Environmental Boundaries as an Error Correction Mechanism for Grid Cells

Neuron

Volumn 86, Issue 3, 2015, Pages 827-839

  Hardcastle, Kiah ^a   Ganguli, Surya ^a   Giocomo, Lisa M ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOACCUMULATION; BIOLOGICAL MODEL; CELL FUNCTION; CONTROLLED STUDY; IN VIVO STUDY; MALE; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; NERVE CELL; NERVE CELL NETWORK; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; RODENT; SIMULATION; ACTION POTENTIAL; ANIMAL; COMPUTER SIMULATION; CYTOLOGY; DEPTH PERCEPTION; ENTORHINAL CORTEX; ENVIRONMENT; EXPLORATORY BEHAVIOR; INFORMATION PROCESSING; MOUSE; PHYSIOLOGY; PROBABILITY; TIME;

ACTION POTENTIALS; ANIMALS; COMPUTER SIMULATION; DATASETS AS TOPIC; ENTORHINAL CORTEX; ENVIRONMENT; EXPLORATORY BEHAVIOR; MICE; MODELS, NEUROLOGICAL; NERVE NET; NEURONS; PROBABILITY; SPACE PERCEPTION; TIME FACTORS;

EID: 84928945420     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.03.039     Document Type: Article

References (59)

1. Barry C., Lever C., Hayman R., Hartley T., Burton S., O'Keefe J., Jeffery K., Burgess N. The boundary vector cell model of place cell firing and spatial memory. Rev. Neurosci. 2006, 17:71-97.
2. Barry C., Hayman R., Burgess N., Jeffery K.J. Experience-dependent rescaling of entorhinal grids. Nat. Neurosci. 2007, 10:682-684.
3. Bartels M. Sinnesphysiologische und psychologische Untersuchungen an der Trichterspinne Agelena labyrinthica (Cl.). Z.Vgl. Physiol. 1929, 10:527-593.
4. Bjerknes T.L., Moser E.I., Moser M.B. Representation of geometric borders in the developing rat. Neuron 2014, 82:71-78.
5. Burak Y., Fiete I.R. Accurate path integration in continuous attractor network models of grid cells. PLoS Comput. Biol. 2009, 5:e1000291.
6. Burgess N. Grid cells and theta as oscillatory interference: theory and predictions. Hippocampus 2008, 18:1157-1174.
7. Burgess N., Barry C., O'Keefe J. An oscillatory interference model of grid cell firing. Hippocampus 2007, 17:801-812.
8. Bush D., Burgess N. A hybrid oscillatory interference/continuous attractor network model of grid cell firing. J.Neurosci. 2014, 34:5065-5079.
9. Buzsáki G., Moser E.I. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 2013, 16:130-138.
10. Darwin C. Origin of certain instincts. Nature 1873, 7:417-418.
11. Derdikman D., Whitlock J.R., Tsao A., Fyhn M., Hafting T., Moser M.B., Moser E.I. Fragmentation of grid cell maps in a multicompartment environment. Nat. Neurosci. 2009, 12:1325-1332.
12. Deshmukh S.S., Knierim J.J. Representation of non-spatial andspatial information in the lateral entorhinal cortex. Front. Behav. Neurosci. 2011, 5:69.
13. Eggink H., Mertens P., Storm I., Giocomo L.M. HCN1 independent grid cell phase precession in mice. Hippocampus 2014, 24:249-256.
14. Etienne A.S. Navigation of a small mammal by dead reckoning and local cues. Curr. Dir. Psychol. Sci. 1992, 1:48-52.
15. Fuhs M.C., Touretzky D.S. A spin glass model of path integration in rat medial entorhinal cortex. J.Neurosci. 2006, 26:4266-4276.
16. Fyhn M., Molden S., Witter M.P., Moser E.I., Moser M.B. Spatial representation in the entorhinal cortex. Science 2004, 305:1258-1264.
17. Garden D.L., 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.
18. Giocomo L.M., Hasselmo M.E. Knock-out of HCN1 subunit flattens dorsal-ventral frequency gradient of medial entorhinal neurons in adultmice. J.Neurosci. 2009, 29:7625-7630.
19. Giocomo L.M., Hussaini S.A., Zheng F., Kandel E.R., Moser M.B., Moser E.I. Grid cells use HCN1 channels for spatial scaling. Cell 2011, 147:1159-1170.
20. 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.
21. Gothard K.M., Skaggs W.E., McNaughton B.L. Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J.Neurosci. 1996, 16:8027-8040.
22. Gothard K.M., Skaggs W.E., Moore K.M., McNaughton B.L. Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J.Neurosci. 1996, 16:823-835.
23. Gothard K.M., Hoffman K.L., Battaglia F.P., McNaughton B.L. Dentate gyrus and ca1 ensemble activity during spatial reference frame shifts in the presence and absence of visual input. J.Neurosci. 2001, 21:7284-7292.
24. 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.
25. Hasselmo M.E. Grid cell mechanisms and function: contributions of entorhinal persistent spiking and phase resetting. Hippocampus 2008, 18:1213-1229.
26. Killian N.J., Jutras M.J., Buffalo E.A. A map of visual space in the primate entorhinal cortex. Nature 2012, 491:761-764.
27. Knierim J.J., Kudrimoti H.S., McNaughton B.L. Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. J.Neurophysiol. 1998, 80:425-446.
28. Kropff E., Treves A. The emergence of grid cells: Intelligent design or just adaptation?. Hippocampus 2008, 18:1256-1269.
29. Krupic J., Bauza M., Burton S., Barry C., O'Keefe J. Grid cell symmetry is shaped by environmental geometry. Nature 2015, 518:232-235.
30. 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.
31. Leutgeb J.K., Leutgeb S., Treves A., Meyer R., Barnes C.A., McNaughton B.L., Moser M.B., Moser E.I. Progressive transformation of hippocampal neuronal representations in "morphed" environments. Neuron 2005, 48:345-358.
32. 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.
33. 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.
34. McNaughton B.L., Nadel L. Hebb-Marr networks and the neurobiological representation of action in space. Neuroscience and Connectionist Theory 1991, 1-64. Erlbaum, Hillsdale, NJ. M.A. Gluck, D.E. Rumelhart (Eds.).
35. McNaughton B.L., Chen L.L., Markus E.J. "Dead reckoning," landmark learning, and the sense of direction: a neurophysiological and computational hypothesis. J.Cogn. Neurosci. 1991, 3:190-202.
36. McNaughton B.L., Barnes C.A., Gerrard J.L., Gothard K., Jung M.W., Knierim J.J., Kudrimoti H., Qin Y., Skaggs W.E., Suster M., Weaver K.L. Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J.Exp. Biol. 1996, 199:173-185.
37. 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.
38. Mittelstaedt M., Mittelstaedt H. Homing by path integration in a mammal. Naturwissenschaften 1980, 67:566-567.
39. Moser E.I., Kropff E., Moser M.B. Place cells, grid cells, and the brain's spatial representation system. Annu. Rev. Neurosci. 2008, 31:69-89.
40. O'Keefe J., Burgess N. Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells. Hippocampus 2005, 15:853-866.
41. Redish A.D., Touretzky D.S. Cognitive maps beyond the hippocampus. Hippocampus 1997, 7:15-35.
42. Roudi Y., Treves A. Representing where along with what information in a model of a cortical patch. PLoS Comput. Biol. 2008, 4:e1000012.
43. Samsonovich A., McNaughton B.L. Path integration and cognitive mapping in a continuous attractor neural network model. J.Neurosci. 1997, 17:5900-5920.
44. Samu D., Eros P., Ujfalussy B., Kiss T. Robust path integration in the entorhinal grid cell system with hippocampal feed-back. Biol. Cybern. 2009, 101:19-34.
45. 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.
46. Savelli F., Yoganarasimha D., Knierim J.J. Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 2008, 18:1270-1282.
47. Skaggs W.E., Knierim J.J., Kudrimoti H.S., McNaughton B.L. Amodel of the neural basis of the rat's sense of direction. Adv. Neural Inf. Process. Syst. 1995, 7:173-180.
48. Skaggs W.E., McNaughton B.L., Wilson M.A., Barnes C.A. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 1996, 6:149-172.
49. 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.
50. Sreenivasan S., Fiete I. Grid cells generate an analog error-correcting code for singularly precise neural computation. Nat. Neurosci. 2011, 14:1330-1337.
51. 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.
52. Stensola T., Stensola H., Moser M.B., Moser E.I. Shearing-induced asymmetry in entorhinal grid cells. Nature 2015, 518:207-212.
53. Touretzky D.S., Redish A.D. Theory of rodent navigation based on interacting representations of space. Hippocampus 1996, 6:247-270.
54. Tsao A., Moser M.-B., Moser E.I. Traces of experience in the lateral entorhinal cortex. Curr. Biol. 2013, 23:399-405.
55. Wehner R., Srinivasan M.V. Searching behavior of desert ants, genus Cataglyphis (Formicidae, Hymenoptera). J.Comp. Physiol. 1981, 142:315-338.
56. Widloski J., Fiete I.R. A model of grid cell development through spatial exploration and spike time-dependent plasticity. Neuron 2014, 83:481-495.
57. Wills T.J., Cacucci F., Burgess N., O'Keefe J. Development of the hippocampal cognitive map in preweanling rats. Science 2010, 328:1573-1576.
58. Zhang K. Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J.Neurosci. 1996, 16:2112-2126.
59. Zhang S.J., Schönfeld F., Wiskott L., Manahan-Vaughan D. Spatial representations of place cells in darkness are supported by path integration and border information. Front. Behav. Neurosci. 2014, 8:222.