Place cells, grid cells, and memory

Cold Spring Harbor Perspectives in Biology

Volumn 7, Issue 2, 2015, Pages

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

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MODEL; BRAIN MAPPING; HIPPOCAMPUS; HUMAN; NERVE CELL; NERVE CELL NETWORK; PHYSIOLOGY; SPATIAL MEMORY;

BRAIN MAPPING; HIPPOCAMPUS; HUMANS; MODELS, NEUROLOGICAL; NERVE NET; NEURONS; SPATIAL MEMORY;

EID: 84922575894     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a021808     Document Type: Article

References (123)

1. Abbott LF, Blum KI. 1996. Functional significance of long-term potentiation for sequence learning and prediction. Cereb Cortex 6: 406–416.
2. Barnes CA, McNaughton BL, Mizumori SJ, Leonard BW, Lin LH. 1990. Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. Prog Brain Res 83: 287–300.
3. Barry C, Lever C, Hayman R, Hartley T, Burton S, O’Keefe J, Jeffery K, Burgess N. 2006. The boundary vector corpcell model of place cell firing and spatial memory. Rev Neurosci 17: 71–97.
4. Barry C, Hayman R, Burgess N, Jeffery KJ. 2007. Experience-dependent rescaling of entorhinal grids. Nat Neurosci 10: 682–684.
5. Bi GQ, Poo MM. 1998. Synaptic modifications in cultured hippocampal neurons: Dependenceonspike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18: 10464–10472.
6. Bjerknes TL, Moser EI, Moser MB. 2014. Representation of geometric borders in the developing rat. Neuron 82: 71– 78.
7. Blum KI, Abbott LF. 1996. Amodelof spatial map formation in the hippocampus of the rat. Neural Comput 8: 85–93.
8. 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.
9. Bostock E, Muller RU, Kubie JL. 1991. Experience-dependent modifications of hippocampal place cell firing. Hippocampus 1: 193–205.
10. Bragin A, Jandό G, Nádasdy Z, Hetke J, Wise K, Buzsáki G. 1995. Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15: 47–60.
11. Brun VH, Otnass MK, Molden S, Steffenach HA, Witter MP, Moser MB, Moser EI. 2002. Place cells and place recognition maintained by direct entorhinal–hippocampal circuitry. Science 296: 2243–2246.
12. Bush D, Barry C, Burgess N. 2014. What do grid cells contribute to place cell firing? Trends Neurosci 37: 136–145.
13. Buzsáki G. 1989. Two-stage model of memory trace formation: A role for “noisy” brain states. Neuroscience 31: 551–570.
14. Buzsáki G, Moser EI. 2013. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 16: 130–138.
15. Buzsáki G, Leung LW, Vanderwolf CH. 1983. Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287: 139–171.
16. Chrobak JJ, Buzsáki G. 1998. Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci 18: 388–398.
17. Chun MM, Turk-Browne NB. 2007. Interactions between attention and memory.CurrOpin Neurobiol 17: 177–184.
18. Cohen NJ, Squire LR. 1980. Preserved learning and retention of pattern analyzing skill in amnesia: Dissociation of knowing how and knowing that. Science 210: 207–209.
19. Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI. 2009. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462: 353–357.
20. Corkin S. 2002. What’s new with the amnesic patient H.M.? Nature Rev Neurosci 3: 153–160.
21. Csicsvari J, Jamieson B, Wise KD, Buzsáki G. 2003. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37: 311–322.
22. 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: 7504–7512.
23. Diba K, Buzsaki G. 2007. Forward and reverse hippocampal place-cell sequences during ripples. Nat Neurosci 10: 1241–1242.
24. Dragoi G, Tonegawa S. 2011. Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 469: 397–401.
25. Dragoi G, Tonegawa S. 2013. Distinct preplay of multiple novel spatial experiences in the rat. Proc Natl Acad Sci 110: 9100–9105.
26. Ebbinghaus H. 1885. Uber das Gedächtnis Untersuchungen zur Experimentellen Psychologie [Memory: A contribution to experimental psychology]. von Duncker and Humber,Leipzig, Germany.
27. Ego-Stengel V, Wilson MA. 2010. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20: 1–10.
28. Eichenbaum H, Kuperstein M, Fagan A, Nagode J. 1987. Cue-sampling and goal-approach correlates of hippocampal unit activity in rats performing an odor-discrimination task. J Neurosci 7: 716–732.
29. Ekstrom AD, Meltzer J, McNaughton BL, Barnes CA. 2001. NMDA receptor antagonism blocks experience-dependent expansion of hippocampal “place fields.” Neuron 31: 631–638.
30. Ferbinteanu J, Shapiro ML. 2003. Prospective and retrospective memory coding in the hippocampus. Neuron 40: 1227–1239.
31. Foster DJ, Wilson MA. 2006. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440: 680–683.
32. Frank LM, Brown EN, Wilson M. 2000. Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27: 169–178.
33. Frank LM, Stanley GB, Brown EN. 2004. Hippocampal plasticity across multiple days of exposure to novel environments. J Neurosci 24: 7681–7689.
34. Frankland PW, O’Brien C, Ohno M, Kirkwood A, Silva AJ. 2001. a-CaMKII-dependent plasticity in the cortex is required for permanent memory. Nature 411: 309–313.
35. Fuhs MC, Touretzky DS. 2006. A spin glass model of path integration in rat medial entorhinal cortex. J Neurosci 26: 4266–4276.
36. Fyhn M, Molden S, Witter MP, Moser EI, Moser M-B. 2004. Spatial representation in the entorhinal cortex. Science 305: 1258–1264.
37. Fyhn M, Hafting T, Treves A, Moser M-B, Moser EI. 2007. Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446: 190–194.
38. Gelbard-Sagiv H, Mukamel R, Harel M, Malach R, Fried I. 2008. Internally generated reactivation of single neurons in human hippocampus during free recall. Science 322: 96–101.
39. Giocomo LM, Stensola T, Bonnevie T, Van Cauter T, Moser M-B, Moser EI. 2014. Topography of head direction cells in medial entorhinal cortex. Curr Biol 24: 252–262.
40. Girardeau G, Benchenane K, Wiener SI, Buzsaki G, Zugaro MB. 2009. Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci 12: 1222–1223.
41. Gupta AS, van der Meer MA, Touretzky DS, Redish AD. 2010. Hippocampal replay is not a simple function of experience. Neuron 65: 695–705.
42. Hafting T, Fyhn M, Molden S, Moser M-B, Moser EI. 2005. Microstructure of a spatial map in the entorhinal cortex. Nature 436: 801–806.
43. Hampson RE, Heyser CJ, Deadwyler SA. 1993. Hippocampal cell firing correlates of delayed-match-to-sample performance in the rat. Behav Neurosci 107: 715–739.
44. Hartley T, Burgess N, Lever C, Cacucci F, O’Keefe J. 2000. Modeling placefieldsin terms of the cortical inputs to the hippocampus. Hippocampus 10: 369–379.
45. Hassabis D, Kumaran D, Maguire EA. 2007. Using imagination to understand the neural basis of episodic memory. J Neurosci 27: 14365–14374.
46. Hebb DO. 1949. The organization of behavior. Wiley, New York.
47. Hill AJ. 1978. First occurrence of hippocampal spatial firing in a new environment. Exp Neurol 62: 282–297.
48. Hoffman KL, McNaughton BL. 2002. Coordinated reactivation of distributed memory traces in primate neocortex. Science 297: 2070–2073.
49. Igarashi KM, Lu L, Colgin LL, Moser M-B, Moser EI. 2014. Coordination of entorhinal–hippocampal ensemble activity during associative learning. Nature 510: 143–147.
50. 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.
51. Kandel ER, Schwartz JH. 1982. Molecular biology of learning: Modulation of transmitter release. Science 218: 433– 443.
52. Karlsson MP, Frank LM. 2009. Awake replay of remote experiences in the hippocampus. Nat Neurosci 12: 913–918.
53. 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.
54. Kentros CG, Agnihotri NT, Streater S, Hawkins RD, Kandel ER. 2004. Increased attention to spatial context increases both place field stability and spatial memory. Neuron 42: 283–295.
55. Kjelstrup KB, Solstad T, Brun VH, Hafting T, Leutgeb S, Witter MP, Moser EI, Moser M-B. 2008. Finite scales of spatial representation in the hippocampus. Science 321: 140–143.
56. 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.
57. Lashley KS. 1929. Brain mechanisms and intelligence: A qualitative study of injuries to the brain. University of Chicago Press, Chicago.
58. Lashley KS. 1950. In search of the engram. In Symposium of the society for experimental biology, Vol. 4. Cambridge University Press, New York.
59. Leutgeb S, Leutgeb JK, Treves A, Moser M-B, Moser EI. 2004. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305: 1295–1298.
60. Leutgeb JK, Leutgeb S, Treves A, Meyer R, Barnes CA, Mc-Naughton BL, Moser M-B, Moser EI. 2005a. Progressive transformationof hippocampal neuronal representations in “morphed” environments. Neuron 48: 345–358.
61. Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, Moser M-B. 2005b. Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309: 619–623.
62. Leutgeb S, Leutgeb JK, Moser EI, Moser MB. 2006. Fast rate coding in hippocampal CA3 cell ensembles. Hippocampus 16: 765–774.
63. Leutgeb JK, Leutgeb S, Moser MB, Moser EI. 2007. Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315: 961–966.
64. 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.
65. Markus EJ, Qin YL, Leonard B, Skaggs WE, McNaughton BL, Barnes CA. 1995. Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J Neurosci 15: 7079–7094.
66. Marr D. 1971. Simple memory: A theory for archicortex. Philos Trans R Soc Lond B Biol Sci 262: 23–81.
67. McClelland JL, McNaughton BL, O’Reilly RC. 1995. Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. Psychol Rev 102: 419–457.
68. McHugh TJ, Blum KI, Tsien JZ, Tonegawa S, Wilson MA. 1996. Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice. Cell 87: 1339– 1349.
69. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser M-B. 2006. Path integration and the neural basis of the “cognitive map.” Nature Rev Neurosci 7: 663–678.
70. Mehta MR, Barnes CA, McNaughton BL. 1997. Experience-dependent, asymmetric expansion of hippocampal place fields. Proc Natl Acad Sci 94: 8918–8921.
71. Mehta MR, Quirk MC, Wilson MA. 2000. Experience-dependent asymmetric shape of hippocampal receptive fields. Neuron 25: 707–715.
72. Miller JF, Neufang M, Solway A,Brandt A, Trippel M, Mader I, Hefft S, Merkow M, Polyn SM, Jacobs J, et al. 2013. Neural activity in human hippocampal formation reveals the spatial context of retrieved memories. Science 342: 1111–1114.
73. Milner B, Corkin S, Teuber HL. 1968. Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M. Neuropsychologia 6: 215–234.
74. Mishkin M. 1978. Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus. Nature 273: 297–298.
75. Moita MA, Rosis S, Zhou Y, LeDoux JE, Blair HT. 2004. Putting fear in its place: Remapping of hippocampal place cells during fear conditioning. J Neurosci 24: 7015–7023.
76. Monaco JD, Abbott LF. 2011. Modular realignment of entorhinal grid cell activity as a basis for hippocampal remapping. J Neurosci 31: 9414–9425.
77. Monaco JD, Rao G, Roth ED, Knierim JJ. 2014. Attentive scanning behavior drives one-trial potentiation of hippocampal place fields. Nat Neurosci 17: 725–731.
78. Moser EI, Kropff E, Moser M-B. 2008. Place cells, grid cells, and the brain’s spatial representation system. Annu Rev Neurosci 31: 69–89.
79. 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.
80. Muzzio IA, Levita L, Kulkarni J, Monaco J, Kentros C, Stead M, Abbott LF, Kandel ER. 2009. Attention enhances the retrieval and stability of visuospatial and olfactory representations in the dorsal hippocampus. PLoS Biol 7: e1000140.
81. O’Keefe J. 1976. Place units in the hippocampus of the freely moving rat. Exp Neurol 51: 78–109.
82. O’Keefe J, Burgess N. 1996. Geometric determinants of the place fields of hippocampal neurons. Nature 381: 425– 428.
83. O’Keefe J, Burgess N. 2005. Dual phase and rate coding in hippocampal place cells: Theoretical significance and relationshiptoentorhinal grid cells. Hippocampus 15: 853– 866.
84. 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.
85. O’Keefe J, Nadel L. 1978. The hippocampus as a cognitive map. Clarendon, Oxford.
86. O’Keefe J, Speakman A. 1987. Single unit activity in the rat hippocampus during a spatial memory task. Exp Brain Res 68: 1–27.
87. O’Neill J, Senior T, Csicsvari J. 2006. Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron 49: 143–155.
88. Pavlides C, Winson J. 1989. Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J Neurosci 9: 2907– 2918.
89. Pfeiffer BE, Foster DJ. 2013. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497: 74–79.
90. 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: 1945–1963.
91. Ranck JB Jr . 1973. Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats: I. Behavioral correlates and firing repertoires. Exp Neurol 41: 461–531.
92. Ranck JB. 1985. Head direction cells in the deep cell layer of dorsal presubiculum in freely moving rats. In Electrical activity of the archicortex (ed. Buzsa´ki G, Vanderwolf CH), pp. 217–220. Akademiai Kiado, Budapest.
93. Rolls ET, Stringer SM, Elliot T. 2006. Entorhinal cortex grid cells can map to hippocampal place cells by competitive learning. Network 17: 447–465.
94. Rotenberg A, Mayford M, Hawkins RD, Kandel ER, Muller RU. 1996. Mice expressing activated CaMKII lack low frequency LTP and do not form stable place cells in the CA1 region of the hippocampus. Cell 87: 1351–1361.
95. Rowland DC, Moser M-B. 2014. From cortical modules to memories. Curr Opin Neurobiol 24C: 22–27.
96. Samsonovich A, McNaughton BL. 1997. Path integration and cognitive mapping in a continuous attractor neural network model. J Neurosci 17: 5900–5920.
97. 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: 754–758.
98. Savelli F, Knierim JJ. 2010. Hebbian analysis of the transformation of medial entorhinal grid-cell inputs to hippocampal place fields. J Neurophysiol 103: 3167–3183.
99. Savelli F, Yoganarasimha D, Knierim JJ. 2008. Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18: 1270–1282.
100. Scoville WB, Milner B. 1957. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20: 11–21.
101. Singer W. 1993. Synchronization of cortical activity and its putative role in information processing and learning. Annu Rev Physiol 55: 349–374.
102. Smith SL, Smith IT, Branco T, Häusser M. 2013. Dendritic spikes enhance stimulus selectivity in cortical neurons in vivo. Nature 503: 115–120.
103. Solstad T, Moser EI, Einevoll GT. 2006. From grid cells to place cells: A mathematical model. Hippocampus 16: 1026–1031.
104. Solstad T, Boccara CN, Kropff E, Moser M-B, Moser EI. 2008. Representation of geometric borders in the entorhinal cortex. Science 322: 1865–1868.
105. Squire LR. 1992. Memoryand the hippocampus:Asynthesis from findings with rats, monkeys, and humans. Psychol Rev 99: 195–231.
106. Squire LR, Alvarez P.1995. Retrograde amnesia and memory consolidation: A neurobiological perspective. Curr Opin Neurobiol 5: 169–177.
107. Stensola H, Stensola T, Solstad T, Frøland K, Moser M-B, Moser EI. 2012. The entorhinal map is discretized. Nature 492: 72–78.
108. Suddendorf T, Corballis MC. 2007. The evolution of foresight: What is mental time travel, and is it unique to humans? Behav Brain Sci 30: 299–313.
109. Taube JS. 2007. The head direction signal: Origins and sensory-motor integration. Annu Rev Neurosci 30: 181– 207.
110. Taube JS, Burton HL. 1995. Head direction cell activity monitored in a novel environment and during a cue conflict situation. J Neurophysiol 74: 1953–1971.
111. 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: 420–435.
112. Tolman EC. 1948. Cognitive maps in rats and men. Psychol Rev 55: 189–208.
113. Watrous AJ, Tandon N, Conner CR, Pieters T, Ekstrom AD. 2013. Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval. Nat Neurosci 16: 349–356.
114. Wills TJ, Cacucci F, Burgess N, O’Keefe J. 2010. Development of the hippocampal cognitive map in preweanling rats. Science 328: 1573–1576.
115. Wilson MA, McNaughton BL. 1993. Dynamics of the hippocampal ensemble code for space. Science 261: 1055– 1058.
116. Wilson MA, McNaughton BL. 1994. Reactivation of hippocampal ensemble memories during sleep. Science 265: 676–679.
117. Wood ER, Dudchenko PA, Eichenbaum H.1999. Theglobal recordof memory in hippocampal neuronal activity. Nature 397: 613–616.
118. Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H. 2000. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27: 623–633.
119. 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: 622–631.
120. Young BJ, Fox GD, Eichenbaum H. 1994. Correlates of hippocampal complex-spike cell activity in rats performing a nonspatial radial maze task. J Neurosci 14: 6553–6563.
121. Zhang SJ, Ye J, Miao CL, Tsao A, Cerniauskas I, Ledergerber D, Moser M-B, Moser EI. 2013. Optogenetic dissection of entorhinal-hippocampal functional connectivity. Science 340: 1232627.
122. Zhang S-J, Ye J, Couey JJ, Witter MP, Moser EI, Moser M-B. 2014. Functional connectivity of the entorhinal-hippocampal space circuit. Philos Trans R Soc Lond B Biol Sci 369: 20120516.
123. Zola-Morgan S, Squire LR, Amaral DG. 1986. Human amnesia and the medial temporal region: Enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 6: 2950–2967.