Grid and Nongrid Cells in Medial Entorhinal Cortex Represent Spatial Location and Environmental Features with Complementary Coding Schemes

Neuron

Volumn 94, Issue 1, 2017, Pages 83-92.e6

  Diehl, Geoffrey W ^a   Hon, Olivia J ^a   Leutgeb, Stefan ^a,b   Leutgeb, Jill K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

border cells; entorhinal cortex; grid cells; hippocampus; memory; nongrid cells; place cell; remapping; spatial navigation

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COLOR; CONTROLLED STUDY; ENVIRONMENT; FIRING RATE; GRID CELL; MALE; MEDIAL ENTORHINAL CORTEX; NERVE CELL; NONGRID SPATIAL CELL; NONHUMAN; OPEN FIELD BEHAVIOR; PHYSICAL PARAMETERS; RAT; SHAPE; SPATIAL DISCRIMINATION; ACTION POTENTIAL; ANIMAL; CYTOLOGY; ENTORHINAL CORTEX; HIPPOCAMPUS; LONG EVANS RAT; PHYSIOLOGY; SPATIAL BEHAVIOR; SPATIAL MEMORY; SPATIAL ORIENTATION;

ACTION POTENTIALS; ANIMALS; ENTORHINAL CORTEX; ENVIRONMENT; HIPPOCAMPUS; NEURONS; RATS; RATS, LONG-EVANS; SPATIAL MEMORY; SPATIAL NAVIGATION; SPATIAL PROCESSING;

EID: 85016019166     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2017.03.004     Document Type: Article

References (48)

1. Aghajan, Z.M., Acharya, L., Moore, J.J., Cushman, J.D., Vuong, C., Mehta, M.R., Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality. Nat. Neurosci. 18 (2015), 121–128.
2. Anderson, M.I., Jeffery, K.J., Heterogeneous modulation of place cell firing by changes in context. J. Neurosci. 23 (2003), 8827–8835.
3. Barry, C., Ginzberg, L.L., O'Keefe, J., Burgess, N., Grid cell firing patterns signal environmental novelty by expansion. Proc. Natl. Acad. Sci. USA 109 (2012), 17687–17692.
4. Bellgowan, P.S., Buffalo, E.A., Bodurka, J., Martin, A., Lateralized spatial and object memory encoding in entorhinal and perirhinal cortices. Learn. Mem. 16 (2009), 433–438.
5. Bjerknes, T.L., Langston, R.F., Kruge, I.U., Moser, E.I., Moser, M.B., Coherence among head direction cells before eye opening in rat pups. Curr. Biol. 25 (2015), 103–108.
6. 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. 13 (2010), 987–994.
7. Buzsáki, G., Moser, E.I., Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 16 (2013), 130–138.
8. Deshmukh, S.S., Spatial and nonspatial representations in the lateral entorhinal cortex. Derdikman, D., Knierim, J.J., (eds.) Space, Time and Memory in the Hippocampal Formation, 2014, Springer Vienna, 127–152.
9. Eichenbaum, H., Sauvage, M., Fortin, N., Komorowski, R., Lipton, P., Towards a functional organization of episodic memory in the medial temporal lobe. Neurosci. Biobehav. Rev. 36 (2012), 1597–1608.
10. Fyhn, M., Hafting, T., Treves, A., Moser, M.B., Moser, E.I., Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446 (2007), 190–194.
11. Hafting, T., Fyhn, M., Molden, S., Moser, M.B., Moser, E.I., Microstructure of a spatial map in the entorhinal cortex. Nature 436 (2005), 801–806.
12. Hargreaves, E.L., Yoganarasimha, D., Knierim, J.J., Cohesiveness of spatial and directional representations recorded from neural ensembles in the anterior thalamus, parasubiculum, medial entorhinal cortex, and hippocampus. Hippocampus 17 (2007), 826–841.
13. Keene, C.S., Bladon, J., McKenzie, S., Liu, C.D., O'Keefe, J., Eichenbaum, H., Complementary functional organization of neuronal activity patterns in the perirhinal, lateral entorhinal, and medial entorhinal cortices. J. Neurosci. 36 (2016), 3660–3675.
14. Killian, N.J., Jutras, M.J., Buffalo, E.A., A map of visual space in the primate entorhinal cortex. Nature 491 (2012), 761–764.
15. Kitamura, T., Sun, C., Martin, J., Kitch, L.J., Schnitzer, M.J., Tonegawa, S., Entorhinal cortical ocean cells encode specific contexts and drive context-specific fear memory. Neuron 87 (2015), 1317–1331.
16. Knierim, J.J., Lee, I., Hargreaves, E.L., Hippocampal place cells: parallel input streams, subregional processing, and implications for episodic memory. Hippocampus 16 (2006), 755–764.
17. Knierim, J.J., Neunuebel, J.P., Deshmukh, S.S., Functional correlates of the lateral and medial entorhinal cortex: objects, path integration and local-global reference frames. Philos. Trans. R. Soc. Lond. B Biol. Sci., 369, 2013, 20130369.
18. 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 (2011), 592–595.
19. Kraus, B.J., Brandon, M.P., Robinson, R.J. 2nd, Connerney, M.A., Hasselmo, M.E., Eichenbaum, H., During running in place, grid cells integrate elapsed time and distance run. Neuron 88 (2015), 578–589.
20. Kropff, E., Carmichael, J.E., Moser, M.B., Moser, E.I., Speed cells in the medial entorhinal cortex. Nature 523 (2015), 419–424.
21. Krupic, J., Bauza, M., Burton, S., Barry, C., O'Keefe, J., Grid cell symmetry is shaped by environmental geometry. Nature 518 (2015), 232–235.
22. 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 328 (2010), 1576–1580.
23. Latuske, P., Toader, O., Allen, K., Interspike intervals reveal functionally distinct cell populations in the medial entorhinal cortex. J. Neurosci. 35 (2015), 10963–10976.
24. Lee, H., Wang, C., Deshmukh, S.S., Knierim, J.J., Neural population evidence of functional heterogeneity along the CA3 transverse axis: pattern completion versus pattern separation. Neuron 87 (2015), 1093–1105.
25. 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 309 (2005), 619–623.
26. Lipton, P.A., White, J.A., Eichenbaum, H., Disambiguation of overlapping experiences by neurons in the medial entorhinal cortex. J. Neurosci. 27 (2007), 5787–5795.
27. Lu, L., Leutgeb, J.K., Tsao, A., Henriksen, E.J., Leutgeb, S., Barnes, C.A., Witter, M.P., Moser, M.B., Moser, E.I., Impaired hippocampal rate coding after lesions of the lateral entorhinal cortex. Nat. Neurosci. 16 (2013), 1085–1093.
28. Mankin, E.A., Sparks, F.T., Slayyeh, B., Sutherland, R.J., Leutgeb, S., Leutgeb, J.K., Neuronal code for extended time in the hippocampus. Proc. Natl. Acad. Sci. USA 109 (2012), 19462–19467.
29. Marozzi, E., Ginzberg, L.L., Alenda, A., Jeffery, K.J., Purely translational realignment in grid cell firing patterns following nonmetric context change. Cereb. Cortex 25 (2015), 4619–4627.
30. Muller, R.U., Kubie, J.L., Ranck, J.B. Jr., Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J. Neurosci. 7 (1987), 1935–1950.
31. Newman, E.L., Hasselmo, M.E., Grid cell firing properties vary as a function of theta phase locking preferences in the rat medial entorhinal cortex. Front. Syst. Neurosci., 8, 2014, 193.
32. O'Keefe, J., Nadel, L., The Hippocampus as a Cognitive Map. 1978, Clarendon Press.
33. Pérez-Escobar, J.A., Kornienko, O., Latuske, P., Kohler, L., Allen, K., Visual landmarks sharpen grid cell metric and confer context specificity to neurons of the medial entorhinal cortex. eLife, 5, 2016, 10.7554/eLife.16937.
34. Quian Quiroga, R., Kraskov, A., Koch, C., Fried, I., Explicit encoding of multimodal percepts by single neurons in the human brain. Curr. Biol. 19 (2009), 1308–1313.
35. Quirk, G.J., Muller, R.U., Kubie, J.L., The firing of hippocampal place cells in the dark depends on the rat's recent experience. J. Neurosci. 10 (1990), 2008–2017.
36. Quirk, G.J., Muller, R.U., Kubie, J.L., Ranck, J.B. Jr., The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells. J. Neurosci. 12 (1992), 1945–1963.
37. Rennó-Costa, C., Lisman, J.E., Verschure, P.F., The mechanism of rate remapping in the dentate gyrus. Neuron 68 (2010), 1051–1058.
38. Rolls, E.T., Treves, A., Tovee, M.J., Panzeri, S., Information in the neuronal representation of individual stimuli in the primate temporal visual cortex. J. Comput. Neurosci. 4 (1997), 309–333.
39. 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 312 (2006), 758–762.
40. Schmitzer-Torbert, N., Jackson, J., Henze, D., Harris, K., Redish, A.D., Quantitative measures of cluster quality for use in extracellular recordings. Neuroscience 131 (2005), 1–11.
41. Skaggs, W.E., McNaughton, B.L., Gothard, K.M., Markus, E.J., An information-theoretic approach to deciphering the hippocampal code. Adv. Neural Inf. Process. Syst. 5 (1993), 1030–1037.
42. Solstad, T., Boccara, C.N., Kropff, E., Moser, M.B., Moser, E.I., Representation of geometric borders in the entorhinal cortex. Science 322 (2008), 1865–1868.
43. Stensola, H., Stensola, T., Solstad, T., Frøland, K., Moser, M.B., Moser, E.I., The entorhinal grid map is discretized. Nature 492 (2012), 72–78.
44. Tang, Q., Burgalossi, A., Ebbesen, C.L., Ray, S., Naumann, R., Schmidt, H., Spicher, D., Brecht, M., Pyramidal and stellate cell specificity of grid and border representations in layer 2 of medial entorhinal cortex. Neuron 84 (2014), 1191–1197.
45. Wills, T.J., Cacucci, F., Burgess, N., O'Keefe, J., Development of the hippocampal cognitive map in preweanling rats. Science 328 (2010), 1573–1576.
46. Winter, S.S., Mehlman, M.L., Clark, B.J., Taube, J.S., Passive transport disrupts grid signals in the parahippocampal cortex. Curr. Biol. 25 (2015), 2493–2502.
47. Wirth, S., Yanike, M., Frank, L.M., Smith, A.C., Brown, E.N., Suzuki, W.A., Single neurons in the monkey hippocampus and learning of new associations. Science 300 (2003), 1578–1581.
48. Zhang, S.J., Ye, J., Miao, C., Tsao, A., Cerniauskas, I., Ledergerber, D., Moser, M.B., Moser, E.I., Optogenetic dissection of entorhinal-hippocampal functional connectivity. Science, 340, 2013, 1232627.