Interdependence of multiple theta generators in the hippocampus: A partial coherence analysis

Journal of Neuroscience

Volumn 19, Issue 14, 1999, Pages 6200-6212

  Kocsis, Bernat ^a,c   Bragin, Anatol ^b,d   Buzsáki, György ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c NATIONAL INSTITUTE OF NEUROSURGERY   (Hungary)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CA3 recurrent system; Coding; Hippocampus; Neuronal oscillators; Partial coherence; Phase locking; Theta rhythm

Indexed keywords

ANALYTIC METHOD; ANIMAL EXPERIMENT; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; ENTORHINAL CORTEX; HIPPOCAMPUS; INTERNEURON; MOSSY FIBER; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; RAT; REM SLEEP; SLOW WAVE SLEEP; THETA RHYTHM;

EID: 0033565946     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-14-06200.1999     Document Type: Article

References (95)

1. Acsády L, Kamondi A, Sik A, Buzsáki G (1998) GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J Neurosci 18:3386-3403.
2. Alonso A, Garcia-Austt E (1987) Neuronal sources of the theta rhythm in the entorhinal cortex of the rat. II. Phase relations between unit discharges and theta field potentials. Exp Brain Res 67:502-509.
3. Amaral DG, Witter MP (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31:571-591.
4. Andersen P (1960) Interhippocampal impulses. II. Apical dendritic activation of CA1 neurons. Acta Physiol Scand 48:178-208.
5. Apostol G, Creutzfeldt OD (1974) Crosscorrelation between the activity of septal units and hippocampal EEG during arousal. Brain Res 67:65-75.
6. Artemenko DP (1972) Role of hippocampal neurons in theta-wave generation. Neurophysiology 4:409-415.
7. Barnes CA (1990) Effects of aging on the dynamics of information processing and synaptic weight changes in the mammalian hippocampus. Prog Brain Res 86:89-104.
8. Barrenechea C, Pedemonte M, Nunez A, Garcia-Austt E (1995) In vivo intracellular recordings of medial septal and diagonal band of Broca neurons: relationships with theta rhythm. Exp Brain Res 103:31-40.
9. Berger TW, Semple-Rowland S, Bassett JL (1981) Hippocampal polymorph neurons are the cells of origin for ipsilateral activation and commissural afferents to the dentate gyrus. Brain Res 215:329-336.
10. Bland BH (1986) Physiology and pharmacology of hippocampal formation theta rhythms. Prog Neurobiol 26:1-54.
11. Bland BH, Colom LV (1993a) Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex. Prog Neurobiol 41:157-208.
12. Bland BH, Colom LV (1993b) Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic system. Prog Neurobiol 41:157-208.
13. Bland BH, Andersen P, Ganes T (1975) Two generators of hippocampal theta activity in rabbits. Brain Res 94:199-218.
14. Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsáki G (1995) Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15:47-60.
15. Brankack J, Stewart M, Fox SE (1993) Current source density analysis of the hippocampal theta rhythm: associated sustained potentials and candidate synaptic generators. Brain Res 615:310-327.
16. Brazhnik ES, Fox SE (1997) Intracellular recordings from medial septal neurons during hippocampal theta rhythm. Exp Brain Res 114:442-453.
17. Buhl EH, Han ZS, Lorinczi Z, Stezhka VV, Karnup SV, Somogyi P (1994) Physiological properties of anatomically identified axo-axonic cells in the rat hippocampus. J Neurophysiol 71:1289-1307.
18. Bullock TH, Buzsáki G, McClune MC (1990) Coherence of compound field potentials reveals discontinuities in the CA1-subiculum of the hippocampus in freely moving rats. Neuroscience 38:609-619.
19. Buzsáki G (1989) A two-stage model model of memory trace formation: a role of "noisy" brain states. Neuroscience 31:551-570.
20. Buzsáki G, Eidelberg E (1982) Direct afferent excitation and long-term potentiation of hippocampal interneurons. J Neurophysiol 48:597-607.
21. Buzsáki G, Leung LS, Vanderwolf CH (1983) Cellular basis of hippocampal EEG in the behaving rat. Brain Res Rev 6:139-171.
22. Buzsáki G, Czopf J, Kondakor I, LK (1986) Laminar distribution of hippocampal rhythmic slow activity (RSA) in the behaving rat: current source density analysis. Brain Res 365:125-137.
23. Buzsáki G, Bickford RG, Ryan LJ, Young S, Prohaska O, Mandel RJ, Gage FH (1989) Multisite recording of brain field potentials and unit activity in freely moving rats. J Neurosci Methods 28:209-217.
24. Buzsáki G, Horvath Z, Urioste R, Hetke J, Wise K (1992) High frequency network oscillation in the hippocampus. Science 256:1025-1027.
25. Buzsáki G, Ylinen A, Penttonen M, Bragin A, Nadasdy Z, Chrobak JJ (1995) Possible physiological role of the perforant path-CA1 projection. Hippocampus 5:141-146.
26. Chrobak JJ, Buzsáki G (1998) Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci 18:388-398.
27. Cobb SR, Buhl EH, Halasy K, Somogyi P (1995) Synchronization of Neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75-98.
28. Colbert CM, Levy WB (1992) Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by glutamate receptors. J Neurophysiol 68:1-8.
29. 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.
30. Deadwyler SA, West JR, Cotman CW, Lynch GS (1975) A neurophysiological analysis of the commissural projections to the dentate gyrus of the rat. J Neurophysiol 38:164-184.
31. Dumermuth G, Molinari L (1991) Relationship among signals, cross spectral analysis of the EEG. In: Digital biosignal processing (Weitkunat R,ed), pp 361-398. Amsterdam: Elsevier.
32. Fisahn A, Pike FG, Buhl EH, Paulsen O (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394:186-189.
33. Fox SE (1989) Membrane potential and impedance changes in hippocampal pyramidal cells during theta rhythm. Exp Brain Res 77:283-294.
34. Fox SE, Wolfson S, Ranck JBJ (1986) Hippocampal theta rhythm and the firing of neurons in walking and urethane anesthetized rats. Exp Brain Res 62:495-508.
35. Freund TF, Antal M (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336:170-173.
36. Fujita Y, Sato T (1964) Intracellular records from hippocampal pyramidal cells in rabbit during theta rhythmic activity. J Neurophysiol 27:1011-1025.
37. Gaztelu JM, Buno WJ (1982) Septo-hippocampal relationships during EEG theta rhythm. Electroencephalogr Clin Neurophysiol 54:375-387.
38. Gersch W, Goddard GV (1970) Epileptic focus location: spectral analysis method. Science 169:701-702.
39. Gogolak G, Stumpf C, Petsche H, Sterc J (1968) The firing pattern of septal neurons and the form of the hippocampal theta wave. Brain Res 7:201-207.
40. Hasselmo ME, Bower JM (1993) Acetylcholine and memory. Trends Neurosci 16:218-222.
41. Holscher C, Anwyl R, Rowan MJ (1997) Stimulation on the positive phase of hippocampal theta rhythm induces long-term potentiation that can be depotentiated by stimulation on the negative phase in area CA1 in vivo. J Neurosci 16:6470-6477.
42. Huerta PT, Lisman JE (1993) Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature 364:723-725.
43. Huerta PT, Lisman JE (1996) Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in the CA1 in vitro. Neuron 15:1053-1063.
44. Jenkins GM, Watts DG (1968) Spectral analysis and its applications. San Francisco: Holden-Day.
45. Kaminski M, Blinowska K, Szelenberger W (1995) Investigation of coherence structure and EEG activity propagation during sleep. Acta Neurobiol Exp 55:213-219.
46. Kaminski M, Blinowska K, Szelenberger W (1997) Topographic analysis of coherence and propagation of EEG activity during sleep and wakefulness. Electroencephalogr Clin Neurophysiol 102:216-227.
47. Kamondi A, Acsády L, Buzsáki G (1998a) Dendritic spikes are enhanced by cooperative network activity in the intact hippocampus. J Neurosci 18:3919-3928.
48. Kamondi A, Acsády L, Wang X-J, Buzsáki G (1998b) Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus 8:244-261.
49. King C, Recce M, O'Keefe J (1998) The rhythmicity of cells of the medial septum/diagonal band of Broca in the awake freely moving rat: relationships with behaviour and hippocampal theta. Eur J Neurosci 10:464-477.
50. Kiss J, Buzsáki G, Morrow JS, Glantz SB, Leranth C (1996) Entorhinal cortical innervation of parvalbumin-containing neurons (basket and chandelier cells) in the rat Ammon's horn. Hippocampus 6:239-246.
51. Kocsis B (1994) Basis for differential coupling between rhythmic discharges of sympathetic efferent nerves. Am J Physiol 267:R1008-R1019.
52. Kocsis B, Vertes RP (1994) Characterization of neurons of the supramammillary nucleus and mammillary body that discharge rhythmically with the hippocampal theta rhythm in the rat. J Neurosci 14:7040-7052.
53. Kocsis B, Vertes RP (1997) Phase relations of theta rhythmic firing of neurons in the supramammillary nucleus and mammillary body to the hippocampal theta activity in urethane anesthetized rats. Hippocampus 7:204-214.
54. Kocsis B, Gebber GL, Barman SM, Kenney MJ (1990) Relationships between activity of sympathetic nerve pairs: phase and coherence. Am J Physiol 259:R549-R560.
55. Kocsis B, Thinschmidt JS, Kinney GG, Vertes RP (1994) Separation of the hippocampal theta rhythm generators by partial coherence analysis in the rat. Brain Res 660:341-345.
56. Konopacki J, MacIver MB, Bland BH, Roth SH (1987) Carbacholinduced EEG "theta" activity in hippocampal brain slices. Brain Res 405:196-198.
57. Konopacki J, Bland BH, Roth SH (1988) Carbachol-induced theta in hippocampal formation slices: evidence for a third generator of theta in CA3C area. Brain Res 451:33-42.
58. Konopacki J, Bland BH, Colom LV, Oddie SD (1992) In vivo intracellular correlates of hippocampal formation theta-on and theta-off cells. Brain Res 586:247-255.
59. Korzeniewska A, Kasicki S, Kaminski M, Blinowska KJ (1997) Information flow between hippocampus and related structures during various types of rat's behavior. J Neurosci Methods 73:49-60.
60. Larson J, Lynch G (1986) Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events. Science 232:985-988.
61. Lee MG, Chrobak JJ, Sik A, Wiley RG, Buzsáki G (1994) Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 62:1033-1047.
62. Leung LS (1984) Model of gradual phase shift of theta rhythm in the rat. J Neurophysiol 52:1051-1065.
63. Leung LS, Yim CY (1986) Intracellular records of theta rhythm in hippocampal CA1 cells of the rat. Brain Res 367:323-327.
64. Leung LS, Yim CY (1991) Intrinsic membrane potential oscillations in hippocampal neurons in vitro. Brain Res 553:261-274.
65. Li X-G, Somogyi P, Tepper JM, Buzsáki G (1992) Axonal and dendritic arborization of an intracellularly labeled chandelier cell in the CA1 region of rat hippocampus. Exp Brain Res 90:519-525.
66. Liberati D, Cursi M, Locatelli T, Comi G, Cerutti S (1997) Total and partial coherence analysis of spontaneous and evoked EEG by means of multi-variable autoregressive processing. Med Biol Eng Comput 35:124-130.
67. Lisman JE (1999) Relating hippocampal circuitry to function: Recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 22:233-242.
68. Lopes da Silva FH, Vos JE, Mooibroek J, van Rotterdam A (1980a) Partial coherence analysis of thalamic and cortical alpha rhythms in dog: a contribution towards a general model of the cortical organization of rhythmic activity. In: Rhythmic EEG activities and cortical functioning (Pfurtscheller G, ed), pp 33-59. Amsterdam: Elsevier.
69. Lopes da Silva FH, Vos JE, Mooibroek J, van Rotterdam A (1980b) Relative contributions of intracortical and thalamo-cortical processes in the generation of alpha rhythms, revealed by partial coherence analysis. Electroencephalogr Clin Neurophysiol 50:449-456.
70. Lopes da Silva FH, Witter M, Boejinga PH, Lohman A (1990) Anatomic organization and physiology of the limbic cortex. Physiol Rev 70:453-511.
71. MacVicar BA, Tse FWY (1989) Local neuronal circuitry underlying cholinergic rhythmical slow activity in CA3 area of rat hippocampal slices. J Physiol (Lond) 417:197-212.
72. McMahon LL, Williams JH, Kauer JA (1998) Functionally distinct groups of interneurons identified during rhythmic carbachol oscillations in hippocampus in vitro. J Neurosci 18:5640-5651.
73. Mitchell SJ, Ranck JBJ, Steward O, Olton DS (1982) Medial septal area lesions disrupt theta rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats. J Neurosci 2:292-302.
74. Nunez A, Garcia-Austt E, Buno WJ (1987) Intracellular theta rhythm generation in identified hippocampal pyramids. Brain Res 416:289-300.
75. Nunez A, Garcia-Austt E, Buno WJ (1990) Synaptic contributions to theta rhythm genesis in rat CA1-CA3 hippocampal pyramidal neurons in vivo. Brain Res 533:176-179.
76. O'Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317-330.
77. Petsche H, Stumpf CH, Gogolak G (1962) 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 14:202-211.
78. Sekihara K, Abraham-Fuchs K, Stefan H, Hellstrandt E (1996) Suppression of background brain activity influence in localizing epileptic spike sources from biomagnetic measurements. Brain Topogr 8:323-328.
79. Sherman DL, Tsai YC, Rossell LA, Mirski MA (1997) Spectral analysis of a thalamus-to-cortex seizure pathway. IEEE Trans Biomed Engn 44:657-664.
80. Skaggs WE, McNaughton BL (1996) Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271:1870-1873.
81. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA (1996) Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6:149-173.
82. Soltesz I, Deschenes M (1993) Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. J Neurophysiol 70:97-116.
83. Stewart M, Fox SE (1989) Firing relations of medial septal neurons to the hippocampal theta rhythm in urethane anesthetized rats. Exp Brain Res 77:507-516.
84. Stewart M, Fox SE (1990) Do septal neurons pace the hippocampal theta rhythm? Trends Neurosci 13:163-168.
85. Toth K, Freund TF, Miles R (1997) Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum. J Physiol (Lond) 500:463-474.
86. Traub RD, Miles R, Buzsáki G (1992) Computer simulation of carbachol-driven rhythmic population oscillations in the CA3 region of the in vitro hippocampus. J Physiol (Lond) 451:653-672.
87. Tucker DM, Roth DL, Bair TB (1986) Functional connections among cortical regions: topography of EEG coherence. Electroencephalogr Clin Neurophysiol 63:242-250.
88. Vanderwolf CH (1969) Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407-418.
89. Vertes RP, Kocsis B (1997) Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81:893-926.
90. Vinogradova OS (1995) Expression, control, and probable functional significance of the neuronal theta rhythm. Prog Neurobiol 45:523-583.
91. Wallenstein GV, Eichenbaum H, Hasselmo ME (1998) The hippocampus as an associator of discontiguous events. Trends Neurosci 21:317-323.
92. Williams JH, Kauer JA (1997) Properties of carbachol-induced oscillatory activity in rat hippocampus. J Neurophysiol 78:2631-2640.
93. Winson J (1974) Patterns of hippocampal theta rhythm in the freely moving rat. Electroencephalogr Clin Neurophysiol 36:291-301.
94. Wu K, Canning KJ, Leung LS (1998) Functional interconnections between CA3 and dentate gyrus revealed by current source density analysis. Hippocampus 8:217-230.
95. Ylinen A, Soltesz I, Bragin A, Penttonen M, Sik A, Buzsáki G (1995) Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells and basket cells. Hippocampus 5:78-90.