Topography of Place Maps along the CA3-to-CA2 Axis of the Hippocampus

Neuron

Volumn 87, Issue 5, 2015, Pages 1078-1092

  Lu, Li ^a   Igarashi, Kei M ^a   Witter, Menno P ^a   Moser, Edvard I ^a   Moser, May Britt ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN MAPPING; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; HISTOLOGY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; ACTION POTENTIAL; ANALYSIS OF VARIANCE; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; ELECTROSTIMULATION; FEEDING BEHAVIOR; FOOD DEPRIVATION; LONG EVANS RAT; NERVE CELL; NERVE CELL NETWORK; PHYSIOLOGY; SPATIAL ANALYSIS;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; BRAIN MAPPING; CA2 REGION, HIPPOCAMPAL; CA3 REGION, HIPPOCAMPAL; ELECTRIC STIMULATION; FEEDING BEHAVIOR; FOOD DEPRIVATION; MALE; MODELS, NEUROLOGICAL; NERVE NET; NEURONS; RATS; RATS, LONG-EVANS; SPATIAL ANALYSIS;

EID: 84940611594     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.07.007     Document Type: Article

References (70)

1. Alme C.B., Miao C., Jezek K., Treves A., Moser E.I., Moser M.B. Place cells in the hippocampus: eleven maps for eleven rooms. Proc. Natl. Acad. Sci. USA 2014, 111:18428-18435.
2. Anderson M.I., Jeffery K.J. Heterogeneous modulation of place cell firing by changes in context. J. Neurosci. 2003, 23:8827-8835.
3. Battaglia F.P., Treves A. Stable and rapid recurrent processing in realistic autoassociative memories. Neural Comput. 1998, 10:431-450.
4. Boccara C.N., Kjonigsen L.J., Hammer I.M., Bjaalie J.G., Leergaard T.B., Witter M.P. A three-plane architectonic atlas of the rat hippocampal region. Hippocampus 2015, 25:838-857.
5. 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.
6. Buckmaster P.S., Strowbridge B.W., Schwartzkroin P.A. A comparison of rat hippocampal mossy cells and CA3c pyramidal cells. J. Neurophysiol. 1993, 70:1281-1299.
7. Burke S.N., Maurer A.P., Nematollahi S., Uprety A.R., Wallace J.L., Barnes C.A. The influence of objects on place field expression and size in distal hippocampal CA1. Hippocampus 2011, 21:783-801.
8. Cappaert N.L., Van Strien N.M., Witter M.P. Hippocampal formation. The Rat Nervous System 2015, 511-574. Elsevier, London. G. Paxinos (Ed.).
9. Chevaleyre V., Siegelbaum S.A. Strong CA2 pyramidal neuron synapses define a powerful disynaptic cortico-hippocampal loop. Neuron 2010, 66:560-572.
10. Colgin L.L., Moser E.I., Moser M.B. Understanding memory through hippocampal remapping. Trends Neurosci. 2008, 31:469-477.
11. Couey J.J., Witoelar A., Zhang S.J., Zheng K., Ye J., Dunn B., Czajkowski R., Moser M.B., Moser E.I., Roudi Y., Witter M.P. Recurrent inhibitory circuitry as a mechanism for grid formation. Nat. Neurosci. 2013, 16:318-324.
12. Deshmukh S.S., Knierim J.J. Representation of non-spatial and spatial information in the lateral entorhinal cortex. Front. Behav. Neurosci. 2011, 5:69.
13. Fenton A.A., Muller R.U. Place cell discharge is extremely variable during individual passes of the rat through the firing field. Proc. Natl. Acad. Sci. USA 1998, 95:3182-3187.
14. 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.
15. Gray C.M., Maldonado P.E., Wilson M., McNaughton B. Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex. J. Neurosci. Methods 1995, 63:43-54.
16. 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.
17. Haglund L., Swanson L.W., Köhler C. The projection of the supramammillary nucleus to the hippocampal formation: an immunohistochemical and anterograde transport study with the lectin PHA-L in the rat. J. Comp. Neurol. 1984, 229:171-185.
18. Hargreaves E.L., Rao G., Lee I., Knierim J.J. Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 2005, 308:1792-1794.
19. Hasselmo M.E., Schnell E., Barkai E. Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3. J. Neurosci. 1995, 15:5249-5262.
20. Henriksen E.J., Colgin L.L., Barnes C.A., Witter M.P., Moser M.B., Moser E.I. Spatial representation along the proximodistal axis of CA1. Neuron 2010, 68:127-137.
21. Hitti F.L., Siegelbaum S.A. The hippocampal CA2 region is essential for social memory. Nature 2014, 508:88-92.
22. Hunsaker M.R., Rosenberg J.S., Kesner R.P. The role of the dentate gyrus, CA3a,b, and CA3c for detecting spatial and environmental novelty. Hippocampus 2008, 18:1064-1073.
23. Igarashi K.M., Lu L., Colgin L.L., Moser M.B., Moser E.I. Coordination of entorhinal-hippocampal ensemble activity during associative learning. Nature 2014, 510:143-147.
24. Ishizuka N., Weber J., Amaral D.G. Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J. Comp. Neurol. 1990, 295:580-623.
25. Ishizuka N., Cowan W.M., Amaral D.G. A quantitative analysis of the dendritic organization of pyramidal cells in the rat hippocampus. J. Comp. Neurol. 1995, 362:17-45.
26. Jones M.W., McHugh T.J. Updating hippocampal representations: CA2 joins the circuit. Trends Neurosci. 2011, 34:526-535.
27. Jung M.W., McNaughton B.L. Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 1993, 3:165-182.
28. Jung M.W., Wiener S.I., McNaughton B.L. Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J. Neurosci. 1994, 14:7347-7356.
29. Kjelstrup K.B., Solstad T., Brun V.H., Hafting T., Leutgeb S., Witter M.P., Moser E.I., Moser M.B. Finite scale of spatial representation in the hippocampus. Science 2008, 321:140-143.
30. Knierim J.J., Zhang K. Attractor dynamics of spatially correlated neural activity in the limbic system. Annu. Rev. Neurosci. 2012, 35:267-285.
31. Kohara K., Pignatelli M., Rivest A.J., Jung H.Y., Kitamura T., Suh J., Frank D., Kajikawa K., Mise N., Obata Y., et al. Cell type-specific genetic and optogenetic tools reveal hippocampal CA2 circuits. Nat. Neurosci. 2014, 17:269-279.
32. Lee I., Yoganarasimha D., Rao G., Knierim J.J. Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 2004, 430:456-459.
33. 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 2015, 87:1093-1105. this issue.
34. Lein E.S., Callaway E.M., Albright T.D., Gage F.H. Redefining the boundaries of the hippocampal CA2 subfield in the mouse using gene expression and 3-dimensional reconstruction. J. Comp. Neurol. 2005, 485:1-10.
35. Leutgeb S., Leutgeb J.K., Treves A., Moser M.B., Moser E.I. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 2004, 305:1295-1298.
36. Leutgeb J.K., Leutgeb S., Treves A., Meyer R., Barnes C.A., McNaughton B.L., Moser M.B., Moser E.I. Progressive transformation of hippocampal neuronal representations in "morphed" environments. Neuron 2005, 48:345-358.
37. 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.
38. Leutgeb J.K., Leutgeb S., Moser M.B., Moser E.I. Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 2007, 315:961-966.
39. Li X.G., Somogyi P., Ylinen A., Buzsáki G. The hippocampal CA3 network: an in vivo intracellular labeling study. J. Comp. Neurol. 1994, 339:181-208.
40. Lorente de Nó R. Studies of the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J. Psychol. Neurol. 1934, 46:113-177.
41. 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.
42. Mankin E.A., Diehl G.W., Sparks F.T., Leutgeb S., Leutgeb J.K. Hippocampal CA2 activity patterns change over time to a larger extent than between spatial contexts. Neuron 2015, 85:190-201.
43. Markus E.J., Qin Y.L., Leonard B., Skaggs W.E., McNaughton B.L., Barnes C.A. Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J. Neurosci. 1995, 15:7079-7094.
44. Marr D. Simple memory: a theory for archicortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1971, 262:23-81.
45. Marrone D.F., Satvat E., Odintsova I.V., Gheidi A. Dissociation of spatial representations within hippocampal region CA3. Hippocampus 2014, 24:1417-1420.
46. McNaughton B.L., Morris R.G.M. Hippocampal synaptic enhancement and information-storage within a distributed memory system. Trends Neurosci. 1987, 10:408-415.
47. McNaughton B.L., Nadel L. Hebb-Marr networks and the neurobiological representation of action in space. Neuroscience and Connectionist Theory 1990, 1-63. L. Erlbaum Associates, Hillsdale, N.J. M.A. Gluck, D.E. Rumelhart (Eds.).
48. Moser E.I., Kropff E., Moser M.B. Place cells, grid cells, and the brain's spatial representation system. Annu. Rev. Neurosci. 2008, 31:69-89.
49. 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.
50. Naber P.A., Lopes da Silva F.H., Witter M.P. Reciprocal connections between the entorhinal cortex and hippocampal fields CA1 and the subiculum are in register with the projections from CA1 to the subiculum. Hippocampus 2001, 11:99-104.
51. Nakamura N.H., Flasbeck V., Maingret N., Kitsukawa T., Sauvage M.M. Proximodistal segregation of nonspatial information in CA3: preferential recruitment of a proximal CA3-distal CA1 network in nonspatial recognition memory. J. Neurosci. 2013, 33:11506-11514.
52. O'Keefe J., Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971, 34:171-175.
53. O'Keefe J., Nadel L. The Hippocampus as a Cognitive Map 1978, Clarendon Press, Oxford.
54. O'Reilly R.C., McClelland J.L. Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus 1994, 4:661-682.
55. Rolls E.T., Treves A. Neural Networks and Brain Function 1998, Oxford University Press, Oxford.
56. Romani S., Tsodyks M. Continuous attractors with morphed/correlated maps. PLoS Comput. Biol. 2010, 6. 10.1371/journal.pcbi.1000869.
57. Rowland D.C., Weible A.P., Wickersham I.R., Wu H., Mayford M., Witter M.P., Kentros C.G. Transgenically targeted rabies virus demonstrates a major monosynaptic projection from hippocampal area CA2 to medial entorhinal layer II neurons. J. Neurosci. 2013, 33:14889-14898.
58. Scharfman H.E. Evidence from simultaneous intracellular recordings in rat hippocampal slices that area CA3 pyramidal cells innervate dentate hilar mossy cells. J. Neurophysiol. 1994, 72:2167-2180.
59. Schmitzer-Torbert N., Jackson J., Henze D., Harris K., Redish A.D. Quantitative measures of cluster quality for use in extracellular recordings. Neuroscience 2005, 131:1-11.
60. Solstad T., Boccara C.N., Kropff E., Moser M.B., Moser E.I. Representation of geometric borders in the entorhinal cortex. Science 2008, 322:1865-1868.
61. Steffenach H.A., Sloviter R.S., Moser E.I., Moser M.B. Impaired retention of spatial memory after transection of longitudinally oriented axons of hippocampal CA3 pyramidal cells. Proc. Natl. Acad. Sci. USA 2002, 99:3194-3198.
62. Stevenson E.L., Caldwell H.K. Lesions to the CA2 region of the hippocampus impair social memory in mice. Eur. J. Neurosci. 2014, 40:3294-3301.
63. Tamamaki N., Abe K., Nojyo Y. Three-dimensional analysis of the whole axonal arbors originating from single CA2 pyramidal neurons in the rat hippocampus with the aid of a computer graphic technique. Brain Res. 1988, 452:255-272.
64. Treves A., Rolls E.T. Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus 1992, 2:189-199.
65. Tsao A., Moser M.B., Moser E.I. Traces of experience in the lateral entorhinal cortex. Curr. Biol. 2013, 23:399-405.
66. Vazdarjanova A., Guzowski J.F. Differences in hippocampal neuronal population responses to modifications of an environmental context: evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles. J. Neurosci. 2004, 24:6489-6496.
67. Wilson M.A., McNaughton B.L. Dynamics of the hippocampal ensemble code for space. Science 1993, 261:1055-1058.
68. Wood E.R., Dudchenko P.A., Eichenbaum H. The global record of memory in hippocampal neuronal activity. Nature 1999, 397:613-616.
69. 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.
70. Zhao M., Choi Y.S., Obrietan K., Dudek S.M. Synaptic plasticity (and the lack thereof) in hippocampal CA2 neurons. J. Neurosci. 2007, 27:12025-12032.