j. 1749-6632.1996.tb34423.x)
186. Scoville WB, Milner B. 1957 Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20, 11-21. (doi:10.1136/jnnp.20.1.11)
187. Spiers HJ, Maguire EA, Burgess N. 2001 Hippocampal amnesia. Neurocase 7, 357-382. (doi:10.1076/neur.7.5.357.16245)
188. Vargha-Khadem F, Gadian DG, Watkins KE, Connelly A, Van Paesschen W, Mishkin M. 1997 Differential effects of early hippocampal pathology on episodic and semantic memory. Science 277, 376-380. (doi:10.1126/science.277.5324.376)
189. Ekstrom AD, Kahana MJ, Caplan JB, Fields TA, Isham EA, Newman EL, Fried I. 2003 Cellular networks underlying human spatial navigation. Nature 425, 184-188. (doi:10.1038/nature01964)
190. King JA, Burgess N, Hartley T, Vargha-Khadem F, O'Keefe J. 2002 The human hippocampus and viewpoint dependence in spatial memory. Hippocampus 12, 811-820. (doi:10.1002/hipo. 10070)
191. Hartley T, Harlow R. 2012 An association between human hippocampal volume and topographical memory in healthy young adults. Front. Hum. Neurosci. 6, 338. (doi:10.3389/fnhum.2012.00338)
192. Habib M, Sirigu A. 1987 Pure topographical disorientation: a definition and anatomical basis. Cortex 23, 73-85. (doi:10.1016/S0010-9452(87) 80020-5)
193. Aguirre GK, D'Esposito M. 1999 Topographical disorientation: a synthesis and taxonomy. Brain 122, 1613-1628. (doi:10.1093/brain/122.9.1613)
194. Epstein RA. 2008 Parahippocampal and retrosplenial contributions to human spatial navigation. Trends Cogn. Sci. 12, 388-396. (doi:10.1016/j.tics.2008. 07.004)
195. Vann SD, Aggleton JP, Maguire EA. 2009 What does the retrosplenial cortex do? Nat. Rev. Neurosci. 10, 792-802. (doi:10.1038/nrn2733)
196. Epstein R, Kanwisher N. 1998 A cortical representation of the local visual environment. Nature 392, 598-601. (doi:10.1038/33402)
197. Hasson U, Nir Y, Levy I, Fuhrmann G, Malach R. 2004 Intersubject synchronization of cortical activity during natural vision. Science 303, 1634-1640. (doi:10.1126/science.1089506)
198. Janzen G, Van Turennout M. 2004 Selective neural representation of objects relevant for navigation. Nat. Neurosci. 7, 673-677. (doi:10.1038/nn1257)
199. Maguire EA, Burgess N, Donnett JG, Frackowiak RS, Frith CD, O'Keefe J. 1998 Knowing where and getting there: a human navigation network. Science 280, 921-924. (doi:10.1126/science.280.5365.921)
200. Hartley T, Maguire EA, Spiers HJ, Burgess N. 2003 The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans. Neuron 37, 877-888. (doi:10.1016/S0896-6273(03)00095-3)
201. Buckner RL, Carroll DC. 2007 Self-projection and the brain. Trends Cogn. Sci. 11, 49-57. (doi:10.1016/j. tics.2006.11.004)
202. Hassabis D, Maguire EA. 2007 Deconstructing episodic memory with construction. Trends Cogn. Sci. 11, 299-306. (doi:10.1016/j.tics. 2007.05.001)
203. Burgess N, Maguire EA, Spiers HJ, O'Keefe J. 2001 A temporoparietal and prefrontal network for retrieving the spatial context of lifelike events. Neuroimage 14, 439-453. (doi:10.1006/nimg.2001. 0806)
204. Byrne P, Becker S, Burgess N. 2007 Remembering the past and imagining the future: a neural model of spatial memory and imagery. Psychol. Rev. 114, 340-375. (doi:10.1037/0033-295X.114.2.340)
205. Schacter DL, Addis DR. 2007 The cognitive neuroscience of constructive memory: remembering the past and imagining the future. Phil. Trans. R. Soc. B 362, 773-786. (doi:10.1098/rstb. 2007.2087)
206. Walther DB, Caddigan E, Fei-Fei L, Beck DM. 2009 Natural scene categories revealed in distributed patterns of activity in the human brain. J. Neurosci. 29, 10 573-10 581. (doi:10.1523/JNEUROSCI.0559-09.2009)
207. Epstein RA, Vass LK. 2014 Neural systems for landmark-based wayfinding in humans. Phil. Trans. R. Soc. B 369, 20120533. (doi:10.1098/rstb.2012. 0533)
208. Doeller CF, Barry C, Burgess N. 2010 Evidence for grid cells in a human memory network. Nature 463, 657-661. (doi:10.1038/nature08704)
209. Jacobs J, Kahana MJ, Ekstrom AD, Mollison MV, Fried I. 2010 A sense of direction in human entorhinal cortex. Proc. Natl Acad. Sci. USA 107, 6487-6492. (doi:10.1073/pnas.0911213107)
210. Oliva A, Torralba A. 2006 Building the gist of a scene: the role of global image features in recognition. Prog. Brain Res. 155, 23-36.
211. Henderson JM, Zhu DC, Larson CL. 2011 Functions of parahippocampal place area and retrosplenial cortex in real-world scene analysis: an fMRI study. Vis. Cogn. 19, 910-927.
212. Kravitz DJ, Peng CS, Baker CI. 2011 Real-world scene representations in high-level visual cortex: it's the spaces more than the places. J. Neurosci. 31, 7322-7333.
213. Vass LK, Epstein RA. 2013 Abstract representations of location and facing direction in the human brain. J. Neurosci. 33, 6133-6142.
214. Amaral D, Witter M. 1989 The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31, 571-591. (doi:10.1016/0306-4522(89)90424-7)
215. Morris RGM, Garrud P, Rawlins JN, O'Keefe J. 1982 Place navigation impaired in rats with hippocampal lesions. Nature 297, 681-683. (doi:10.1038/ 297681a0)
216. Rolls ET, Treves A. 1997 Neural networks and brain function. Oxford, UK: Oxford University Press.