Spatial and memory circuits in the medial entorhinal cortex

Current Opinion in Neurobiology

Volumn 32, Issue , 2015, Pages 16-23

  Sasaki, Takuya ^a   Leutgeb, Stefan ^a,b   Leutgeb, Jill K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DEVELOPMENT; BRAIN ELECTROPHYSIOLOGY; CELL FUNCTION; CONNECTOME; ENTORHINAL CORTEX; EPISODIC MEMORY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; LATERAL ENTORHINAL CORTEX; MEDIAL ENTORHINAL CORTEX; NERVE CELL NETWORK; NEUROPHYSIOLOGY; NONHUMAN; REVIEW; SEPTUM PELLUCIDUM; SIGNAL TRANSDUCTION; SPATIAL DISCRIMINATION; ANIMAL; CYTOLOGY; DEPTH PERCEPTION; MEMORY; NERVE CELL; PHYSIOLOGY;

ANIMALS; ENTORHINAL CORTEX; HIPPOCAMPUS; MEMORY; NERVE NET; NEURONS; SPACE PERCEPTION;

EID: 84908611398     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2014.10.008     Document Type: Review

References (52)

1. Scoville W.B., Milner B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 1957, 20:11-21.
2. Zola-Morgan S., Squire L.R. The neuropsychology of memory. Parallel findings in humans and nonhuman primates. Ann N Y Acad Sci 1990, 608:434-450. (discussion 436-450).
3. 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 2012, 36:1597-1608.
4. Witter M.P., Wouterlood F.G., Naber P.A., Van Haeften T. Anatomical organization of the parahippocampal-hippocampal network. Ann N Y Acad Sci 2000, 911:1-24.
5. Squire L.R., Zola-Morgan S. The medial temporal lobe memory system. Science 1991, 253:1380-1386.
6. 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.
7. 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.
8. Taube J.S. The head direction signal: origins and sensory-motor integration. Annu Rev Neurosci 2007, 30:181-207.
9. Solstad T., Moser E.I., Einevoll G.T. From grid cells to place cells: a mathematical model. Hippocampus 2006, 16:1026-1031.
10. 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.
11. 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.
12. Stensola H., Stensola T., Solstad T., Froland K., Moser M.B., Moser E.I. The entorhinal grid map is discretized. Nature 2012, 492:72-78.
13. Yartsev M.M., Witter M.P., Ulanovsky N. Grid cells without theta oscillations in the entorhinal cortex of bats. Nature 2011, 479:103-107.
14. Killian N.J., Jutras M.J., Buffalo E.A. A map of visual space in the primate entorhinal cortex. Nature 2012, 491:761-764.
15. 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.
16. Ray S., Naumann R., Burgalossi A., Tang Q., Schmidt H., Brecht M. Grid-layout and theta-modulation of layer 2 pyramidal neurons in medial entorhinal cortex. Science 2014, 343:891-896.
17. Kitamura T., Pignatelli M., Suh J., Kohara K., Yoshiki A., Abe K., Tonegawa S. Island cells control temporal association memory. Science 2014, 343:896-901.
18. Varga C., Lee S.Y., Soltesz I. Target-selective GABAergic control of entorhinal cortex output. Nat Neurosci 2010, 13:822-824.
19. Domnisoru C., Kinkhabwala A.A., Tank D.W. Membrane potential dynamics of grid cells. Nature 2013, 495:199-204.
20. Schmidt-Hieber C., Hausser M. Cellular mechanisms of spatial navigation in the medial entorhinal cortex. Nat Neurosci 2013, 16:325-331.
21. 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.
22. 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.
23. 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 2013, 340:1232627.
24. 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.
25. Wills T.J., Cacucci F., Burgess N., O'Keefe J. Development of the hippocampal cognitive map in preweanling rats. Science 2010, 328:1573-1576.
26. Bjerknes T.L., Moser E.I., Moser M.B. Representation of geometric borders in the developing rat. Neuron 2014, 82:71-78.
27. Brandon M.P., Koenig J., Leutgeb J.K., Leutgeb S. New and distinct hippocampal place codes are generated in a new environment during septal inactivation. Neuron 2014, 82:789-796.
28. 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.
29. Bostock E., Muller R.U., Kubie J.L. Experience-dependent modifications of hippocampal place cell firing. Hippocampus 1991, 1:193-205.
30. 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.
31. McHugh T.J., Jones M.W., Quinn J.J., Balthasar N., Coppari R., Elmquist J.K., Lowell B.B., Fanselow M.S., Wilson M.A., Tonegawa S. Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 2007, 317:94-99.
32. 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 2013, 16:1085-1093.
33. 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.
34. Buzsaki G., Moser E.I. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 2013, 16:130-138.
35. Rowland D.C., Moser M.B. From cortical modules to memories. Curr Opin Neurobiol 2014, 24:22-27.
36. Hayman R.M., Jeffery K.J. How heterogeneous place cell responding arises from homogeneous grids - a contextual gating hypothesis. Hippocampus 2008, 18:1301-1313.
37. Monaco J.D., Abbott L.F. Modular realignment of entorhinal grid cell activity as a basis for hippocampal remapping. J Neurosci 2011, 31:9414-9425.
38. Barry C., Heys J.G., Hasselmo M.E. Possible role of acetylcholine in regulating spatial novelty effects on theta rhythm and grid cells. Front Neural Circ 2012, 6:5.
39. Winson J. Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 1978, 201:160-163.
40. Hasselmo M.E., Bower J.M. Acetylcholine and memory. Trends Neurosci 1993, 16:218-222.
41. Brandon M.P., Koenig J., Leutgeb S. Parallel and convergent processing in grid cell, head-direction cell, boundary cell, and place cell networks. Wiley Interdiscip Rev Cogn Sci 2014, 5:207-219.
42. Bush D., Barry C., Burgess N. What do grid cells contribute to place cell firing?. Trends Neurosci 2014, 37:136-145.
43. Zipser B. Sequential steps in axonal targeting are mediated by carbohydrate markers. J Neurobiol 1995, 27:326-334.
44. O'Keefe J., Burgess N. Geometric determinants of the place fields of hippocampal neurons. Nature 1996, 381:425-428.
45. Shapiro M.L., Hetherington P.A. A simple network model simulates hippocampal place fields: parametric analyses and physiological predictions. Behav Neurosci 1993, 107:34-50.
46. Yoganarasimha D., Rao G., Knierim J.J. Lateral entorhinal neurons are not spatially selective in cue-rich environments. Hippocampus 2011, 21:1363-1374.
47. Tsao A., Moser M.B., Moser E.I. Traces of experience in the lateral entorhinal cortex. Curr Biol 2013, 23:399-405.
48. Van Cauter T., Poucet B., Save E. Unstable CA1 place cell representation in rats with entorhinal cortex lesions. Eur J Neurosci 2008, 27:1933-1946.
49. Hales J.B., Schlesiger M.I., Leutgeb J.K., Squire L.R., Leutgeb S., Clark R.E. Medial entorhinal cortex lesions only partially disrupt hippocampal place cells and hippocampus-dependent place memory. Cell Rep 2014, (in press).
50. Lipton P.A., Eichenbaum H. Complementary roles of hippocampus and medial entorhinal cortex in episodic memory. Neural Plast 2008, 2008:258467.
51. Hafting T., Fyhn M., Bonnevie T., Moser M.B., Moser E.I. Hippocampus-independent phase precession in entorhinal grid cells. Nature 2008, 453:1248-1252.
52. 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.