The structure of networks that produce the transformation from grid cells to place cells

Neuroscience

Volumn 197, Issue , 2011, Pages 293-306

  Cheng, S ^a   Frank, L M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Global remapping; Hippocampus; Medial entorhinal cortex; Unsupervised learning

Indexed keywords

ALGORITHM; ANIMAL BEHAVIOR; ARTICLE; BRAIN MAPPING; BRAIN NERVE CELL; CELL TRANSFORMATION; CONTROLLED STUDY; ENTORHINAL CORTEX; GRID CELL; INTERMETHOD COMPARISON; LEARNING; MATHEMATICAL MODEL; NERVE CELL NETWORK; NOISE; PLACE CELL; PRIORITY JOURNAL; SIMULATION; SYNAPSE;

ALGORITHMS; ANIMALS; ENTORHINAL CORTEX; HIPPOCAMPUS; HUMANS; MODELS, NEUROLOGICAL; MODELS, THEORETICAL; NERVE NET; NEURAL NETWORKS (COMPUTER); NEURONS; SPACE PERCEPTION;

EID: 82855161298     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.09.002     Document Type: Article

References (63)

1. Amaral D.G., Ishizuka N., Claiborne B. Neurons, numbers and the hippocampal network. Prog Brain Res 1990, 83:1-11.
2. Barry C., Burgess N. Learning in a geometric model of place cell firing. Hippocampus 2007, 17:786-800.
3. Blair H.T., Welday A.C., Zhang K. Scale-invariant memory representations emerge from moiré interference between grid fields that produce theta oscillations: a computational model. J Neurosci 2007, 27:3211-3229.
4. Boccara C.N., Sargolini F., Thoresen V.H., Solstad T., Witter M.P., Moser E.I., Moser M.B. Grid cells in pre- and parasubiculum. Nat Neurosci 2010, 13:987-994.
5. Brandon M.P., Bogaard A.R., Libby C.P., Connerney M.A., Gupta K., Hasselmo M.E. Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science 2011, 332:595-599.
6. Brown E.N., Barbieri R., Ventura V., Kass R.E., Frank L.M. The time-rescaling theorem and its application to neural spike train data analysis. Neural Comput 2002, 14:325-346.
7. Brun V.H., Solstad T., Kjelstrup K.B., Fyhn M., Witter M.P., Moser E.I., Moser M.B. Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex. Hippocampus 2008, 18:1200-1212.
8. Burak Y., Fiete I.R. Accurate path integration in continuous attractor network models of grid cells. PLoS Comput Biol 2009, 5:e1000291.
9. Burgess N. Grid cells and theta as oscillatory interference: theory and predictions. Hippocampus 2008, 18:1157-1174.
10. Burgess N., Barry C., O'Keefe J. An oscillatory interference model of grid cell firing. Hippocampus 2007, 17:801-812.
11. Chawla M.K., Guzowski J.F., Ramirez-Amaya V., Lipa P., Hoffman K.L., Marriott L.K., Worley P.F., McNaughton B.L., Barnes C.A. Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus 2005, 15:579-586.
12. Cheng S., Frank L.M. New experiences enhance coordinated neural activity in the hippocampus. Neuron 2008, 57:303-313.
13. Colgin L.L., Denninger T., Fyhn M., Hafting T., Bonnevie T., Jensen O., Moser M.B., Moser E.I. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 2009, 462:353-357.
14. de Almeida L., Idiart M., Lisman J.E. The input-output transformation of the hippocampal granule cells: from grid cells to place fields. J Neurosci 2009, 29:7504-7512.
15. Epsztein J., Brecht M., Lee A.K. Intracellular determinants of hippocampal CA1 place and silent cell activity in a novel environment. Neuron 2011, 70:109-120.
16. Fenton A.A., Kao H.Y., Neymotin S.A., Olypher A., Vayntrub Y., Lytton W.W., Ludvig N. 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 2008, 28:11250-11262.
17. Frank L.M., Stanley G.B., Brown E.N. Hippocampal plasticity across multiple days of exposure to novel environments. J Neurosci 2004, 24:7681-7689.
18. Franzius M., Vollgraf R., Wiskott L. From grids to places. J Comput Neurosci 2007, 22:297-299.
19. Fuhs M.C., Touretzky D.S. A spin glass model of path integration in rat medial entorhinal cortex. J Neurosci 2006, 26:4266-4276.
20. Fyhn M., Hafting T., Treves A., Moser M.B., Moser E.I. Hippocampal remapping and grid realignment in entorhinal cortex. Nature 2007, 446:190-194.
21. Giocomo L.M., Zilli E.A., Fransén E., Hasselmo M.E. Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science 2007, 315:1719-1722.
22. Golding N.L., Staff N.P., Spruston N. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 2002, 418:326-331.
23. Gorchetchnikov A., Grossberg S. Space, time and learning in the hippocampus: how fine spatial and temporal scales are expanded into population codes for behavioral control. Neural Netw 2007, 20:182-193.
24. Gütig R., Sompolinsky H. The tempotron: a neuron that learns spike timing-based decisions. Nat Neurosci 2006, 9:420-428.
25. Guzowski J.F., McNaughton B.L., Barnes C.A., Worley P.F. Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 1999, 2:1120-1124.
26. Hafting T., Fyhn M., Molden S., Moser M.B., Moser E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436:801-806.
27. Hargreaves E.L., Rao G., Lee I., Knierim J.J. Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 2005, 308:1792-1794.
28. Hartley T., Burgess N., Lever C., Cacucci F., O'Keefe J. Modeling place fields in terms of the cortical inputs to the hippocampus. Hippocampus 2000, 10:369-379.
29. Hasselmo M.E., Brandon M.P. Linking cellular mechanisms to behavior: entorhinal persistent spiking and membrane potential oscillations may underlie path integration, grid cell firing, and episodic memory. Neural Plast 2008, 2008:658323.
30. Hayman R.M., Jeffery K.J. How heterogeneous place cell responding arises from homogeneous grids-a contextual gating hypothesis. Hippocampus 2008, 18:1301-1313.
31. Hjorth S. Projection of the lateral part of the entorhinal area to the hippocampus and fascia dentata. J Comp Neurol 1972, 146:219-232.
32. Jung M.W., McNaughton B.L. Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 1993, 3:165-182.
33. Káli S., Dayan P. The involvement of recurrent connections in area CA3 in establishing the properties of place fields: a model. J Neurosci 2000, 20:7463-7477.
34. Karlsson M.P., Frank L.M. Network dynamics underlying the formation of sparse, informative representations in the hippocampus. J Neurosci 2008, 28:14271-14281.
35. Kjelstrup K.B., Solstad T., Brun V.H., Hafting T., Leutgeb S., Witter M.P., Moser E.I., Moser M.B. Finite scale of spatial representation in the hippocampus. Science 2008, 321:140-143.
36. Koenig J., Linder A.N., Leutgeb J.K., Leutgeb S. The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science 2011, 332:592-595.
37. Kropff E., Treves A. The emergence of grid cells: intelligent design or just adaptation?. Hippocampus 2008, 18:1256-1269.
38. Langston R.F., Ainge J.A., Couey J.J., Canto C.B., Bjerknes T.L., Witter M.P., Moser E.I., Moser M.B. Development of the spatial representation system in the rat. Science 2010, 328:1576-1580.
39. Leutgeb J.K., Henriksen E.J., Leutgeb S., Witter M.P., Moser M.B., Moser E.I. Hippocampal rate coding depends on input from the lateral entorhinal cortex 2008, Abstract Society for Neuroscience, Washington, DC.
40. Leutgeb J.K., Leutgeb S., Moser M.B., Moser E.I. Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 2007, 315:961-966.
41. Leutgeb S., Leutgeb J.K., Barnes C.A., Moser E.I., McNaughton B.L., Moser M.B. Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 2005, 309:619-623.
42. Leutgeb S., Leutgeb J.K., Treves A., Moser M.B., Moser E.I. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 2004, 305:1295-1298.
43. Li S., Cullen W.K., Anwyl R., Rowan M.J. Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty. Nat Neurosci 2003, 6:526-531.
44. Lisman J.E., Grace A.A. The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 2005, 46:703-713.
45. Manahan-Vaughan D., Braunewell K.H. Novelty acquisition is associated with induction of hippocampal long-term depression. Proc Natl Acad Sci U S A 1999, 96:8739-8744.
46. McNaughton B.L., Battaglia F.P., Jensen O., Moser E.I., Moser M.B. Path integration and the neural basis of the "cognitive map". Nat Rev Neurosci 2006, 7:663-678.
47. Mhatre H, Gorchetchnikov A, Grossberg S (in press) Grid cell hexagonal patterns formed by fast self-organized learning within entorhinal cortex. Hippocampus, in press.
48. Molter C., Yamaguchi Y. Entorhinal theta phase precession sculpts dentate gyrus place fields. Hippocampus 2008, 18:919-930.
49. Monaco JD, Abbott LF Modular realignment of entorhinal grid cell activity as a basis for hippocampal remapping. J Neurosci 31:9414-9425.
50. Muller R.U., Kubie J.L. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci 1987, 7:1951-1968.
51. O'Keefe J., Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 1971, 34:171-175.
52. O'Keefe J., Nadel L. The hippocampus as a cognitive map 1978, Oxford University Press, London.
53. Rennó-Costa C., Lisman J.E., Verschure P.F. The mechanism of rate remapping in the dentate gyrus. Neuron 2010, 68:1051-1058.
54. Rolls E.T., Stringer S.M., Elliot T. Entorhinal cortex grid cells can map to hippocampal place cells by competitive learning. Network 2006, 17:447-465.
55. Samsonovich A., McNaughton B.L. Path integration and cognitive mapping in a continuous attractor neural network model. J Neurosci 1997, 17:5900-5920.
56. Savelli F., Knierim J.J. Hebbian analysis of the transformation of medial entorhinal grid-cell inputs to hippocampal place fields. J Neurophysiol 2010, 103:3167-3183.
57. Si B., Treves A. The role of competitive learning in the generation of DG fields from EC inputs. Cogn Neurodyn 2009, 3:177-187.
58. Solstad T., Moser E.I., Einevoll G.T. From grid cells to place cells: a mathematical model. Hippocampus 2006, 16:1026-1031.
59. Stensland H., Kirkesola T., Moser M.B., Moser E.I. Orientational geometry of entorhinal grid cells 2010, Abstract Society for Neuroscience, San Diego, CA.
60. Straube T., Korz V., Frey J.U. Bidirectional modulation of long-term potentiation by novelty-exploration in rat dentate gyrus. Neurosci Lett 2003, 344:5-8.
61. Wills T.J., Cacucci F., Burgess N., O'Keefe J. Development of the hippocampal cognitive map in preweanling rats. Science 2010, 328:1573-1576.
62. Wilson M.A., McNaughton B.L. Dynamics of the hippocampal ensemble code for space. Science 1993, 261:1055-1058.
63. Xu L., Anwyl R., Rowan M.J. Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature 1998, 394:891-894.