Glutamatergic synaptic transmission participates in generating the hippocampal EEG

Hippocampus

Volumn 14, Issue 4, 2004, Pages 510-525

  Leung, L Stan ^a   Shen, Bixia ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

AMPA receptors; Gamma rhythm; Medial septum; NMDA receptors; Theta rhythm

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 6,7 DINITRO 2,3 QUINOXALINEDIONE; AMPA RECEPTOR ANTAGONIST; GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ARTICLE; BRAIN COMMISSURE; BRAIN LATERAL VENTRICLE; CONTROLLED STUDY; DELTA RHYTHM; ELECTROENCEPHALOGRAPHY; ENTORHINAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIAL; FREQUENCY MODULATION; GAMMA RHYTHM; HIPPOCAMPUS POTENTIAL; HIPPOCAMPUS THETA RHYTHM; INJECTION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RECORDING; SENSORY NERVE CONDUCTION; SEPTUM NUCLEUS; SYNAPTIC TRANSMISSION;

ANIMALS; CEREBRAL VENTRICLES; ELECTROENCEPHALOGRAPHY; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; HIPPOCAMPUS; INJECTIONS, INTRAVENTRICULAR; KINETICS; MALE; N-METHYLASPARTATE; QUINOXALINES; RATS; RATS, LONG-EVANS; SYNAPTIC TRANSMISSION;

EID: 3042727186     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/hipo.10199     Document Type: Article

References (89)

1. Alreja M, Wu M, Liu W, Atkins JB, Leranth C, Shanabrough M. 2000. Muscarinic tone sustains impulse flow in the septohippocampal GABA but not cholinergic pathway: implications for learning and memory. J Neurosci 20:8103-8110.
2. Armstrong JN, MacVicar BA. 2001.Theta-frequency facilitation of AMPA receptor-mediated synaptic currents in the principal cells of the medial septum. J Neurophysiol 85:1709-1718.
3. Bland BH. 1986. The physiology and pharmacology of hippocampal formation theta rhythms. Prog Neurobiol 26:1-54.
4. Bland BH, Colom LV. 1993. Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex. Prog Neurobiol 41:157-208.
5. Bland BH, Trepel C, Oddie SD, Kirk IJ. 1996. Intraseptal microinfusion of muscimol: effects on hippocampal formation theta field activity and phasic theta-ON cell discharges. Exp Neurol 138:286-297.
6. Bland BH, Konopacki J, Dyck RH. 2002. Relationship between membrane potential oscillations and rhythmic discharges in identified hippocampal theta-related cells. J Neurophysiol 88:3046-3066.
7. Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G. 1995. Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15:47-60.
8. Brazhnik ES, Fox SE. 1997. Intracellular recordings from medial septal neurons during hippocampal theta rhythm. Exp Brain Res 114:442-453.
9. Buzsaki G. 2002. Theta oscillations in the hippocampus. Neuron 33:325-340.
10. Buzsaki G, Leung LW, Vanderwolf CH. 1983. Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287:139-171.
11. 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.
12. Colbert CM, Levy WB. 1992. Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by glutamate receptors. J Neurophysiol 68:1-8.
13. Csicsvari J, Jamieson B, Wise KD, Buzsaki G. 2003. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311-322.
14. DeClerck S, Bland BH, Oddie SD. 2002. Glutamatergic cells in septum modulate hippocampal theta amplitude and movement in rats. Soc Neurosci Abs 28:577.17.
15. Diamond DM, Dunwiddie TV, Rose GM. 1988. Characteristics of hippocampal primed burst potentiation in vitro and in the awake rat. J Neurosci 8:4079-4088.
16. Dudar JD, Whishaw IQ, Szerb JC. 1979. Release of acetylcholine from the hippocampus of freely moving rats during sensory stimulation and running. Neuropharmacology 18:673-678.
17. Fellous JM, Sejnowski TJ. 2000. Cholinergic induction of oscillations in the hippocampal slice in the slow (0.5-2 Hz), theta (5-12 Hz), and gamma (35-70 Hz) bands. Hippocampus 10:187-197.
18. 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.
19. Fischer Y, Wittner L, Freund TF, Gahwiler BH. 2002. Simultaneous activation of gamma and theta network oscillations in rat hippocampal slice cultures. J Physiol 539:857-868.
20. Fox SE. 1989. Membrane potential and impedance changes in hippocampal pyramidal cells during theta rhythm. Exp Brain Res 77:283-294.
21. Freund TF, Buzsaki G. 1996. Interneurons of the hippocampus. Hippocampus 6:347-470.
22. Fujita Y, Sato T. 1964. Intracellular records from hippocampal pyramidal cells in rabbit during theta rhythm activity. J Neurophysiol 27:1011-1025.
23. Gillies MJ, Traub RD, LeBeau FE, Davies CH, Gloveli T, Buhl EH, Whittington MA. 2002. A model of atropine-resistant theta oscillations in rat hippocampal area CA1. J Physiol 543:779-793.
24. Giovannini MG, Giovannelli L, Bianchi L, Kalfin R, Pepeu G. 1997. Glutamatergic modulation of cortical acetylcholine release in the rat: a combined in vivo microdialysis, retrograde tracing and immunohistochemical study. Eur J Neurosci 9:1678-1689.
25. Green JD. 1964. The hippocampus. Physiol Rev 44:561-608.
26. Grunze HC, Rainnie DG, Hasselmo ME, Barkai E, Hearn EF, McCarley RW, et al. 1996. NMDA-dependent modulation of CA1 local circuit inhibition. J Neurosci 16:2034-2043.
27. Heynen AJ, Bilkey DK. 1991. Induction of RSA-like oscillations in both the in-vitro and in-vivo hippocampus. NeuroReport 2:401-404.
28. Heynen AJ, Bilkey DK. 1994. Effects of perforant path procaine on hippocampal type 2 rhythmical slow-wave activity (theta) in the urethane-anesthetized rat. Hippocampus 4:683-695.
29. Horvarth Z Kamondi A, Czopf J, Bliss TVP, Buzsaki G. 1988. NMDA receptors may be involved in generation of hippocampal theta rhythm. In: Hass HL, Buzsaki G, editors. Synaptic plasticity of the hippocampus. Berlin: Springer-Verlag. p 45.
30. Izquierdo I, da Cunha C, Rosat R, Jerusalinsky D, Ferreira MB, Medina JH. 1992. Neurotransmitter receptors involved in post-training memory processing by the amygdala, medial septum, and hippocampus of the rat. Behav Neural Biol 58:16-26.
31. Jones BE. 2003. Arousal systems. Front Biosci 8:S438-S451.
32. Kaibara T, Leung LS. 1993. Basal versus apical dendritic long-term potentiation in hippocampal CA1: a current-source density study. J Neurosci 13:2391-2404.
33. Kamondi A, Acsady L, Wang XJ, Buzsaki 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.
34. Kirk IJ. 1998. Frequency modulation of hippocampal theta by the supramammillary nucleus, and other hypothalamo-hippocampal interactions: mechanisms and functional implications. Neurosci Biobehav Rev 22:pp. 291-302.
35. Kirk IJ, Oddie SD, Konopacki J, Bland BH. 1996. Evidence for differential control of posterior hypothalamic, supramammillary, and medial mammillary theta-related cellular discharge by ascending and descending pathways. J Neurosci 16:5547-5554.
36. D-aspartate autoradiographic and immunohistochemical study. Neuroscience 97:657-669.
37. 3H]D-aspartate labelling and immunocytochemistry. Neuroscience 111:671-691.
38. Kocsis B, Bragin A, Buzsaki G. 1999. Interdependence of multiple theta generators in the hippocampus: a partial coherence analysis. J Neurosci 19:6200-6212.
39. Konopacki J, MacIver MB, Bland BH, Roth SH. 1987. Carbachol-induced EEG "theta" activity in hippocampal brain slices. Brain Res 405:196-198.
40. Larson J, Wong D, Lynch G. 1986. Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 368:347-350.
41. Leranth C, Kiss J. 1996. A population of supramammillary area calretinin neurons terminating on medial septal area cholinergic and lateral septal area calbindin-containing cells are aspartate/glutamatergic. J Neurosci 16:7699-7710.
42. Leung LS. 1982. Nonlinear feedback model of neuronal populations in hippocampal CA1 region. J Neurophysiol 47:845-868.
43. Leung LS. 1984a. Pharmacology of theta phase shift in the hippocampal CA1 region of freely moving rats. Electroencephalogr Clin Neurophysiol 58:457-466.
44. Leung LS. 1984b. Theta rhythm during REM sleep and waking: correlations between power, phase and frequency. Electroencephalogr Clin Neurophysiol 58:553-564.
45. Leung LS. 1984c. Model of gradual phase shift of theta rhythm in the rat. J Neurophysiol 52:1051-1065.
46. Leung LS. 1985. Spectral analysis of hippocampal EEG in the freely moving rat: effects of centrally active drugs and relations to evoked potentials. Electroencephalogr Clin Neurophysiol 60:65-77.
47. Leung LS. 1998. Generation of theta and gamma rhythms in the hippocampus. Neurosci Biobehav Rev 22:275-290
48. Leung LS, Desborough KA. 1988. APV, an N-methyl-D-aspartate receptor antagonist, blocks the hippocampal theta rhythm in behaving rats. Brain Res 463:148-152.
49. Leung LS, Shen B. 1999. N-methyl-D-aspartate receptor antagonists are less effective in blocking long-term potentiation at apical than basal dendrites in hippocampal CA1 of awake rats. Hippocampus 9,617-630.
50. Leung LS, Yim CY. 1986. Intracellular records of theta rhythm in hippocampal CA1 cells of the rat. Brain Res 367:323-327.
51. Leung LS, Yim CY. 1991. Intrinsic membrane potential oscillations in hippocampal neurons in vitro. Brain Res 553:261-274.
52. Leung LS, Lopes da Silva FH, Wadman WJ. 1982. Spectral characteristics of the hippocampal EEG in the freely moving rat. Electroencephalogr Clin Neurophysiol 54:203-219.
53. Leung LS, Martin LA, Stewart DJ. 1994. Hippocampal theta rhythm in behaving rats following ibotenic acid lesion of the septum. Hippocampus 4:136-147.
54. Ma J, Leung LS. 2002. Metabotropic glutamate receptors in the hippocampus and nucleus accumbens are involved in generating seizure-induced hippocampal gamma waves and behavioral hyperactivity. Behav Brain Res 133:45-56.
55. Ma J, Shen B, Stewart LS, Herrick IA, Leung LS. 2002. The septohippocampal system participates in general anesthesia. J Neurosci 22: RC200.
56. 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.
57. Manns ID, Alonso A, Jones BE. 2003. Rhythmically discharging basal forebrain units comprise cholinergic, GABAergic, and putative glutamatergic cells. J Neurophysiol 89:1057-1066.
58. Martin JH. 1991. Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat. Neurosci Lett 127:160-164.
59. Morris GRM, Frey U. 1997. Hippocampal synaptic plasticity: role in spatial learning or the automatic recording of attended experience? Philos Trans R Soc Lond B 352:1489-1503.
60. Muller D, Joly M, Lynch G. 1988. Contributions of quisqualate and NMDA receptors to the induction and expression of LTP. Science 242:1694-1697.
61. Nunez A, Garcia-Austt E, Buno W Jr. 1987. Intracellular theta-rhythm generation in identified hippocampal pyramids. Brain Res 416:289-300.
62. Oddie SD, Stefanek W, Kirk IJ, Bland BH. 1996. Intraseptal procaine abolishes hypothalamic stimulation-induced wheel-running and hippocampal theta field activity in rats. J Neurosci 16:1948-1956.
63. O'Keefe J, Recce ML. 1993. Phase relationship between hippocampal place units and the EEG theta-rhythm. Hippocampus 3:317-330.
64. Page KJ, Everitt BJ. 1995. The distribution of neurons coexpressing immunoreactivity to AMPA-sensitive glutamate receptor subtypes (GluR1-4) and nerve growth factor receptor in the rat basal forebrain. Eur J Neurosci 7:1022-1033.
65. Petsche H, Stumpf C, Gogolak G. 1962. The significance of the rabbit's septum as a relay station between the midbrain and the hippocampus. I. The control of hippocampal arousal activity by the septum cells. Electroencephalogr Clin Neurophysiol 14:202-211.
66. Puma C, Bizot JC. 1999. Hippocampal theta rhythm in anesthetized rats: role of AMPA glutamate receptors. NeuroReport 10:2297-2300.
67. Puma C, Monmaur V, Sharif A, Monmaur P. 1996. Intraseptal infusion of selective and competitive glutamate receptor agonist NMDA and antagonist D-2-amino-5-phosphonopentanoic acid spectral implications for the physostigmine-induced hippocampal theta rhythm in urethane-anesthetized rats. Exp Brain Res 109:384-392.
68. Rawlins JNP, Feldon J, Gray JA. 1979. Septohippocampal connections and the hippocampal theta rhythm. Exp Brain Res 37:49-63.
69. Riedel G, Micheau J, Lam AG, Roloff E, Martin SJ, Bridge H, Hoz L, Poeschel B, McCulloch J, Morris RG. 1999. Reversible neural inactivation reveals hippocampal participation in several memory processes. Nat Neurosci 2:898-905.
70. Soltesz I, Deschenes M. 1993. Low-frequency 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.
71. Stewart DJ, Vanderwolf CH. 1987. Hippocampal rhythmical slow activity following ibotenic acid lesions of the septal region. I. Relations to behavior and effects of atropine and urethane. Brain Res 423:88-100.
72. Stewart M, Fox SE. 1990. Do septal neurons pace the hippocampal theta rhythm? Trends Neurosci 13:163-168.
73. Stumpf C. 1965. Drug action on the electrical activity of the hippocampus. Int Rev Neurobiol 8:77-138.
74. Traub RD, Miles RA. 1991. Neuronal networks of the hippocampus. Cambridge, MA: Cambridge University Press.
75. Traub RD, Whittington MA, Coiling SB, Buzsaki G, Jefferys JG. 1996. Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J Physiol 493(Pt 2):471-484.
76. Traub RD, Jefferys JG, Whittington MA. 1997. Simulation of gamma rhythms in networks of interneurons and pyramidal cells. J Comput Neurosci 4:141-150.
77. Traub RD, Bibbig A, Fisahn A, LeBeau FE, Whittington MA, Buhl EH. 2000. A model of gamma-frequency network oscillations induced in the rat CA3 region by carbachol in vitro. Eur J Neurosci 12:4093-4106.
78. Vanderwolf CH. 1969. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407-418.
79. Vanderwolf CH. 1988. Cerebral activity and behavior: control by cholinergic and serotonergic systems. Int Rev Neurobiol 30:225-340.
80. Vanderwolf CH, Leung LWS. 1983. Hippocampal rhythmical slow activity: a brief history and the effects of entorhinal lesions and phencyclidine. In: Siefert G, editor. Neurobiology of the hippocampus. London: Academic Press. p 275-302.
81. Vertes RP, Kocsis B. 1997. Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81:893-926.
82. Whishaw IQ, Vanderwolf CH. 1973. Hippocampal EEG and behavior: changes in amplitude and frequency of RSA (theta rhythm) associated with spontaneous and learned movement patterns in rats and cats. Behav Biol 8:461-484.
83. Whittington MA, Traub RD, Jefferys JG. 1995. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373:612-615.
84. Williams JH, Kauer JA. 1997. Properties of carbachol-induced oscillatory activity in rat hippocampus. J Neurophysiol 78:2631-2640.
85. Winson J. 1974. Patterns of hippocampal theta rhythm in the freely moving rat. Electroencephalogr Clin Neurophysiol 36:291-301.
86. Winson J. 1978. Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 201:160-163.
87. Wu C, Shen H, Luk WP, Zhang L. 2002. A fundamental oscillatory state of isolated rodent hippocampus. J Physiol 540:509-527.
88. Ylinen A, Soltesz, I, Bragin A, Penttonen M, Sik A, Buzsaki G. 1995a. Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells. Hippocampus 5:78-90.
89. Ylinen A, Bragin A, Nadasdy Z, Jando G, Szabo I, Sik A, Buzsaki G. 1995b. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular, mechanisms. J Neurosci 15:30-46.