Spatial Maps in the Entorhinal Cortex and Adjacent Structures

Chapter

Abstract

This chapter presents an introductory overview on grid cells and other cell types in the entorhinal cortex and adjacent regions, which are believed to be part of the brain’s representation of space. Grid cells, which have been discovered only recently, are thought to be part of a class of cells in the mammalian hippocampal and parahippocampal cortices which are involved in the cognitive mapping of the spatial environment. These cells include also place cells, head-direction cells, and border cells. In this chapter, we shall portray the phenomenological characteristics of the recently discovered grid cells and compare them to the other types of mapping-related cells in hippocampal and parahippocampal regions.

References

  1. Barnes CA, McNaughton BL, Mizumori SJ, Leonard BW, Lin LH (1990) Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. Prog Brain Res 83:287–300PubMedCrossRefGoogle Scholar
  2. 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 17:71–97PubMedCentralPubMedCrossRefGoogle Scholar
  3. Barry C, Hayman R, Burgess N, Jeffery KJ (2007) Experience-dependent rescaling of entorhinal grids. Nat Neurosci 10:682–684PubMedCrossRefGoogle Scholar
  4. Best PJ, White AM, Minai A (2001) Spatial processing in the brain: the activity of hippocampal place cells. Annu Rev Neurosci 24:459–486PubMedCrossRefGoogle Scholar
  5. Boccara CN, Sargolini F, Thoresen VH, Solstad T, Witter MP, Moser EI, Moser M-B (2010) Grid cells in pre- and parasubiculum. Nat Neurosci 13:987–994PubMedCrossRefGoogle Scholar
  6. Bonnevie T, Dunn B, Fyhn M, Hafting T, Derdikman D, Kubie JL, Roudi Y, Moser EI, Moser M-B (2013) Grid cells require excitatory drive from the hippocampus. Nat Neurosci 16:309–317PubMedCrossRefGoogle Scholar
  7. Brandon MP, Bogaard AR, Libby CP, Connerney MA, Gupta K, Hasselmo ME (2011) Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science 332:595–599PubMedCentralPubMedCrossRefGoogle Scholar
  8. Brun VH, Otnass MK, Molden S, Steffenach H-A, Witter MP, Moser M-B, Moser EI (2002) Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296:2243–2246PubMedCrossRefGoogle Scholar
  9. Brun VH, Solstad T, Kjelstrup KB, Fyhn M, Witter MP, Moser EI, Moser M-B (2008) Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex. Hippocampus 18:1200–1212PubMedCrossRefGoogle Scholar
  10. Burgalossi A, Herfst L, von Heimendahl M, Förste H, Haskic K, Schmidt M, Brecht M (2011) Microcircuits of functionally identified neurons in the rat medial entorhinal cortex. Neuron 70:773–786PubMedCrossRefGoogle Scholar
  11. Buzsaki G (2002) Theta oscillations in the hippocampus. Neuron 33:325–340PubMedCrossRefGoogle Scholar
  12. Buzsáki G, Moser EI (2013) Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 16:130–138PubMedCrossRefGoogle Scholar
  13. Couey JJ, Witoelar A, Zhang S-J, Zheng K, Ye J, Dunn B, Czajkowski R, Moser M-B, Moser EI, Roudi Y (2013) Recurrent inhibitory circuitry as a mechanism for grid formation. Nat Neurosci 16:318–324PubMedCrossRefGoogle Scholar
  14. Derdikman D (2009) Are the boundary-related cells in the subiculum boundary-vector cells? J Neurosci 29:13429–13431PubMedCrossRefGoogle Scholar
  15. Derdikman D, Whitlock JR, Tsao A, Fyhn M, Hafting T, Moser M-B, Moser EI (2009) Fragmentation of grid cell maps in a multicompartment environment. Nat Neurosci 12:1325–1332PubMedCrossRefGoogle Scholar
  16. Deshmukh SS (2014) Spatial and nonspatial representations in the lateral entorhinal cortex. In: Derdikman D, Knierim JJ (eds) Space, time and memory in the hippocampal formation. Springer, HeidelbergGoogle Scholar
  17. Dolorfo CL, Amaral DG (1998) Entorhinal cortex of the rat: organization of intrinsic connections. J Comp Neurol 398:49–82PubMedCrossRefGoogle Scholar
  18. Eichenbaum H, MacDonald CJ, Kraus BJ (2014) Time and the hippocampus. In: Derdikman D, Knierim JJ (eds) Space, time and memory in the hippocampal formation. Springer, HeidelbergGoogle Scholar
  19. Frank LM, Brown EN, Wilson M (2000) Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27:169–178PubMedCrossRefGoogle Scholar
  20. Frank LM, Brown EN, Wilson MA (2001) A comparison of the firing properties of putative excitatory and inhibitory neurons from CA1 and the entorhinal cortex. J Neurophysiol 86:2029–2040PubMedGoogle Scholar
  21. Fyhn M, Molden S, Witter MP, Moser EI, Moser MB (2004) Spatial representation in the entorhinal cortex. Science 305:1258–1264PubMedCrossRefGoogle Scholar
  22. Fyhn M, Hafting T, Treves A, Moser MB, Moser EI (2007) Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446:190–194PubMedCrossRefGoogle Scholar
  23. Giocomo LM, Hussaini SA, Zheng F, Kandel ER, Moser M-B, Moser EI (2011) Grid cells use HCN1 channels for spatial scaling. Cell 147:1159–1170PubMedCrossRefGoogle Scholar
  24. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–806PubMedCrossRefGoogle Scholar
  25. Hafting T, Fyhn M, Bonnevie T, Moser MB, Moser EI (2008) Hippocampus-independent phase precession in entorhinal grid cells. Nature 453:1248–1252PubMedCrossRefGoogle Scholar
  26. Hargreaves EL, Rao G, Lee I, Knierim JJ (2005) Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 308:1792–1794PubMedCrossRefGoogle Scholar
  27. 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 10:369–379PubMedCrossRefGoogle Scholar
  28. Jezek K, Henriksen EJ, Treves A, Moser EI, Moser M-B (2011) Theta-paced flickering between place-cell maps in the hippocampus. Nature 478:246–249PubMedCrossRefGoogle Scholar
  29. Jung MW, Wiener SI, McNaughton BL (1994) Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J Neurosci 14:7347–7356PubMedGoogle Scholar
  30. Kjelstrup KB, Solstad T, Brun VH, Hafting T, Leutgeb S, Witter MP, Moser EI, Moser MB (2008) Finite scale of spatial representation in the hippocampus. Science 321:140–143PubMedCrossRefGoogle Scholar
  31. Koenig J, Linder AN, Leutgeb JK, Leutgeb S (2011) The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science 332:592–595PubMedCrossRefGoogle Scholar
  32. Langston RF, Ainge JA, Couey JJ, Canto CB, Bjerknes TL, Witter MP, Moser EI, Moser M-B (2010) Development of the spatial representation system in the rat. Science 328:1576–1580PubMedCrossRefGoogle Scholar
  33. Las L, Ulanovsky N (2014) Hippocampal neurophysiology across species. In: Derdikman D, Knierim JJ (eds) Space, time and memory in the hippocampal formation. Springer, HeidelbergGoogle Scholar
  34. Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, Moser MB (2005) Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309:619–623PubMedCrossRefGoogle Scholar
  35. Lever C, Burton S, Jeewajee A, O’Keefe J, Burgess N (2009) Boundary vector cells in the subiculum of the hippocampal formation. J Neurosci 29:9771–9777PubMedCentralPubMedCrossRefGoogle Scholar
  36. Lever C, Kaplan R, Burgess N (2014) The function of oscillations in the hippocampal formation. In: Derdikman D, Knierim JJ (eds) Space, time and memory in the hippocampal formation. Springer, HeidelbergGoogle Scholar
  37. Lu L, Leutgeb JK, Tsao A, Henriksen EJ, Leutgeb S, Barnes CA, Witter MP, Moser M-B, Moser EI (2013) Impaired hippocampal rate coding after lesions of the lateral entorhinal cortex. Nat Neurosci 16:1085–1093PubMedCrossRefGoogle Scholar
  38. Mathis A, Herz A, Stemmler M (2012) Optimal population codes for space: grid cells outperform place cells. Neural Comput 24:2280–2317PubMedCrossRefGoogle Scholar
  39. Mcnaughton BL, Barnes CA, Meltzer J, Sutherland RJ (1989) Hippocampal granule cells are necessary for normal spatial-learning but not for spatially-selective pyramidal cell discharge. Exp Brain Res 76:485–496PubMedCrossRefGoogle Scholar
  40. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB (2006) Path integration and the neural basis of the ‘cognitive map’. Nat Rev Neurosci 7:663–678PubMedCrossRefGoogle Scholar
  41. Monaco JD, Abbott LF (2011) Modular realignment of entorhinal grid cell activity as a basis for hippocampal remapping. J Neurosci 31:9414–9425PubMedCentralPubMedCrossRefGoogle Scholar
  42. Navratilova Z, McNaughton BL (2014) Models of path integration in the hippocampal complex. In: Derdikman D, Knierim JJ (eds) Space, time and memory in the hippocampal formation. Springer, HeidelbergGoogle Scholar
  43. Neunuebel JP, Yoganarasimha D, Rao G, Knierim JJ (2013) Conflicts between local and global spatial frameworks dissociate neural representations of the lateral and medial entorhinal cortex. J Neurosci 33:9246–9258PubMedCentralPubMedCrossRefGoogle Scholar
  44. O’Keefe J, Burgess N (1996) Geometric determinants of the place fields of hippocampal neurons. Nature 381:425–428PubMedCrossRefGoogle Scholar
  45. O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Clarendon Press/Oxford University Press, Oxford/New YorkGoogle Scholar
  46. O’Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317–330PubMedCrossRefGoogle Scholar
  47. Pastalkova E, Itskov V, Amarasingham A, Buzsaki G (2008) Internally generated cell assembly sequences in the rat hippocampus. Science 321:1322–1327PubMedCentralPubMedCrossRefGoogle Scholar
  48. Quirk GJ, Muller RU, Kubie JL, Ranck JB Jr (1992) The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells. J Neurosci 12:1945–1963PubMedGoogle Scholar
  49. Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser MB, Moser EI (2006) Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312:758–762PubMedCrossRefGoogle Scholar
  50. Savelli F, Knierim JJ (2010) Hebbian analysis of the transformation of medial entorhinal grid-cell inputs to hippocampal place fields. J Neurophysiol 103:3167–3183PubMedCentralPubMedCrossRefGoogle Scholar
  51. Savelli F, Yoganarasimha D, Knierim JJ (2008) Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18:1270–1282PubMedCentralPubMedCrossRefGoogle Scholar
  52. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA (1996) Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6:149–172PubMedCrossRefGoogle Scholar
  53. Solstad T, Moser EI, Einevoll GT (2006) From grid cells to place cells: a mathematical model. Hippocampus 16:1026–1031PubMedCrossRefGoogle Scholar
  54. Solstad T, Boccara C, Kropff E, Moser MB, Moser EI (2008) Representation of geometric borders in the entorhinal cortex. Science 322:1865–1868PubMedCrossRefGoogle Scholar
  55. Stensola H, Stensola T, Solstad T, Frøland K, Moser M-B, Moser EI (2012) The entorhinal grid map is discretized. Nature 492:72–78PubMedCrossRefGoogle Scholar
  56. Stensola T, Stensola H, Moser M-B, Moser EI (2013) Environmental constraints on grid cell orientation. Soc Neurosci Abstr 769.15Google Scholar
  57. Taube JS, Muller RU, Ranck JB (1990) Head-direction cells recorded from the postsubiculum in freely moving rats.1. Description and quantitative-analysis. J Neurosci 10:420–435PubMedGoogle Scholar
  58. Tolman EC (1948) Cognitive maps in rats and men. Psychol Rev 55:189–208PubMedCrossRefGoogle Scholar
  59. Van Cauter T, Poucet B, Save E (2008) Unstable CA1 place cell representation in rats with entorhinal cortex lesions. Eur J Neurosci 27:1933–1946PubMedCrossRefGoogle Scholar
  60. Van Cauter T, Camon J, Alvernhe A, Elduayen C, Sargolini F, Save E (2012) Distinct roles of medial and lateral entorhinal cortex in spatial cognition. Cereb Cortex 23:451–459PubMedCrossRefGoogle Scholar
  61. Vanderwolf CH (1969) Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407–418PubMedCrossRefGoogle Scholar
  62. Vanderwolf CH, Kramis R, Robinson TE (1977) Hippocampal electrical activity during waking behaviour and sleep: analyses using centrally acting drugs. Ciba Found Symp (58) 199–226Google Scholar
  63. Whitlock JR, Derdikman D (2012) Head direction maps remain stable despite grid map fragmentation. Front Neural Circuits 6:9PubMedCentralPubMedCrossRefGoogle Scholar
  64. Widloski J, Fiete I (2014) How does the brain solve the computational problems of spatial navigation? In: Derdikman D, Knierim JJ (eds) Space, time and memory in the hippocampal formation. Springer, HeidelbergGoogle Scholar
  65. Wills TJ, Cacucci F, Burgess N, O’Keefe J (2010) Development of the hippocampal cognitive map in preweanling rats. Science 328:1573–1576PubMedCentralPubMedCrossRefGoogle Scholar
  66. Wilson MA, McNaughton BL (1993) Dynamics of the hippocampal ensemble code for space. Science 261:1055–1058PubMedCrossRefGoogle Scholar
  67. Witter MP, Amaral DG (2004) Hippocampal formation. In: Paxinos G (ed) The rat nervous system. Elsevier, San Diego, CA, pp 635–704Google Scholar
  68. 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 33:161–253PubMedCrossRefGoogle Scholar
  69. Wood ER, Dudchenko PA, Eichenbaum H (1999) The global record of memory in hippocampal neuronal activity. Nature 397:613–616PubMedCrossRefGoogle Scholar
  70. Wood ER, Agster KM, Eichenbaum H (2004) One-trial odor-reward association: a form of event memory not dependent on hippocampal function. Behav Neurosci 118:526–539PubMedCrossRefGoogle Scholar
  71. Yartsev M, Witter M, Ulanovsky N (2011) Grid cells without theta oscillations in the entorhinal cortex of bats. Nature 479:103–107PubMedCrossRefGoogle Scholar
  72. Yoon K, Buice MA, Barry C, Hayman R, Burgess N, Fiete IR (2013) Specific evidence of low-dimensional continuous attractor dynamics in grid cells. Nat Neurosci 16:1077–1084PubMedCentralPubMedCrossRefGoogle Scholar
  73. 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 340:1232627PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  1. 1.Rappaport Faculty of MedicineTechnion—Israel Institute of TechnologyBat-GalimIsrael
  2. 2.Kavli Institute for Systems Neuroscience and Centre for Neural ComputationNorwegian University of Science and Technology (NTNU)TrondheimNorway

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