Selective reduction of AMPA currents onto hippocampal interneurons impairs network oscillatory activity

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Caputi, Antonio ^a   Fuchs, Elke C ^a   Allen, Kevin ^a   Magueresse, Corentin ^a   Monyer, Hannah ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR A4; UNCLASSIFIED DRUG; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 4;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SELECTION; CONTROLLED STUDY; FORAGING; GABAERGIC TRANSMISSION; GENOTYPE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; HIPPOCAMPUS THETA RHYTHM; IN VIVO STUDY; INTERNEURON; MOUSE; NONHUMAN; PROBABILITY; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; PYRAMIDAL NERVE CELL; SPATIAL MEMORY; WORKING MEMORY; ACTION POTENTIAL; ANIMAL; CHANNEL GATING; CHICKEN; EXPLORATORY BEHAVIOR; GENE DELETION; MAZE TEST; METABOLISM; NERVE CELL NETWORK; PHYSIOLOGY; SHORT TERM MEMORY;

MUS;

ACTION POTENTIALS; ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; CA1 REGION, HIPPOCAMPAL; CHICKENS; EXPLORATORY BEHAVIOR; GENE DELETION; HIPPOCAMPUS; INTERNEURONS; ION CHANNEL GATING; MAZE LEARNING; MEMORY, SHORT-TERM; MICE; NERVE NET; PYRAMIDAL CELLS; RECEPTORS, AMPA;

EID: 84861844049     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037318     Document Type: Article

References (63)

1. Buzsáki G, (1989) Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience 31: 551-570.
2. Mizuseki K, Sirota A, Pastalkova E, Buzsáki G, (2009) Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 64: 267-280.
3. Jensen O, Lisman JE, (2005) Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer. Trends Neurosci 28: 67-72.
4. Hasselmo ME, (2005) What is the function of hippocampal theta rhythm?-linking behavioral data to phasic properties of field potential and unit recording data. Hippocampus 15: 936-949.
5. 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.
6. Buzsáki G, (2005) Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15: 827-840.
7. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA, (1996) Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6: 149-172.
8. Wilson MA, McNaughton BL, (1994) Reactivation of hippocampal ensemble memories during sleep. Science (80-) 265: 676-679.
9. O'Keefe J, Nadel L, (1978) The hippocampus as a cognitive map. Oxford University Press.
10. O'Neill J, Senior T, Csicsvari J, (2006) Place-selective firing of ca1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron 49: 143-155.
11. Dupret D, O'Neill J, Pleydell-Bouverie B, Csicsvari J, (2010) The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nat Neurosci 13: 995-1002.
12. Taxidis J, Coombes S, Mason R, Owen MR, (2012) Modeling sharp wave-ripple complexes through a ca3-ca1 network model with chemical synapses. Hippocampus 22: 995-1017.
13. Ylinen A, Bragin A, Nádasdy Z, Jandó G, Szabó I, et al. (1995) Sharp wave-associated high-frequency oscillation (200 hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15: 30-46.
14. Traub RD, Bibbig A, (2000) A model of high-frequency ripples in the hippocampus based on synaptic coupling plus axon-axon gap junctions between pyramidal neurons. J Neurosci 20: 2086-2093.
15. Csicsvari J, Hirase H, Czurkó A, Mamiya A, Buzsáki G, (1999) Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 19: 274-287.
16. Maurer AP, Cowen SL, Burke SN, Barnes CA, McNaughton BL, (2006) Phase precession in hippocampal interneurons showing strong functional coupling to individual pyramidal cells. J Neurosci 26: 13485-13492.
17. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P, (1995) Synchronization of neuronal activity in hippocampus by individual gabaergic interneurons. Nature 378: 75-78.
18. Rácz A, Ponomarenko AA, Fuchs EC, Monyer H, (2009) Augmented hippocampal ripple oscillations in mice with reduced fast excitation onto parvalbumin-positive cells. J Neurosci 29: 2563-2568.
19. Fuchs EC, Zivkovic AR, Cunningham MO, Middleton S, Lebeau FEN, et al. (2007) Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior. Neuron 53: 591-604.
20. Korotkova T, Fuchs EC, Ponomarenko A, von Engelhardt J, Monyer H, (2010) Nmda receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory. Neuron 68: 557-569.
21. Murray AJ, Sauer J, Riedel G, McClure C, Ansel L, et al. (2011) Parvalbumin-positive ca1 interneurons are required for spatial working but not for reference memory. Nat Neurosci 14: 297-299.
22. Fuhs MC, Touretzky DS, (2006) A spin glass model of path integration in rat medial entorhinal cortex. J Neurosci 26: 4266-4276.
23. Monaco JD, Abbott LF, (2011) Modular realignment of entorhinal grid cell activity as a basis for hippocampal remapping. J Neurosci 31: 9414-9425.
24. Solstad T, Moser EI, Einevoll GT, (2006) From grid cells to place cells: a mathematical model. Hippocampus 16: 1026-1031.
25. de Almeida L, Idiart M, Lisman JE, (2009) The input-output transformation of the hippocampal granule cells: from grid cells to place fields. J Neurosci 29: 7504-7512.
26. de Almeida L, Idiart M, Lisman JE, (2012) The single place fields of ca3 cells: a two-stage transformation from grid cells. Hippocampus 22: 200-208.
27. Savelli F, Knierim JJ, (2010) Hebbian analysis of the transformation of medial entorhinal grid-cell inputs to hippocampal place fields. J Neurophysiol 103: 3167-3183.
28. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser M, (2006) Path integration and the neural basis of the 'cognitive map'. Nat Rev Neurosci 7: 663-678.
29. Castro L, Aguiar P, (2012) Phase precession through acceleration of local theta rhythm: a biophysical model for the interaction between place cells and local inhibitory neurons. J Comput Neurosci.
30. Cutsuridis V, Hasselmo M, (2012) Gabaergic contributions to gating, timing, and phase precession of hippocampal neuronal activity during theta oscillations. Hippocampus ahead of print. Doi:10.1002/hipo.21002.
31. Losonczy A, Zemelman BV, Vaziri A, Magee JC, (2010) Network mechanisms of theta related neuronal activity in hippocampal ca1 pyramidal neurons. Nat Neurosci 13: 967-972.
32. O'Keefe J, Recce ML, (1993) Phase relationship between hippocampal place units and the eeg theta rhythm. Hippocampus 3: 317-330.
33. Catania MV, Bellomo M, Giuffrida R, Giuffrida R, Stella AM, et al. (1998) Ampa receptor subunits are differentially expressed in parvalbumin- and calretinin-positive neurons of the rat hippocampus. Eur J Neurosci 10: 3479-3490.
34. Geiger JR, Melcher T, Koh DS, Sakmann B, Seeburg PH, et al. (1995) Relative abundance of subunit mrnas determines gating and ca2+ permeability of ampa receptors in principal neurons and interneurons in rat cns. Neuron 15: 193-204.
35. Deacon RMJ, Bannerman DM, Kirby BP, Croucher A, Rawlins JNP, (2002) Effects of cytotoxic hippocampal lesions in mice on a cognitive test battery. Behav Brain Res 133: 57-68.
36. Derdikman D, Whitlock JR, Tsao A, Fyhn M, Hafting T, et al. (2009) Fragmentation of grid cell maps in a multicompartment environment. Nat Neurosci 12: 1325-1332.
37. Royer S, Sirota A, Patel J, Buzsáki G, (2010) Distinct representations and theta dynamics in dorsal and ventral hippocampus. J Neurosci 30: 1777-1787.
38. Csicsvari J, Hirase H, Mamiya A, Buzsáki G, (2000) Ensemble patterns of hippocampal ca3-ca1 neurons during sharp wave-associated population events. Neuron 28: 585-594.
39. Draguhn A, Traub RD, Schmitz D, Jefferys JG, (1998) Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394: 189-192.
40. Traub RD, Schmitz D, Jefferys JG, Draguhn A, (1999) High-frequency population oscillations are predicted to occur in hippocampal pyramidal neuronal networks interconnected by axoaxonal gap junctions. Neuroscience 92: 407-426.
41. Csicsvari J, Hirase H, Czurkó A, Mamiya A, Buzsáki G, (1999) Fast network oscillations in the hippocampal ca1 region of the behaving rat. J Neurosci 19: RC20.
42. Ellender TJ, Nissen W, Colgin LL, Mann EO, Paulsen O, (2010) Priming of hippocampal population bursts by individual perisomatic-targeting interneurons. J Neurosci 30: 5979-5991.
43. O'Neill J, Senior TJ, Allen K, Huxter JR, Csicsvari J, (2008) Reactivation of experience-dependent cell assembly patterns in the hippocampus. Nat Neurosci 11: 209-215.
44. Qin YL, McNaughton BL, Skaggs WE, Barnes CA, (1997) Memory reprocessing in corticocortical and hippocampocortical neuronal ensembles. Philos Trans R Soc Lond B Biol Sci 352: 1525-1533.
45. Nakashiba T, Buhl DL, McHugh TJ, Tonegawa S, (2009) Hippocampal ca3 output is crucial for ripple-associated reactivation and consolidation of memory. Neuron 62: 781-787.
46. Lovett-Barron M, Turi GF, Kaifosh P, Lee PH, Bolze F, et al. (2012) Regulation of neuronal input transformations by tunable dendritic inhibition. Nat Neurosci 15: 423-430.
47. Hafting T, Fyhn M, Bonnevie T, Moser M, Moser EI, (2008) Hippocampus-independent phase precession in entorhinal grid cells. Nature 453: 1248-1252.
48. Burgess N, O'Keefe J, (2011) Models of place and grid cell firing and theta rhythmicity. Curr Opin Neurobiol 21: 734-744.
49. Magee JC, (2001) Dendritic mechanisms of phase precession in hippocampal ca1 pyramidal neurons. J Neurophysiol 86: 528-532.
50. Kamondi A, Acsády L, Wang XJ, Buzsáki G, (1998) Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus 8: 244-261.
51. Harris KD, Henze DA, Hirase H, Leinekugel X, Dragoi G, et al. (2002) Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417: 738-741.
52. Allen K, Fuchs EC, Jaschonek H, Bannerman DM, Monyer H, (2011) Gap junctions between interneurons are required for normal spatial coding in the hippocampus and short-term spatial memory. J Neurosci 31: 6542-6552.
53. Cacucci F, Yi M, Wills TJ, Chapman P, O'Keefe J, (2008) Place cell firing correlates with memory deficits and amyloid plaque burden in tg2576 alzheimer mouse model. Proc Natl Acad Sci U S A 105: 7863-7868.
54. Robbe D, Buzsáki G, (2009) Alteration of theta timescale dynamics of hippocampal place cells by a cannabinoid is associated with memory impairment. J Neurosci 29: 12597-12605.
55. Monory K, Massa F, Egertová M, Eder M, Blaudzun H, et al. (2006) The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51: 455-466.
56. Klugmann M, Symes CW, Leichtlein CB, Klaussner BK, Dunning J, et al. (2005) Aav-mediated hippocampal expression of short and long homer 1 proteins differentially affect cognition and seizure activity in adult rats. Mol Cell Neurosci 28: 347-360.
57. Clark KR, Liu X, McGrath JP, Johnson PR, (1999) Highly purified recombinant adeno-associated virus vectors are biologically active and free of detectable helper and wild-type viruses. Hum Gene Ther 10: 1031-1039.
58. Soriano P, (1999) Generalized lacz expression with the rosa26 cre reporter strain. Nat Genet 21: 70-71.
59. Schmitt WB, Deacon RMJ, Seeburg PH, Rawlins JNP, Bannerman DM, (2003) A within-subjects, within-task demonstration of intact spatial reference memory and impaired spatial working memory in glutamate receptor-a-deficient mice. J Neurosci 23: 3953-3959.
60. Harris KD, Hirase H, Leinekugel X, Henze DA, Buzsáki G, (2001) Temporal interaction between single spikes and complex spike bursts in hippocampal pyramidal cells. Neuron 32: 141-149.
61. Schmitzer-Torbert N, Jackson J, Henze D, Harris K, Redish AD, (2005) Quantitative measures of cluster quality for use in extracellular recordings. Neuroscience 131: 1-11.
62. Press WH, Teukolsky SA, Vetterling WT, Flannery BP, (2007) Numerical recipes 3rd edition: the art of scientific computing. Cambridge University Press.
63. Fisher NI, (1995) Statistical analysis of circular data. Cambridge University Press.