Functional connectivity of the entorhinal - Hippocampal space circuit

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1635, 2014, Pages

  Zhang, Sheng Jia ^a   Ye, Jing ^a   Couey, Jonathan J ^a,b   Witter, Menno ^a   Moser, Edvard I ^a   Moser, May Britt ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Border cells; Entorhinal cortex; Grid cells; Hippocampus; Optogenetics; Place cells

Indexed keywords

BRAIN; GENETIC ANALYSIS; LIGHT EFFECT; MAMMAL; NEUROLOGY; SPATIAL DISTRIBUTION;

EID: 84890897387     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0516     Document Type: Review

References (65)

1. O'Keefe J, Dostrovsky J. 1971 The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171-175. (doi:10.1016/0006-8993(71)90358-1).
2. O'Keefe J, Nadel L. 1978 The hippocampus as a cognitive map. Oxford, UK: Clarendon Press.
3. Fenton AA, Kao HY, Neymotin SA, Olypher A, Vayntrub Y, Lytton WW, Ludvig N. 2008 Unmasking the CA1 ensemble place code by exposures to small and large environments: more place cells and multiple, irregularly arranged, and expanded place fields in the larger space. J. Neurosci. 28, 11 250-11 262. (doi:10.1523/JNEUROSCI.2862-08.2008)
4. Park E, Dvorak D, Fenton AA. 2011 Ensemble place codes in hippocampus: CA1, CA3, and dentate gyrus place cells have multiple place fields in large environments. PLoS ONE 6, e22349. (doi:10.1371/ journal.pone.0022349)
5. Muller RU, Kubie JL, Ranck Jr JB. 1987 Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J. Neurosci. 7, 1935-1950.
6. Jung MW, McNaughton BL. 1993 Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 33, 165-182. (doi:10.1002/hipo. 450030209)
7. Wilson MA, McNaughton BL. 1993 Dynamics of the hippocampal ensemble code for space. Science 261, 1055-1058. (doi:10.1126/science.8351520)
8. Leutgeb JK, Leutgeb S, Moser M-B, Moser EI. 2007 Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315, 961-966. (doi:10. 1126/science.1135801)
9. Henriksen EJ, Colgin LL, Barnes CA, Witter MP, Moser MB, Moser EI. 2010 Spatial representation along the proximodistal axis of CA1. Neuron 68, 127-137. (doi:10.1016/j.neuron.2010.08.042)
10. McNaughton BL, Barnes CA, Meltzer J, Sutherland RJ. 1989 Hippocampal granule cells are necessary for normal spatial learning but not for spatiallyselective pyramidal cell discharge. Exp. Brain Res. 76, 485-496. (doi:10.1007/BF00248904)
11. Brun VH, Otnass MK, Molden S, Steffenach HA, Witter MP, Moser MB, Moser EI. 2002 Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296, 2243-2246. (doi:10.1126/science.1071089)
12. Köhler C. 1985 Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex. J. Comp. Neurol. 236, 504-522. (doi:10.1002/cne.902360407)
13. Witter MP, Holtrop R, van de Loosdrecht AA. 1988 Direct projections from the periallocortical subicular complex to the fascia dentata in the rat. An anatomical tracing study using Phaseolus vulgaris leucoagglutinin. Neurosci. Res. Commun. 2, 61-68.
14. Naber PA, Witter MP, Lopes da Silva FH. 2001 Evidence for a direct projection from the postrhinal cortex to the subiculum in the rat. Hippocampus 11, 105-117. (doi:10.1002/hipo.1029)
15. Naber PA, Witter MP, Lopez da Silva FH. 1999 Perirhinal cortex input to the hippocampus in the rat: evidence for parallel pathways, both direct and indirect. A combined physiological and anatomical study. Eur. J. Neurosci. 11, 4119-4133. (doi:10. 1046/j.1460-9568.1999.00835.x)
16. Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AH. 1989 Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog. Neurobiol. 33, 161-253. (doi:10.1016/0301-0082(89)90009-9)
17. Dolorfo CL, Amaral DG. 1998 Entorhinal cortex of the rat: topographic organization of the cells of origin of the perforant path projection to the dentate gyrus. J. Comp. Neurol. 398, 25-48. (doi:10.1002/(SICI)1096-9861(19980817)398: 1,25::AID-CNE3.3.0.CO;2-B)
18. Fyhn M, Molden S, Witter MP, Moser EI, Moser M-B. 2004 Spatial representation in the entorhinal cortex. Science 305, 1258-1264. (doi:10.1126/science. 1099901)
19. Hafting T, Fyhn M, Molden S, Moser M-B, Moser EI. 2005 Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801-806. (doi:10.1038/nature03721)
20. Stensola H, Stensola T, Solstad T, Frøland K, Moser MB, Moser EI. 2012 The entorhinal grid map is discretized. Nature 492, 72-78. (doi:10.1038/ nature11649)
21. Taube JS, Muller RU, Ranck Jr JB. 1990 Headdirection cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10, 420-435.
22. Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser M-B, Moser EI. 2006 Conjunctive representation of position, direction and velocity in entorhinal cortex. Science 312, 754-758. (doi:10. 1126/science.1125572)
23. Boccara CN, Sargolini F, Thoresen VH, Solstad T, Witter MP, Moser EI, Moser M-B. 2010 Grid cells in pre-and parasubiculum. Nat. Neurosci. 13, 987-994. (doi:10.1038/nn.2602)
24. Savelli F, Yoganarasimha D, Knierim JJ. 2008 Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18, 1270-1282. (doi:10.1002/ hipo.20511)
25. Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI. 2008 Representation of geometric borders in the entorhinal cortex. Science 322, 1865-1868. (doi:10. 1126/science.1166466)
26. Varga C, Lee SY, Soltesz I. 2010 Target-selective GABAergic control of entorhinal cortex output. Nat. Neurosci. 13, 822-824. (doi:10.1038/nn.2570)
27. Zhang SJ, Ye J, Miao C, Tsao A, Cerniauskas I, Ledergerber D, Moser M-B, Moser EI. 2013 Optogenetic dissection of entorhinal-hippocampal functional connectivity. Science 340, 1232627. (doi:10.1126/science.1232627)
28. Moser EI, Krobert KA, Moser M-B, Morris RGM. 1998 Saturation of long-term potentiation does impair spatial learning. Science 281, 2038-2042. (doi:10. 1126/science.281.5385.2038)
29. Gradinaru V, Zhang F, Ramakrishnan C, Mattis J, Prakash R, Diester I, Goshen I, Thompson KR, Deisseroth K. 2010 Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141, 154-165. (doi:10.1016/j. cell.2010.02.037)
30. Nagel G, Brauner M, Liewald JF, Adeishvili N, Bamberg E, Gottschalk A. 2005 Millisecondtimescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263-1268. (doi:10.1038/nn1525)
31. Dhillon A, Jones RS. 2000 Laminar differences in recurrent excitatory transmission in the rat entorhinal cortex in vitro. Neuroscience 99, 413-422. (doi:10.1016/S0306-4522(00)00225-6)
32. Couey JJ et al. 2013 Recurrent inhibitory circuitry as a mechanism for grid formation. Nat. Neurosci. 16, 318-324. (doi:10.1038/nn.3310)
33. Pastoll H, Solanka L, van Rossum MC, Nolan MF. 2013 Feedback inhibition enables u-nested g-oscillations and grid firing fields. Neuron 77, 141-154. (doi:10.1016/j.neuron.2012.11.032)
34. Arenkiel BR, Peca J, Davison IG, Feliciano C, Deisseroth K, Augustine GJ, Ehlers MD, Feng G. 2007 In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54, 205-218. (doi:10.1016/j.neuron. 2007.03.005)
35. Petreanu L, Huber D, Sobczyk A, Svoboda K. 2007 Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat. Neurosci. 10, 663-668. (doi:10.1038/nn1891)
36. Huber D, Petreanu L, Ghitani N, Ranade S, Hromádka T, Mainen Z, Svoboda K. 2008 Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice. Nature 451, 61-64. (doi:10.1038/nature06445)
37. Wang H et al. 2007 High-speed mapping of synaptic connectivity using photostimulation in channelrhodopsin-2 transgenic mice. Proc. Natl Acad. Sci. USA 104, 8143-8148. (doi:10.1073/pnas. 0700384104)
38. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI. 2009 Driving fastspiking cells induces gamma rhythm and controls sensory responses. Nature 459, 663-667. (doi:10. 1038/nature08002)
39. O'Keefe J, Burgess N. 2005 Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells. Hippocampus 15, 853-866. (doi:10.1002/ hipo.20115)
40. Fuhs MC, Touretzky DS. 2006 A spin glass model of path integration in rat medial entorhinal cortex. J. Neurosci. 26, 4266-4276. (doi:10.1523/ JNEUROSCI.4353-05.2006)
41. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser M-B. 2006 Path integration and the neural basis of the 'cognitive map'. Nat. Rev. Neurosci. 7, 663-678. (doi:10.1038/nrn1932)
42. Solstad T, Moser EI, Einevoll GT. 2006 From grid cells to place cells: a mathematical model. Hippocampus 16, 1026-1031. (doi:10.1002/ hipo.20244)
43. Molter C, Yamaguchi Y. 2008 Entorhinal theta phase precession sculpts dentate gyrus place fields. Hippocampus 18, 919-930. (doi:10.1002/ hipo.20450)
44. Rolls ET, Stringer SM, Ellio T. 2006 Entorhinal cortex grid cells can map to hippocampal place cells by competitive learning. Network 17, 447-465. (doi:10.1080/09548980601064846)
45. Si B, Treves A. 2009 The role of competitive learning in the generation of DG fields from EC inputs. Cogn. Neurodyn. 3, 177-187. (doi:10.1007/s11571-009-9079-z)
46. Savelli F, Knierim JJ. 2010 Hebbian analysis of the transformation of medial entorhinal gridcell inputs to hippocampal place fields. J. Neurophysiol. 103, 3167-3183. (doi:10.1152/ jn.00932.2009)
47. de Almedia L, Idiart M, Lisman JE. 2009 The input-output transformation of the hippocampal granule cells: from grid cells to place cells. J. Neurosci. 29, 7504-7512. (doi:10.1523/ JNEUROSCI.6048-08.2009)
48. Monaco JD, Abbott LF. 2011 Modular reealignment of entorhinal grid cell activity as a basis for hippocampal remapping. J. Neurosci. 31, 9414-9425. (doi:10.1523/JNEUROSCI. 1433-11.2011)
49. Lee D, Lin BJ, Lee AK. 2012 Hippocampal place fields emerge upon single-cell manipulation of excitability during behavior. Science 337, 849-853. (doi:10.1126/science.1221489)
50. Jia H, Rochefort NL, Konnerth A. 2010 Dendritic organization of sensory input to cortical neurons in vivo. Nature 464, 1307-1312. (doi:10.1038/ nature08947)
51. Chen X, Leischner U, Rochefort NL, Nelken I, Konnerth A. 2011 Functional mapping of single spines in cortical neurons in vivo. Nature 475, 502-505. (doi:10.1038/nature10193)
52. O'Keefe J. 1976 Place units in the hippocampus of the freely moving rat. Exp. Neurol. 51, 78-109. (doi:10.1016/0014-4886(76)90055-8)
53. O'Keefe J, Burgess N. 1996 Geometric determinants of the place fields of hippocampal neurons. Nature 381, 425-428. (doi:10.1038/381425a0)
54. Hartley T, Burgess N, Lever C, Cacucci F, O'Keefe J. 2000 Modeling place fields in terms of the cortical inputs to the hippocampus. Hippocampus 10, 369-379. (doi:10.1002/1098-1063(2000)10: 4,369::AID-HIPO3.3.0.CO;2-0)
55. Barry C, Lever C, Hayman R, Hartley T, Burton S, O'Keefe J, Jeffery K, Burgess N. 2006 The boundary vector cell model of place cell firing and spatial memory. Rev. Neurosci. 17, 71-97. (doi:10.1515/ REVNEURO.2006.17.1-2.71)
56. Langston RF, Ainge JA, Couey JJ, Canto CB, Bjerknes TL, Witter MP, Moser EI, Moser MB. 2010 Development of the spatial representation system in the rat. Science 328, 1576-1580. (doi:10.1126/ science.1188210)
57. Wills TJ, Cacucci F, Burgess N, O'Keefe J. 2010 Development of the hippocampal cognitive map in preweanling rats. Science 328, 1573-1576. (doi:10. 1126/science.1188224)
58. Koenig J, Linder AN, Leutgeb JK, Leutgeb S. 2011 The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science 332, 592-595. (doi:10.1126/science.1201685)
59. Giocomo LM, Moser MB, Moser EI. 2011 Computational models of grid cells. Neuron 71, 589-603. (doi:10.1016/j.neuron.2011.07.023)
60. Burgess N, O'Keefe J. 2011 Models of place and grid cell firing and theta rhythmicity. Curr. Opin. Neurobiol. 21, 734-744. (doi:10.1016/j.conb.2011. 07.002)
61. Gothard KM, Skaggs WE, McNaughton BL. 1996 Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J. Neurosci. 16, 8027-8040.
62. Terrazas A, Krause M, Lipa P, Gothard KM, Barnes CA, McNaughton BL. 2005 Self-motion and the hippocampal spatial metric. J. Neurosci. 25, 8085-8096. (doi:10.1523/JNEUROSCI.0693-05.2005)
63. Marshel JH, Mori T, Nielsen KJ, Callaway EM. 2010 Targeting single neuronal networks for gene expression and cell labeling in vivo. Neuron 67, 562-574. (doi:10.1016/j.neuron.2010.08.001)
64. Schmidt-Hieber C, Häusser M. 2013 Cellular mechanisms of spatial navigation in the medial entorhinal cortex. Nat. Neurosci. 16, 325-331. (doi:10.1038/nn.3340)
65. Domnisoru C, Kinkhabwala AA, Tank DW. 2013 Membrane potential dynamics of grid cells. Nature 495, 199-204. (doi:10.1038/nature11973)