Grid cells require excitatory drive from the hippocampus

Nature Neuroscience

Volumn 16, Issue 3, 2013, Pages 309-317

  Bonnevie, Tora ^a   Dunn, Benjamin ^a   Fyhn, Marianne ^a,c   Hafting, Torkel ^a,c   Derdikman, Dori ^a,d   Kubie, John L ^b   Roudi, Yasser ^a   Moser, Edvard I ^a   Moser, May Britt ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b SUNY DOWNSTATE MEDICAL CENTER   (United States)

^c UNIVERSITY OF OSLO   (Norway)

^d TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CELL ACTIVITY; CELL TYPE; ENTORHINAL CORTEX; GRID CELL; HIPPOCAMPUS; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; REFRACTORY PERIOD; STRUCTURE ACTIVITY RELATION; THETA RHYTHM; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; COMPUTER SIMULATION; CYTOLOGY; DRUG EFFECT; LONG EVANS RAT; MALE; NERVE CELL; NERVE CELL NETWORK; PHYSIOLOGY;

4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; MUSCIMOL;

ACTION POTENTIALS; ANIMALS; COMPUTER SIMULATION; GABA-A RECEPTOR ANTAGONISTS; HIPPOCAMPUS; MALE; MODELS, NEUROLOGICAL; MUSCIMOL; NERVE NET; NEURONS; RATS; RATS, LONG-EVANS;

MLCS; MLOWN;

EID: 84875902101     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3311     Document Type: Article

References (43)

1. O'Keefe, J. & Dostrovsky, J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171-175 (1971).
2. Fyhn, M., Molden, S., Witter, M.P., Moser, E.I. & Moser, M.B. Spatial representation in the entorhinal cortex. Science 305, 1258-1264 (2004). (Pubitemid 39129224)
3. Hafting, T., Fyhn, M., Molden, S., Moser, M.B. & Moser, E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801-806 (2005). (Pubitemid 41160632)
4. Moser, E.I., Kropff, E. & Moser, M.-B. Place cells, grid cells, and the brain's spatial representation system. Annu. Rev. Neurosci. 31, 69-89 (2008).
5. Giocomo, L.M., Moser, M.-B. & Moser, E.I. Computational models of grid cells. Neuron 71, 589-603 (2011).
6. 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. 7, 663-678 (2006). (Pubitemid 44106748)
7. Taube, J.S., Muller, R.U. & Ranck, J.B. Jr. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10, 420-435 (1990).
8. Sargolini, F. et al. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312, 758-762 (2006).
9. Savelli, F., Yoganarasimha, D. & Knierim, J.J. Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18, 1270-1282 (2008).
10. Solstad, T., Boccara, C.N., Kropff, E., Moser, M.B. & Moser, E.I. Representation of geometric borders in the entorhinal cortex. Science 322, 1865-1868 (2008).
11. Fyhn, M., Hafting, T., Treves, A., Moser, M.-B. & Moser, E.I. Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446, 190-194 (2007). (Pubitemid 46398668)
12. Fuhs, M.C. & Touretzky, D.S. A spin glass model of path integration in rat medial entorhinal cortex. J. Neurosci. 26, 4266-4276 (2006). (Pubitemid 44315386)
13. Solstad, T., Moser, E.I. & Einevoll, G.T. From grid cells to place cells: a mathematical model. Hippocampus 16, 1026-1031 (2006). (Pubitemid 46062829)
14. Molter, C. & Yamaguchi, Y. Entorhinal theta phase precession sculpts dentate gyrus place fields. Hippocampus 18, 919-930 (2008).
15. Rolls, E.T., Stringer, S.M. & Elliot, T. Entorhinal cortex grid cells can map to hippocampal place cells by competitive learning. Network 17, 447-465 (2006). (Pubitemid 44905324)
16. 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. 29, 7504-7512 (2009).
17. Savelli, F. & Knierim, J.J. Hebbian analysis of the transformation of medial entorhinal grid-cell inputs to hippocampal place fields. J. Neurophysiol. 103, 3167-3183 (2010).
18. Si, B. & Treves, A. The role of competitive learning in the generation of DG fields from EC inputs. Cogn. Neurodyn. 3, 177-187 (2009).
19. Monaco, J.D. & Abbott, L.F. Modular realignment of entorhinal grid cell activity as a basis for hippocampal remapping. J. Neurosci. 31, 9414-9425 (2011); erratum 31, 11096 (2011).
20. O'Keefe, J. & Burgess, N. Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells. Hippocampus 15, 853-866 (2005). (Pubitemid 41556415)
21. Burgess, N., Barry, C. & O'Keefe, J. An oscillatory interference model of grid cell firing. Hippocampus 17, 801-812 (2007). (Pubitemid 47493460)
22. Kropff, E. & Treves, A. The emergence of grid cells: intelligent design or just adaptation? Hippocampus 18, 1256-1269 (2008).
23. Sreenivasan, S. & Fiete, I. Grid cells generate an analog error-correcting code for singularly precise neural computation. Nat. Neurosci. 14, 1330-1337 (2011).
24. Samu, D., Erös, P., Ujfalussy, B. & Kiss, T. Robust path integration in the entorhinal grid cell system with hippocampal feed-back. Biol. Cybern. 101, 19-34 (2009).
25. Hafting, T., Fyhn, M., Bonnevie, T., Moser, M.-B. & Moser, E.I. Hippocampus-independent phase precession in entorhinal grid cells. Nature 453, 1248-1252 (2008). (Pubitemid 351913591)
26. Allen, T.A. et al. Imaging the spread of reversible brain inactivations using fluorescent muscimol. J. Neurosci. Methods 171, 30-38 (2008).
27. Boccara, C.N. et al. Grid cells in pre-and parasubiculum. Nat. Neurosci. 13, 987-994 (2010).
28. Langston, R.F. et al. Development of the spatial representation system in the rat. Science 328, 1576-1580 (2010).
29. O'Keefe, J. & Recce, M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317-330 (1993). (Pubitemid 23231466)
30. Burak, Y. & Fiete, I.R. Accurate path integration in continuous attractor network models of grid cells. PLOS Comput. Biol. 5, e1000291 (2009).
31. Couey, J.J. et al. Recurrent inhibitory circuitry as a mechanism for grid formation. Nat. Neurosci. doi:10.1038/nn.3310 (20 January 2013).
32. Van Haeften, T., Baks-te-Bulte, L., Goede, P.H., Wouterlood, F.G. & Witter, M.P. Morphological and numerical analysis of synaptic interactions between neurons in deep and superficial layers of the entorhinal cortex of the rat. Hippocampus 13, 943-952 (2003). (Pubitemid 38100743)
33. Kloosterman, F., Van Haeften, T., Witter, M.P. & Lopes Da Silva, F.H. Electrophysiological characterization of interlaminar entorhinal connections: an essential link for re-entrance in the hippocampal-entorhinal system. Eur. J. Neurosci. 18, 3037-3052 (2003). (Pubitemid 38021545)
34. Brandon, M.P. et al. Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science 332, 595-599 (2011).
35. Koenig, J., Linder, A.N., Leutgeb, J.K. & Leutgeb, S. The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science 332, 592-595 (2011).
36. Alonso, A. & Klink, R. Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. J. Neurophysiol. 70, 128-143 (1993). (Pubitemid 23220304)
37. Yoshida, M., Giocomo, L.G. & Hasselmo, M.E. Frequency of subthreshold oscillations at different membrane potential voltages in neurons at different anatomical positions on the dorsoventral axis in the rat medial entorhinal cortex. J. Neurosci. 31, 12683-12694 (2011).
38. Zilli, E.A. & Hasselmo, M.E. Coupled noisy spiking neurons as velocity-controlled oscillators in a model of grid cell spatial firing. J. Neurosci. 30, 13850-13860 (2010).
39. Stensola, H. et al. The entorhinal grid map is discretized. Nature 492, 72-78 (2012).
40. Yartsev, M.M., Witter, M.P. & Ulanovsky, N. Grid cells without theta oscillations in the entorhinal cortex of bats. Nature 479, 103-107 (2011).
41. Wills, T.J., Cacucci, F., Burgess, N. & O'Keefe, J. Development of the hippocampal cognitive map in preweanling rats. Science 328, 1573-1576 (2010).
42. Burwell, R.D. & Hafeman, D.M. Positional firing properties of postrhinal cortex neurons. Neuroscience 119, 577-588 (2003). (Pubitemid 36588833)
43. Muller, R.U. & Kubie, J.L. The firing of hippocampal place cells predicts the future position of freely moving rat. J. Neurosci. 9, 4101-4110 (1989). (Pubitemid 20027231)