Oscillatory dynamics and place field maps reflect hippocampal ensemble processing of sequence and place memory under NMDA receptor control

Neuron

Volumn 81, Issue 2, 2014, Pages 402-415

  Cabral, Henrique O ^a,b,c,d   Vinck, Martin ^a,b   Fouquet, Celine ^e,g   Pennartz, Cyriel M A ^a,b   Rondi Reig, Laure ^e,g   Battaglia, Francesco P ^a,b,c,d,f  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b Cognitive Sciences Center Amsterdam ^*  (Netherlands)

^c Belgium   (Belgium)

^d RADBOUD UNIVERSITY   (Netherlands)

^e SORBONNE UNIVERSITÉ   (France)

^f DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^g and Centre National de la Recherche Scientifique Unité Mixte de Recherche 8246   (France)

Author keywords

[No Author keywords available]

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BEHAVIORAL SCIENCE; CELL FUNCTION; CONTROLLED STUDY; DYNAMICS; ENTORHINAL CORTEX; FOREBRAIN; GAMMA RHYTHM; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS THETA RHYTHM; INTERNEURON; KNOCKOUT MOUSE; LEARNING; MEMORY; MEMORY CONSOLIDATION; MOUSE; NONHUMAN; PLACE CELL; PLACE MEMORY; PRIORITY JOURNAL; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; SEQUENCE MEMORY; TASK PERFORMANCE;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; BIOLOGICAL CLOCKS; BRAIN WAVES; CARRIER PROTEINS; HIPPOCAMPUS; MAZE LEARNING; MEMORY; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURONS; NONLINEAR DYNAMICS; PATCH-CLAMP TECHNIQUES; SERIAL LEARNING; SPACE PERCEPTION; SPECTRUM ANALYSIS;

EID: 84892691022     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.11.010     Document Type: Article

References (64)

1. Bannerman D.M., Good M.A., Butcher S.P., Ramsay M., Morris R.G. Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature 1995, 378:182-186.
2. Battaglia F.P., Kalenscher T., Cabral H., Winkel J., Bos J., Manuputy R., van Lieshout T., Pinkse F., Beukers H., Pennartz C. The Lantern: an ultra-light micro-drive for multi-tetrode recordings in mice and other small animals. J. Neurosci. Methods 2009, 178:291-300.
3. Belluscio M.A., Mizuseki K., Schmidt R., Kempter R., Buzsáki G. Cross-frequency phase-phase coupling between θ and γ oscillations in the hippocampus. J. Neurosci. 2012, 32:423-435.
4. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
5. Bragin A., Jandó G., Nádasdy Z., Hetke J., Wise K., Buzsáki G. Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci. 1995, 15:47-60.
6. Brun V.H., Otnass M.K., Molden S., Steffenach H.A., Witter M.P., Moser M.B., Moser E.I. Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 2002, 296:2243-2246.
7. Brun V.H., Leutgeb S., Wu H.Q., Schwarcz R., Witter M.P., Moser E.I., Moser M.B. Impaired spatial representation in CA1 after lesion of direct input from entorhinal cortex. Neuron 2008, 57:290-302.
8. Carlén M., Meletis K., Siegle J.H., Cardin J.A., Futai K., Vierling-Claassen D., Rühlmann C., Jones S.R., Deisseroth K., Sheng M., et al. A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior. Mol. Psychiatry 2012, 17:537-548.
9. Chance F.S. Hippocampal phase precession from dual input components. J. Neurosci. 2012, 32. 16693-703a.
10. Colgin L.L., Denninger T., Fyhn M., Hafting T., Bonnevie T., Jensen O., Moser M.B., Moser E.I. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 2009, 462:353-357.
11. de Almeida L., Idiart M., Lisman J.E. The input-output transformation of the hippocampal granule cells: from grid cells to place fields. J. Neurosci. 2009, 29:7504-7512.
12. Derdikman D., Whitlock J.R., Tsao A., Fyhn M., Hafting T., Moser M.-B.B., Moser E.I. Fragmentation of grid cell maps in a multicompartment environment. Nat. Neurosci. 2009, 12:1325-1332.
13. Deshmukh S.S., Yoganarasimha D., Voicu H., Knierim J.J. Theta modulation in the medial and the lateral entorhinal cortices. J. Neurophysiol. 2010, 104:994-1006.
14. Eichenbaum H. A cortical-hippocampal system for declarative memory. Nat. Rev. Neurosci. 2000, 1:41-50.
15. Fouquet C., Tobin C., Rondi-Reig L. A new approach for modeling episodic memory from rodents to humans: the temporal order memory. Behav. Brain Res. 2010, 215:172-179.
16. Fouquet C., Petit G.H., Auffret A., Gaillard E., Rovira C., Mariani J., Rondi-Reig L. Early detection of age-related memory deficits in individual mice. Neurobiol. Aging 2011, 32:1881-1895.
17. Fries P. A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn. Sci. 2005, 9:474-480.
18. Gilbert P.E., Kesner R.P. The role of the dorsal CA3 hippocampal subregion in spatial working memory and pattern separation. Behav. Brain Res. 2006, 169:142-149.
19. Gothard K.M., Skaggs W.E., McNaughton B.L. Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J. Neurosci. 1996, 16:8027-8040.
20. Gothard K.M., Skaggs W.E., Moore K.M., McNaughton B.L. Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J. Neurosci. 1996, 16:823-835.
21. 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.
22. Harris K.D., Henze D.A., Csicsvari J., Hirase H., Buzsáki G. Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. J. Neurophysiol. 2000, 84:401-414.
23. Hazan L., Zugaro M., Buzsáki G. Klusters, NeuroScope, NDManager: a free software suite for neurophysiological data processing and visualization. J. Neurosci. Methods 2006, 155:207-216.
24. Iglói K., Doeller C.F., Berthoz A., Rondi-Reig L., Burgess N. Lateralized human hippocampal activity predicts navigation based on sequence or place memory. Proc. Natl. Acad. Sci. USA 2010, 107:14466-14471.
25. Jackson J., Redish A.D. Network dynamics of hippocampal cell-assemblies resemble multiple spatial maps within single tasks. Hippocampus 2007, 17:1209-1229.
26. Kelemen E., Fenton A.A. Dynamic grouping of hippocampal neural activity during cognitive control of two spatial frames. PLoS Biol. 2010, 8:e1000403.
27. Korotkova T., Fuchs E.C., Ponomarenko A., von Engelhardt J., Monyer H. NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory. Neuron 2010, 68:557-569.
28. Lazarewicz M.T., Ehrlichman R.S., Maxwell C.R., Gandal M.J., Finkel L.H., Siegel S.J. Ketamine modulates theta and gamma oscillations. J. Cogn. Neurosci. 2010, 22:1452-1464.
29. Leão R.N., Mikulovic S., Leão K.E., Munguba H., Gezelius H., Enjin A., Patra K., Eriksson A., Loew L.M., Tort A.B., Kullander K. OLM interneurons differentially modulate CA3 and entorhinal inputs to hippocampal CA1 neurons. Nat. Neurosci. 2012, 15:1524-1530.
30. Lee I., Kesner R.P. Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. J. Neurosci. 2003, 23:1517-1523.
31. 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.
32. Lee I., Jerman T.S., Kesner R.P. Disruption of delayed memory for a sequence of spatial locations following CA1- or CA3-lesions of the dorsal hippocampus. Neurobiol. Learn. Mem. 2005, 84:138-147.
33. Lisman J.E., Jensen O. The θ-γ neural code. Neuron 2013, 77:1002-1016.
34. MacDonald C.J., Lepage K.Q., Eden U.T., Eichenbaum H. Hippocampal "time cells" bridge the gap in memory for discontiguous events. Neuron 2011, 71:737-749.
35. Maris E., Schoffelen J.M., Fries P. Nonparametric statistical testing of coherence differences. J. Neurosci. Methods 2007, 163:161-175.
36. Maurer A.P., Cowen S.L., Burke S.N., Barnes C.A., McNaughton B.L. Organization of hippocampal cell assemblies based on theta phase precession. Hippocampus 2006, 16:785-794.
37. McHugh T.J., Blum K.I., Tsien J.Z., Tonegawa S., Wilson M.A. Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice. Cell 1996, 87:1339-1349.
38. 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.
39. Middleton S., Jalics J., Kispersky T., Lebeau F.E., Roopun A.K., Kopell N.J., Whittington M.A., Cunningham M.O. NMDA receptor-dependent switching between different gamma rhythm-generating microcircuits in entorhinal cortex. Proc. Natl. Acad. Sci. USA 2008, 105:18572-18577.
40. Mizuseki K., Sirota A., Pastalkova E., Buzsáki G. Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 2009, 64:267-280.
41. Mizuseki K., Royer S., Diba K., Buzsáki G. Activity dynamics and behavioral correlates of CA3 and CA1 hippocampal pyramidal neurons. Hippocampus 2012, 22:1659-1680.
42. Montgomery S.M., Buzsáki G. Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance. Proc. Natl. Acad. Sci. USA 2007, 104:14495-14500.
43. Montgomery S.M., Betancur M.I., Buzsáki G. Behavior-dependent coordination of multiple theta dipoles in the hippocampus. J. Neurosci. 2009, 29:1381-1394.
44. Morris R.G., Anderson E., Lynch G.S., Baudry M. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 1986, 319:774-776.
45. Moser E.I., Moser M.-B. A metric for space. Hippocampus 2008, 18:1142-1156.
46. Nakashiba T., Young J.Z., McHugh T.J., Buhl D.L., Tonegawa S. Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning. Science 2008, 319:1260-1264.
47. Nakazawa K., Quirk M.C., Chitwood R.A., Watanabe M., Yeckel M.F., Sun L.D., Kato A., Carr C.A., Johnston D., Wilson M.A., Tonegawa S. Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 2002, 297:211-218.
48. O'Keefe J., Recce M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 1993, 3:317-330.
49. Packard M.G., McGaugh J.L. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol. Learn. Mem. 1996, 65:65-72.
50. Pastalkova E., Itskov V., Amarasingham A., Buzsáki G. Internally generated cell assembly sequences in the rat hippocampus. Science 2008, 321:1322-1327.
51. Reifenstein E.T., Kempter R., Schreiber S., Stemmler M.B., Herz A.V. Grid cells in rat entorhinal cortex encode physical space with independent firing fields and phase precession at the single-trial level. Proc. Natl. Acad. Sci. USA 2012, 109:6301-6306.
52. Rondi-Reig L., Petit G.H., Tobin C., Tonegawa S., Mariani J., Berthoz A. Impaired sequential egocentric and allocentric memories in forebrain-specific-NMDA receptor knock-out mice during a new task dissociating strategies of navigation. J. Neurosci. 2006, 26:4071-4081.
53. Royer S., Sirota A., Patel J., Buzsáki G. Distinct representations and theta dynamics in dorsal and ventral hippocampus. J. Neurosci. 2010, 30:1777-1787.
54. Schmidt R., Diba K., Leibold C., Schmitz D., Buzsáki G., Kempter R. Single-trial phase precession in the hippocampus. J. Neurosci. 2009, 29:13232-13241.
55. Shapiro M.L., Tanila H., Eichenbaum H. Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus 1997, 7:624-642.
56. Skaggs W.E., McNaughton B.L., Wilson M.A., Barnes C.A. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 1996, 6:149-172.
57. Treves A., Rolls E.T. Computational analysis of the role of the hippocampus in memory. Hippocampus 1994, 4:374-391.
58. Tsien J.Z., Chen D.F., Gerber D., Tom C., Mercer E.H., Anderson D.J., Mayford M., Kandel E.R., Tonegawa S. Subregion- and cell type-restricted gene knockout in mouse brain. Cell 1996, 87:1317-1326.
59. Tsien J.Z., Huerta P.T., Tonegawa S. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 1996, 87:1327-1338.
60. van Wingerden M., Vinck M.A., Tijms V., Ferreira I.R., Jonker A.J., Pennartz C.M.A. NMDA receptors control cue-outcome selectivity and plasticity of orbitofrontal firing patterns during associative stimulus-reward learning. Neuron 2012, 76:813-825.
61. Vinck M., van Wingerden M., Womelsdorf T., Fries P., Pennartz C. The pairwise phase consistency: a bias-free measure of rhythmic neural synchronization. Neuroimage 2010, 51:112-122.
62. Vinck M., Battaglia F.P., Womelsdorf T., Pennartz C. Improved measures of phase-coupling between spikes and the Local Field Potential. J. Comput. Neurosci. 2012, 33:53-75.
63. White N.M., McDonald R.J. Multiple parallel memory systems in the brain of the rat. Neurobiol. Learn. Mem. 2002, 77:125-184.
64. Whittington M.A., Traub R.D., Jefferys J.G. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 1995, 373:612-615.