A model of grid cell development through spatial exploration and spike time-dependent plasticity

Neuron

Volumn 83, Issue 2, 2014, Pages 481-495

  Widloski, John ^a   Fiete, Ila R ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL MATURATION; CONTROLLED STUDY; ENTORHINAL CORTEX; EXPLORATORY BEHAVIOR; GRID CELL; GRID CELL NETWORK; HUMAN; HUMAN CELL; INTERNEURON; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; PHASE TRANSITION; PRIORITY JOURNAL; SPIKE TIME DEPENDENT PLASTICITY; SPIKE WAVE;

ACTION POTENTIALS; ANIMALS; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; INTERNEURONS; MODELS, NEUROLOGICAL; NEURONAL PLASTICITY; NEURONS; SPATIAL BEHAVIOR;

EID: 84904281918     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.06.018     Document Type: Article

References (62)

1. Barry C., Hayman R., Burgess N., Jeffery K.J. Experience-dependent rescaling of entorhinal grids. Nat. Neurosci. 2007, 10:682-684.
2. Barry C., Ginzberg L.L., O'Keefe J., Burgess N. Grid cell firing patterns signal environmental novelty by expansion. Proc. Natl. Acad. Sci. USA 2012, 109:17687-17692.
3. Beed P., Gundlfinger A., Schneiderbauer S., Song J., Böhm C., Burgalossi A., Brecht M., Vida I., Schmitz D. Inhibitory gradient along the dorsoventral axis in the medial entorhinal cortex. Neuron 2013, 79:1197-1207.
4. Bjerknes T.L., Moser E.I., Moser M.B. Representation of geometric borders in the developing rat. Neuron 2014, 82:71-78.
5. Blair H.T., Gupta K., Zhang K. Conversion of a phase- to a rate-coded position signal by a three-stage model of theta cells, grid cells, and place cells. Hippocampus 2008, 18:1239-1255.
6. Bonnevie T., Dunn B., Fyhn M., Hafting T., Derdikman D., Kubie J.L., Roudi Y., Moser E.I., Moser M.B. Grid cells require excitatory drive from the hippocampus. Nat. Neurosci. 2013, 16:309-317.
7. 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.
8. Brandon M.P., Bogaard A.R., Andrews C.M., Hasselmo M.E. Head direction cells in the postsubiculum do not show replay of prior waking sequences during sleep. Hippocampus 2012, 22:604-618.
9. Burak Y., Fiete I. Do we understand the emergent dynamics of grid cell activity?. J.Neurosci. 2006, 26:9352-9354. discussion 9354.
10. Burak Y., Fiete I.R. Accurate path integration in continuous attractor network models of grid cells. PLoS Comput. Biol. 2009, 5:e1000291.
11. Burgess N., Barry C., O'Keefe J. An oscillatory interference model of grid cell firing. Hippocampus 2007, 17:801-812.
12. Canto C.B., Koganezawa N., Beed P., Moser E.I., Witter M.P. All layers of medial entorhinal cortex receive presubicular and parasubicular inputs. J.Neurosci. 2012, 32:17620-17631.
13. Coogan T.A., Burkhalter A. Hierarchical organization of areas in rat visual cortex. J.Neurosci. 1993, 13:3749-3772.
14. Couey J.J., Witoelar A., Zhang S.J., Zheng K., Ye J., Dunn B., Czajkowski R., Moser M.B., Moser E.I., Roudi Y., Witter M.P. Recurrent inhibitory circuitry as a mechanism for grid formation. Nat. Neurosci. 2013, 16:318-324.
15. Deshmukh S.S., Knierim J.J. Influence of local objects on hippocampal representations: Landmark vectors and memory. Hippocampus 2013, 23:253-267.
16. Dhillon A., Jones R.S. Laminar differences in recurrent excitatory transmission in the rat entorhinal cortex invitro. Neuroscience 2000, 99:413-422.
17. Doeller C.F., Barry C., Burgess N. Evidence for grid cells in a human memory network. Nature 2010, 463:657-661.
18. Domnisoru C., Kinkhabwala A.A., Tank D.W. Membrane potential dynamics of grid cells. Nature 2013, 495:199-204.
19. Feldman D.E. The spike-timing dependence of plasticity. Neuron 2012, 75:556-571.
20. Fiete I.R., Burak Y., Brookings T. What grid cells convey about rat location. J.Neurosci. 2008, 28:6858-6871.
21. Fino E., Venance L. Spike-timing dependent plasticity in the striatum. Front. Synaptic Neurosci 2010, 2. 10.3389/fnsyn.2010.00006.
22. Fuhs M.C., Touretzky D.S. A spin glass model of path integration in rat medial entorhinal cortex. J.Neurosci. 2006, 26:4266-4276.
23. Fyhn M., Hafting T., Witter M.P., Moser E.I., Moser M.-B. Grid cells in mice. Hippocampus 2008, 18:1230-1238.
24. Garden D.L.F., Dodson P.D., O'Donnell C., White M.D., Nolan M.F. Tuning of synaptic integration in the medial entorhinal cortex to the organization of grid cell firing fields. Neuron 2008, 60:875-889.
25. Giocomo L.M., Stensola T., Bonnevie T., Van Cauter T., Moser M.B., Moser E.I. Topography of head direction cells in medial entorhinal cortex. Curr. Biol. 2014, 24:252-262.
26. Gorchetchnikov A., Grossberg S. Neural Netw. 2007, 21:182-193.
27. Guanella A., Kiper D., Verschure P. A model of grid cells based on a twisted torus topology. Int. J. Neural Syst. 2007, 17:231-240.
28. Haas J.S., Nowotny T., Abarbanel H.D.I. Spike-timing-dependent plasticity of inhibitory synapses in the entorhinal cortex. J.Neurophysiol. 2006, 96:3305-3313.
29. 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.
30. Hahnloser R.H.R. Emergence of neural integration in the head-direction system by visual supervision. Neuroscience 2003, 120:877-891.
31. Hasselmo M.E., Bodelón C., Wyble B.P. A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput. 2002, 14:793-817.
32. Hasselmo M.E., Giocomo L.M., Zilli E.A. Grid cell firing may arise from interference of theta frequency membrane potential oscillations in single neurons. Hippocampus 2007, 17:1252-1271.
33. Heeger D.J. Normalization of cell responses in cat striate cortex. Vis. Neurosci. 1992, 9:181-197.
34. Hinton G.E. Neural Comp. 2002, 14.
35. Hinton G.E., Dayan P., Frey B.J., Neal R.M. The "wake-sleep" algorithm for unsupervised neural networks. Science 1995, 268:1158-1161.
36. Holmgren C.D., Zilberter Y. Coincident spiking activity induces long-term changes in inhibition of neocortical pyramidal cells. J.Neurosci. 2001, 21:8270-8277.
37. Huang S., Huganir R.L., Kirkwood A. Adrenergic gating ofHebbian spike-timing-dependent plasticity in cortical interneurons. J.Neurosci. 2013, 33:13171-13178.
38. Kerr K.M., Agster K.L., Furtak S.C., Burwell R.D. Functional neuroanatomy of the parahippocampal region: the lateral and medial entorhinal areas. Hippocampus 2007, 17:697-708.
39. Killian N.J., Jutras M.J., Buffalo E.A. A map of visual space in the primate entorhinal cortex. Nature 2012, 491:761-764.
40. Kropff E., Treves A. The emergence of grid cells: Intelligent design or just adaptation?. Hippocampus 2008, 18:1256-1269.
41. Kruge I.U., Wernle T., Moser E.I., Moser M.B. Grid cells of animals raised in spherical environments. Society for Neuroscience 2013.
42. 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.
43. Lever C., Burton S., Jeewajee A., O'Keefe J., Burgess N. Boundary vector cells in the subiculum of the hippocampal formation. J.Neurosci. 2009, 29:9771-9777.
44. Lu J.T., Li C.Y., Zhao J.-P., Poo M.M., Zhang X.H. Spike-timing-dependent plasticity of neocortical excitatory synapses on inhibitory interneurons depends on target cell type. J.Neurosci. 2007, 27:9711-9720.
45. Mathis A., Herz A.V., Stemmler M. Optimal population codes for space: grid cells outperform place cells. Neural Comput. 2012, 24:2280-2317.
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. Grid cell hexagonal patterns formed by fast self-organized learning within entorhinal cortex. Hippocampus 2012, 22:320-334.
48. Muir G.M., Bilkey D.K. Theta- and movement velocity-related firing of hippocampal neurons is disrupted by lesions centered on the perirhinal cortex. Hippocampus 2003, 13:93-108.
49. Pastoll H., Solanka L., van Rossum M.C.W., Nolan M.F. Feedback inhibition enables θ-nested γ oscillations and grid firing fields. Neuron 2013, 77:141-154.
50. Sargolini F., Fyhn M., Hafting T., McNaughton B.L., Witter M.P., Moser M.-B., Moser E.I. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 2006, 312:758-762.
51. Schmidt-Hieber C., Häusser M. Cellular mechanisms of spatial navigation in the medial entorhinal cortex. Nat. Neurosci. 2013, 16:325-331.
52. Solstad T., Boccara C.N., Kropff E., Moser M.-B., Moser E.I. Representation of geometric borders in the entorhinal cortex. Science 2008, 322:1865-1868.
53. Sreenivasan S., Fiete I. Grid cells generate an analog error-correcting code for singularly precise neural computation. Nat. Neurosci. 2011, 14:1330-1337.
54. Stensola H., Stensola T., Solstad T., Frøland K., Moser M.B., Moser E.I. The entorhinal grid map is discretized. Nature 2012, 492:72-78.
55. Stensola T., Stensola H., Moser M.B., Moser E.I. Environmental constraints on grid cell orientation. Society for Neuroscience 2013.
56. Stewart S., Jeewajee A., Wills T.J., Burgess N., Lever C. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014, 369. 10.1098/rstb.2012.0514.
57. Stringer S.M., Trappenberg T.P., Rolls E.T., Araujo I.E.T. Network. Comput in Neural Sys 2002, 13:217-242.
58. Taube J.S. The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 2007, 30:181-207.
59. Wills T.J., Cacucci F., Burgess N., O'Keefe J. Development of the hippocampal cognitive map in preweanling rats. Science 2010, 328:1573-1576.
60. Yartsev M.M., Witter M.P., Ulanovsky N. Grid cells without theta oscillations in the entorhinal cortex of bats. Nature 2011, 479:103-107.
61. Yoon K., Buice M.A., Barry C., Hayman R., Burgess N., Fiete I.R. Specific evidence of low-dimensional continuous attractor dynamics in grid cells. Nat. Neurosci. 2013, 16:1077-1084.
62. Zhang K. Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J.Neurosci. 1996, 16:2112-2126.