Traveling Theta Waves along the Entire Septotemporal Axis of the Hippocampus

Neuron

Volumn 75, Issue 3, 2012, Pages 410-417

  Patel, Jagdish ^a   Fujisawa, Shigeyoshi ^a   Berényi, Antal ^a,b   Royer, Sébastien ^a,c   Buzsáki, György ^a,d  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSITY OF SZEGED   (Hungary)

^c Korea Institute of Science and Technology   (South Korea)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DORSAL HIPPOCAMPUS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; HIPPOCAMPUS THETA RHYTHM; LOCOMOTION; MALE; NEUROTRANSMISSION; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PYRAMIDAL TRACT; RAT; SEPTOTEMPORAL AXIS; VELOCITY; VENTRAL HIPPOCAMPUS;

ANIMALS; HIPPOCAMPUS; MALE; RATS; RATS, LONG-EVANS; THETA RHYTHM;

EID: 84864951695     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2012.07.015     Document Type: Article

References (56)

1. Amaral D., Lavenex P. Hippocampal neuroanatomy. The Hippocampus Book 2007, Oxford University Press, New York. P. Andersen, R. Morris, D. Amaral, T. Bliss, J. O'Keefe (Eds.).
2. Bannerman D.M., Grubb M., Deacon R.M., Yee B.K., Feldon J., Rawlins J.N. Ventral hippocampal lesions affect anxiety but not spatial learning. Behav. Brain Res. 2003, 139:197-213.
3. Bast T., Wilson I.A., Witter M.P., Morris R.G. From rapid place learning to behavioral performance: a key role for the intermediate hippocampus. PLoS Biol. 2009, 7:e1000089.
4. Benucci A., Frazor R.A., Carandini M. Standing waves and traveling waves distinguish two circuits in visual cortex. Neuron 2007, 55:103-117.
5. Bilkey D.K., Goddard G.V. Medial septal facilitation of hippocampal granule cell activity is mediated by inhibition of inhibitory interneurones. Brain Res. 1985, 361:99-106.
6. Bullock T.H., Buzsáki G., McClune M.C. Coherence of compound field potentials reveals discontinuities in the CA1-subiculum of the hippocampus in freely-moving rats. Neuroscience 1990, 38:609-619.
7. Buzsáki G. Theta oscillations in the hippocampus. Neuron 2002, 33:325-340.
8. Buzsáki G., Horváth Z., Urioste R., Hetke J., Wise K. High-frequency network oscillation in the hippocampus. Science 1992, 256:1025-1027.
9. Cenquizca L.A., Swanson L.W. Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex. Brain Res. Brain Res. Rev. 2007, 56:1-26.
10. Cohen A.H., Ermentrout G.B., Kiemel T., Kopell N., Sigvardt K.A., Williams T.L. Modelling of intersegmental coordination in the lamprey central pattern generator for locomotion. Trends Neurosci. 1992, 15:434-438.
11. Csicsvari J., Hirase H., Czurko A., Buzsáki G. Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat. Neuron 1998, 21:179-189.
12. Dolorfo C.L., Amaral D.G. Entorhinal cortex of the rat: topographic organization of the cells of origin of the perforant path projection to the dentate gyrus. J. Comp. Neurol. 1998, 398:49-82.
13. Dong H.W., Swanson L.W., Chen L., Fanselow M.S., Toga A.W. Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc. Natl. Acad. Sci. USA 2009, 106:11794-11799.
14. Dragoi G., Buzsáki G. Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 2006, 50:145-157.
15. Dragoi G., Carpi D., Recce M., Csicsvari J., Buzsáki G. Interactions between hippocampus and medial septum during sharp waves and theta oscillation in the behaving rat. J. Neurosci. 1999, 19:6191-6199.
16. Ermentrout G.B., Kleinfeld D. Traveling electrical waves in cortex: insights from phase dynamics and speculation on a computational role. Neuron 2001, 29:33-44.
17. Freund T.F., Antal M. GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 1988, 336:170-173.
18. Gage F.H., Björklund A., Stenevi U. Reinnervation of the partially deafferented hippocampus by compensatory collateral sprouting from spared cholinergic and noradrenergic afferents. Brain Res. 1983, 268:27-37.
19. Geisler C., Robbe D., Zugaro M., Sirota A., Buzsáki G. Hippocampal place cell assemblies are speed-controlled oscillators. Proc. Natl. Acad. Sci. USA 2007, 104:8149-8154.
20. Geisler C., Diba K., Pastalkova E., Mizuseki K., Royer S., Buzsáki G. Temporal delays among place cells determine the frequency of population theta oscillations in the hippocampus. Proc. Natl. Acad. Sci. USA 2010, 107:7957-7962.
21. Giocomo L.M., Zilli E.A., Fransén E., Hasselmo M.E. Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science 2007, 315:1719-1722.
22. Grillner S., Deliagina T., Ekeberg O., el Manira A., Hill R.H., Lansner A., Orlovsky G.N., Wallén P. Neural networks that co-ordinate locomotion and body orientation in lamprey. Trends Neurosci. 1995, 18:270-279.
23. Hampson R.E., Simeral J.D., Deadwyler S.A. Distribution of spatial and nonspatial information in dorsal hippocampus. Nature 1999, 402:610-614.
24. Hinman J.R., Penley S.C., Long L.L., Escabí M.A., Chrobak J.J. Septotemporal variation in dynamics of theta: speed and habituation. J. Neurophysiol. 2011, 105:2675-2686.
25. 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.
26. Jeewajee A., Barry C., O'Keefe J., Burgess N. Grid cells and theta as oscillatory interference: electrophysiological data from freely moving rats. Hippocampus 2008, 18:1175-1185.
27. Jinno S., Klausberger T., Marton L.F., Dalezios Y., Roberts J.D., Fuentealba P., Bushong E.A., Henze D., Buzsáki G., Somogyi P. Neuronal diversity in GABAergic long-range projections from the hippocampus. J. Neurosci. 2007, 27:8790-8804.
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.G., Tuvnes F.A., Steffenach H.A., Murison R., Moser E.I., Moser M.B. Reduced fear expression after lesions of the ventral hippocampus. Proc. Natl. Acad. Sci. USA 2002, 99:10825-10830.
30. 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.
31. Kocsis B., Bragin A., Buzsáki G. Interdependence of multiple theta generators in the hippocampus: a partial coherence analysis. J. Neurosci. 1999, 19:6200-6212.
32. Konopacki J., Bland B.H., Roth S.H. Phase shifting of CA1 and dentate EEG theta rhythms in hippocampal formation slices. Brain Res. 1987, 417:399-402.
33. Kopell N., Ermentrout G.B. Symmetry and phase locking in chains of weakly coupled oscillators. Commun. Pure Appl. Math. 1986, 39:623-660.
34. Lee M.G., Chrobak J.J., Sik A., Wiley R.G., Buzsáki G. Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 1994, 62:1033-1047.
35. 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.
36. Lubenov E.V., Siapas A.G. Hippocampal theta oscillations are travelling waves. Nature 2009, 459:534-539.
37. Magee J.C., Johnston D.A. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 1997, 275:209-213.
38. Markram H., Lübke J., Frotscher M., Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 1997, 275:213-215.
39. Maurer A.P., Vanrhoads S.R., Sutherland G.R., Lipa P., McNaughton B.L. Self-motion and the origin of differential spatial scaling along the septo-temporal axis of the hippocampus. Hippocampus 2005, 15:841-852.
40. McFarland W.L., Teitelbaum H., Hedges E.K. Relationship between hippocampal theta activity and running speed in the rat. J. Comp. Physiol. Psychol. 1975, 88:324-328.
41. Miles R., Traub R.D., Wong R.K. Spread of synchronous firing in longitudinal slices from the CA3 region of the hippocampus. J. Neurophysiol. 1988, 60:1481-1496.
42. Montgomery S.M., Betancur M.I., Buzsáki G. Behavior-dependent coordination of multiple theta dipoles in the hippocampus. J. Neurosci. 2009, 29:1381-1394.
43. 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.
44. O'Keefe J. Hippocampal Neurophysiology in the behaving animal. The Hippocampus Book 2007, Oxford University Press, New York. P. Andersen, R. Morris, D. Amaral, T. Bliss, J. O'Keefe (Eds.).
45. O'Keefe J., Nadel L. The Hippocampus as a Cognitive Map 1978, Oxford University Press, USA.
46. Petrovich G.D., Canteras N.S., Swanson L.W. Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res. Brain Res. Rev. 2001, 38:247-289.
47. Petsche H., Stumpf C., Gogolak G. [The significance of the rabbit's septum as a relay station between the midbrain and the hippocampus. I. The control of hippocampus arousal activity by the septum cells]. Electroencephalogr. Clin. Neurophysiol. 1962, 14:202-211.
48. Risold P.Y., Swanson L.W. Structural evidence for functional domains in the rat hippocampus. Science 1996, 272:1484-1486.
49. Royer S., Sirota A., Patel J., Buzsáki G. Distinct representations and theta dynamics in dorsal and ventral hippocampus. J. Neurosci. 2010, 30:1777-1787.
50. Segal M., Richter-Levin G., Maggio N. Stress-induced dynamic routing of hippocampal connectivity: a hypothesis. Hippocampus 2010, 20:1332-1338.
51. Small S.A. The longitudinal axis of the hippocampal formation: its anatomy, circuitry, and role in cognitive function. Rev. Neurosci. 2002, 13:183-194.
52. Thompson C.L., Pathak S.D., Jeromin A., Ng L.L., MacPherson C.R., Mortrud M.T., Cusick A., Riley Z.L., Sunkin S.M., Bernard A., et al. Genomic anatomy of the hippocampus. Neuron 2008, 60:1010-1021.
53. Tóth K., Borhegyi Z., Freund T.F. Postsynaptic targets of GABAergic hippocampal neurons in the medial septum-diagonal band of broca complex. J. Neurosci. 1993, 13:3712-3724.
54. Wiener S.I. Spatial, behavioral and sensory correlates of hippocampal CA1 complex spike cell activity: implications for information processing functions. Prog. Neurobiol. 1996, 49:335-361.
55. Witter M.P., Groenewegen H.J., Lopes da Silva F.H., Lohman A.H. Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog. Neurobiol. 1989, 33:161-253.
56. Yoder R.M., Pang K.C. Involvement of GABAergic and cholinergic medial septal neurons in hippocampal theta rhythm. Hippocampus 2005, 15:381-392.