Theta rhythmicity in the medial septum: Entraining by the GABAergic neurons

Zhurnal Vysshei Nervnoi Deyatelnosti Imeni I.P. Pavlova

Volumn 54, Issue 2, 2004, Pages 192-201

  Brazhnik, Elena S ^a  

^a RUSSIAN ACADEMY OF SCIENCES   (Russian Federation)

Author keywords

Diagonal band of broca; Hippocampus; Network oscillations; Rhythmic bursting; Synchronization

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMATE RECEPTOR;

ANIMAL; ARTICLE; CHOLINERGIC NERVE; HIPPOCAMPUS; HISTOLOGY; METABOLISM; NERVE CELL; NERVE CELL INHIBITION; NERVE CELL NETWORK; PHYSIOLOGY; SEPTUM PELLUCIDUM; SYNAPTIC TRANSMISSION; THETA RHYTHM;

ANIMALS; CHOLINERGIC FIBERS; HIPPOCAMPUS; NERVE NET; NEURAL INHIBITION; NEURONS; RECEPTORS, GABA; RECEPTORS, GLUTAMATE; SEPTUM PELLUCIDUM; SYNAPTIC TRANSMISSION; THETA RHYTHM;

EID: 4644335788     PISSN: 00444677     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (90)

1. Allen C.N., Crawford I.L. GABAergic agents in the medial septal nucleus affect hippocampal theta rhythm and acetylcholine utilization // Brain Res. 1984. V. 322. P. 261-267.
2. Alonso A., Khateb A., Fort P., Jones B.E., Mühlethaler M. Differential oscillatory properties of cholinergic and non-cholinergic nucleus basalis neurons in guinea pig brain slice // Eur. J. Neurosci. 1996. V. 8. P. 169-182.
3. Amaral D.G, Kurz J. An analysis of the origins of the cholinergic and non-cholinergic septal projections to the hippocampal formation of the rat // J. Comp. Neurol. 1985. V. 240. P. 37-59.
4. Apartis E., Poindessous-Jazat F.R., Lamour Y.A., Bassant M.H. Loss of rhythmically bursting neurons in rat medial septum following selective lesion of septohippocampal cholinergic system // J. Neurophysiol. 1998. V. 79. P. 1633-1642.
5. Baisden R.H., Woodruff M.L., Hoover D.B. Cholinergic and non-cholinergic septohippocampal projections: a double-label horseradish peroxidase-acetylcholinesterase study in the rabbit // Brain Res. 1984. V. 290. P. 146-151.
6. Bland B.H. The physiology and pharmacology of hippocampal formation theta rhythms // Prog. Neurobiol. 1986. V. 26. P. 1-54. Review.
7. Boehmer G., Greffrath W., Martin E., Hermann S. Subthreshold oscillation of the membrane potential in magnocellular neurones of the rat supraoptic nucleus // J. Physiol. (Lond.). 2000. V. 526. P. 115-128.
8. Bokor H., Csaki A., Kocsis K., Kiss J. Cellular architecture of the nucleus reuniens thalami and its putative aspartatergic/glutamatergic projection to the hippocampus and medial septum in the rat // Eur. J. Neurosci. 2002. V. 16. P. 1227-1239.
9. Borhegyi Z., Freund T.F. Dual projection from the medial septum to the supramammillary nucleus in the rat // Brain Res. Bull. 1998. V. 46. P. 453-459.
10. Borhegyi Z., Magloczky Z., Acsady L., Freund T.F. The supramammillary nucleus innervates cholinergic and GABAergic neurons in the medial septum-diagonal band of Broca complex // Neuroscience. 1998. V. 82. P. 1053-1065.
11. Bracci E., Centonze D., Bernardi G., Calabresi P. Voltage-dependent membrane potential oscillations of rat striatal fast-spiking interneurons // J. Physiol. 2003. V. 549(Pt 1). P. 121-130.
12. Brashear H.R., Zaborszky L., Heimer L. Distribution of GABAergic and cholinergic neurons in the rat diagonal band // Neuroscience. 1986. V. 17. P. 439-451.
13. Brauer K., Seeger G., Hartig W., Rossner S., Poethke R., Kacza J., Schliebs R., Bruckner G., Bigl V. Electron microscopic evidence for a cholinergic innervation of GABAergic parvalbumin-immunoreactive neurons in the rat medial septum // J. Neurosci. Res. 1998. V. 54. P. 248-253.
14. Brazhnik E.S., Fox S.E. Intracellular recordings from medial neurons during the hippocampal theta rhythm // Exp. Brain Res. 1997. V. 114. P. 442-453.
15. Brazhnik E.S., Fox S.E. Action potentials and relations to the theta rhythm of medial septal neurons in vivo // Exp. Brain Res. 1999. V. 127. P. 244-258.
16. Brazhnik E.S., Fox S.E. Muscarinic, GABA-A and ionotropic glutamate receptors on septal neurons all contribute to the hippocampal theta rhythm // SFN. Abstract. 2000.
17. Brazhnik E.S., Vinogradova O.S. Control of the rhythmic bursts in the septal pacemaker of theta-rhythm: effects of anaesthetic and anticholinergic drugs // Brain Res. 1986. V. 380. P. 94-110.
18. Buzsaki G., Chrobak J.J. Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks // Curr. Opin. Neurobiol. 1995. V. 5. P. 504-510.
19. Carnes K.M., Fuller T.A., Price J.L. Sources of presumptive glutamatergic/aspartatergic afferents to the magnocellular basal forebrain in the rat // J. Comp. Neurol. 1990. V. 302. P. 824-852.
20. Chow C.C., White J.A., Ritt J., Kopell N. Frequency control in synchronized networks of inhibitory neurons // J. Comp. Neurosci. 1998. V. 5. P. 407-420.
21. Chu D.C.M., Albin R.L., Young A.B., Penney J.B. Distribution and kinetics of GABAB binding sites in rat central nervous system: a quantitative autoradiographic study // Neuroscience. 1990. V. 34. P. 341-357.
22. Cobb S.R., Buhl E.H., Halasy K., Paulsen O., Somogyi P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons // Nature. 1995. V. 378(6552). P. 75-78.
23. Colom L.V., Bland B.H. Medial septal cell interactions in relation to hippocampal field activity and effects of atropine // Hippocampus. 1991. V. 1. P. 15-30.
24. Csicsvari J., Hirase H., Czurko A., Mamiya A., Buzsaki G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat // J. Neurosci. 1999. V. 19. P. 274-287.
25. Denham M.J., Borisyuk R.M. A model of theta rhythm production in the septal-hippocampal system and its modulation by ascending brain stem pathways // Hippocampus. 2000. V. 10. P. 698-716.
26. Dickson C.T., Magistretti J., Shalinsky M.H., Fransen E., Hasselmo M.E., Alonso A. Properties and role of Ih in the pacing of subthreshold oscillations in entorhinal cortex layer II neurons // J. Neurophysiol. 2000. V. 83. P. 2562-2579.
27. Fisher R.S., Levine M.S. Transmitter cosynthesis by corticopetal basal forebrain neurons // Brain Res. 1989. V. 491. P. 163-168.
28. Freund T.F. GABAergic septohippocampal neurons contain parvalbumin // Brain Res. 1989. V. 478. P. 375-381.
29. Freund T.F., Antal M. GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus // Nature. 1988. V. 336. P. 170-173.
30. Gao B., Hornung J.P., Fritschy J.M. Identification of distinct GABAA-receptor subtypes in cholinergic and parvalbumin-positive neurons of the rat and marmoset medial septum-diagonal band complex // Neuroscience. 1995. V. 65. P. 101-117.
31. Giovannini M.G., Mutolo D., Bianchi L., Michelassi A., Pepeu G. NMDA receptor antagonists decrease GABA outflow from the septum and increase acetylcholine outflow from the hippocampus: a microdialysis study // J. Neurosci. 1994. V. 14. P. 1358-1365.
32. Gorelova N., Reiner P.B. Role of the afterhyperpolarization in the control of discharge properties of septal cholinergic neurons in vitro // J. Neurophysiol. 1996. V. 75. P. 695-706.
33. Griffith W.H. Membrane properties of cell types within guinea pig basal forebrain nuclei in vitro // J. Neurophysiol. 1988. V. 59. P. 1590-1612.
34. Griffith W.H., Matthews R.T. Electrophysiology of Ache-positive neurons in basal forebrain slices // Neurosci. Lett. 1986. V. 71. P. 169-174.
35. Gritti I., Mainville L., Jones B.E. Codistribution of GABA- with acetylcholine-synthetizing neurons in the basal forebrain of the rat // J. Comp. Neurol. 1993. V. 329. P. 438-457.
36. Gutfreund Y., Yarom Y., Segev I. Subthreshold oscillations and resonant frequency in guinea-pig cortical neurons: physiology and modeling // J. Physiol. (Lond.). 1995. V. 483. P. 621-640.
37. Han S.H., McCool B.A., Murchison D., Nahm S.S., Parrish A.R., Griffith W.H. Single-cell RT-PCR detects shifts in mRNA expression profiles of basal forebrain neurons during aging // Mol. Brain Res. 2002. V. 98. P. 67-80.
38. Henderson Z. Expression of GABAA receptor subunit messenger RNA in non-cholinergic neurons of the rat basal forebrain // Neuroscience. 1995. V. 5. P. 1077-1086.
39. Henderson Z., Morris N.P., Grimwood P., Fiddler G., Yang H.W., Appenteng K. Morphology of local axon collaterals of electrophysiologically characterised neurons in the rat medial septal/diagonal band complex // J. Comp. Neurol. 2001. V. 430. P. 410-432.
40. Huguenard J.R., Prince D.A. A novel T-type current underlies prolonged Ca(2+)-dependent burst firing in GABAergic neurons of rat thalamic reticular nucleus // J. Neurosci. 1992. V. 12. P. 3804-3817.
41. Jaskiw G.E., Tizabi Y., Lipska B.K., Kolachana B.S., Wyatt R.J., Gilad G.M. Evidence for a frontocorticalseptal glutamatergic pathway and compensatory changes in septal glutamate uptake after cortical and fornix lesions in the rat // Brain Res. 1991. V. 550. P. 7-10.
42. Kiss J., Borhegyi Z., Csaky A., Szeiffert G., Leranth C. Parvalbumin-containing cells of the angular portion of the vertical limb terminate on calbindin-immunoreactive neurons located at the border between the lateral and medial septum of the rat // Exp. Brain Res. 1997. V. 113. P. 48-56.
43. Kiss J., Csaki A., Bokor H., Shanabrough M., Leranth C. The supramammillo-hippocampal and supramammilloseptal glutamatergic/aspartatergic projections in the rat: a combined [3H]D-aspartate autoradiographic and immunohistochemical study // Neurosci. 2000. V. 97. P. 657-669.
44. Kiss J., Csaki A., Bokor H., Zaborszky L. Demonstration of glutamatergic/aspartatergic neurons in the neuronal structure of the septum-diagonal band complex of the rat by using [3H]D-aspartate retrograde transport autoradiography // SFN Abstracts. 2000, online.
45. Kiss J., Magloczky Z., Somogyi J., Freund T.F. Distribution of calretinin-containing neurons relative to other neurochemically identified cell types in the medial septum of the rat // Neuroscience. 1999. V. 78. P. 399-410.
46. Kiss J., Patel A.J., Baimbridge K.G., Freund T.F. Topographical localization of neurons containing parvalbumine and choline acetyltransferase in the medial septumdiagonal band region of the rat // Neuroscience. 1990. V. 36. P. 61-72.
47. Kichigina V.F., Kudina T.A., Zenchenko K.I., Vinogradova O.S. Background activity of rabbit hippocampal neurons in conditions of functional exclusion of structures, which regulate the theta rhythm // Neurosci. Behav. Physiol. 1999. V. 29. P. 377-384.
48. Kichigina V.F., Kutyreva E.V., Brazhnik E.S. Modulation of theta rhythmicity in the medial septal neurons and the hippocampal EEG in awake rabbit via actions at noradrenergic α2-receptors // Neuroscience. 2003. V. 120. P. 509-521.
49. Klink R., Alonso A. Ionic mechanisms for the subthreshold oscillations and differential electroresponsiveness of medial entorhinal cortex layer II neurons // J. Neurophysiol. 1993. V. 70. P. 144-157.
50. Knapp J.A., Morris N.P., Henderson Z., Matthews R.T. Electrophysiological characteristics of non-bursting, glutamate decarboxylase messenger RNA-positive neurons of the medial septum/diagonal band nuclei of guinea-pig and rat // Neuroscience. 2000. V. 98. P. 661-668.
51. Kocsis B., Vertes R.P. Characterization of neurons of the supramammillary nucleus and mammillary body that discharge rhythmically with the hippocampal theta rhythm in the rat // J. Neurosci. 1994. V. 14(11, Pt 2). P. 7040-7052.
52. Kohler C., Chan-Palay V., Wu J.J. Septal neurons containing glutamic acid decarboxylase immunoreactivity project to the hippocampal region in the rat brain // Anat. Emryol. 1984. V. 169. P. 41-44.
53. Kosaka T, Tauchi M., Dahl J.L. Cholinergic neurons containing GABA-like and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat // Exp. Brain Res. 1988. V. 70. P. 605-617.
54. Leranth C., Frotscher M. Organization of the septal region in the rat brain: cholinergic-GABAergic interconnections and the termination of hippocampo-septal fibers // J. Comp. Neurol. 1989. V. 289. P. 304-314.
55. Leranth C., Kiss J. 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. 1996. V. 16. P. 7699-7710.
56. Leranth C., Carpi D., Buzsaki G., Kiss J. The entorhinosepto- supramammillary nucleus connection in the rat: morphological basis of a feedback mechanism regulating hippocampal theta rhythm // Neuroscience. 1999. V. 88. P. 701-718.
57. Luthi A., McCormick D.A. H-current: properties of a neuronal and network pacemaker // Neuron. 1998. V. 21. P. 9-12.
58. Markram H., Segal M. Electrophysiological characteristics of cholinergic and non-cholinergic neurons in the medial septum-diagonal band complex // Brain Res. 1990. V. 513. P. 171-174.
59. Matthews R.T., Lee W.L. A comparison of extracellular and intracellular recordings from medial septum-diagonal band neurons in vitro // Neuroscience. 1991. V. 42. P. 451-462.
60. McBain C.J., Fisahn A. Interneurons unbound // Nat. Rev. Neurosci. 2001. V. 2. P. 11-23.
61. Melander T., Staines W.A., Hokfelt T., Rokaeus A., Eckenstein F., Salvaterra P.M., Wainer B.H. Galanin-like immunoreactivity in cholinergic neurons of the septumbasal forebrain complex projecting to the hippocampus of the rat // Brain Res. 1985. V. 360. P. 130-138.
62. Miller J.J. Characteristics of neuronal activity in striatal and limbic forebrain regions maintained in the in vitro // Electrophysiology of Isolated Mammalian CNS Preparations / Eds Kerkut G.A., Weal H.V. London: Acad. Press, 1981. P. 309-336.
63. Moor E., DeBoer P., Westerink B.H. GABA receptors and benzodiazepine binding sites modulate hippocampal acetylcholine release in vivo // Eur. J. Pharmacol. 1998. V. 359. P. 119-126.
64. Morris N.P., Harris S.J., Henderson Z. Parvalbumin-immunoreactive, fast-spiking neurons in the medial septum / diagonal band complex of the rat: intracellular recordings in vitro // Neuroscience. 1999. V. 92. P. 589-600.
65. Onteniente B., Tago H., Kimura H., Maeda T. Distribution of gamma-aminobutyric acid-immunoreactive neurons in the septal region of rat brain // J. Comp. Neurol. 1986. V. 248. P. 422-430.
66. Panula P., Revuelta A.V., Cheney D.L., Wu J.Y., Costa E. An immunohistochemical study on the location of GABAergic neurons in the rat septum // J. Comp. Neurol. 1984. V. 222. P. 69-80.
67. Pasqualotto B.A., Vincent S.R. Galanin and NADPH-diaphorase coexistence in cholinergic neurons of the rat basal forebrain // Brain Res. 1991. V. 551. P. 78-86.
68. Rawlins J.N.P., Feldon J., Gray J.A. Septo-hippocampal connections and the hippocampal theta rhythm // Exp. Brain Res. 1979. V. 37. P. 49-63.
69. Serafin M., Williams S., Khateb A., Fort P., Muhlethaler M. Rhythmic firing of medial septum non-cholinergic neurons // Neuroscience. 1996. V. 75. P. 671-675.
70. Skinner F.K., Zhang L., Velazquez J.L., Carlen P.L. Bursting in inhibitory interneuronal networks: A role for gap-junctional coupling // J. Neurophysiol. 1999. V. 81. P. 1274-1283.
71. Sotty F., Danik M., Manseau F., Laplante F., Quirion R., Williams S. Glutamatergic, cholinergic and GABAergic neurons contribute to the septohippocampal pathway and exhibit distinct electrophysiological properties: novel implications for hippocampal rhythmicity // J. Physiol. 2003.
72. Stewart M., Fox S.E. Two populations of rhythmically bursting neurons in the rat medial septum are revealed by atropine // J. Neurophysiol. 1989. V. 61. P. 982-983.
73. Stewart M., Fox S.E. Do septal neurons pace the hippocampal theta rhythm? // Trends in Neurosci. 1990. V. 13. P. 163-168.
74. Suszhiw J.B., Schaffer A.E., Barker J.L. Electrophysiological properties of early postnatal rat septal neurons in short-term culture // Brain Res. 1992. V. 588. P. 246-254.
75. Toth K., Borhegyi Z., Freund T.F. Postsynaptic targets of GABAergic hippocampal neurons in the medial septumdiagonal band of broca complex // J. Neurosci. 1993. V. 13. P. 3712-3724.
76. Toth K., Freund T.F., Miles R. Disinhibition of rat hippocampal pyramidal cells by GABAergic afferent from the septum // J. Physiol. (Lond). 1997. V. 500. P. 463-474.
77. Van der Zee E.A., Luiten P.G. Cholinergic and GABAergic neurons in the rat medial septum express muscarinic acetylcholine receptors // Brain Res. 1994. V. 652. P. 263-272.
78. Vertes R.P., Kocsis B. Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus // Neuroscience. 1997. V. 81. P. 893-926.
79. Vinogradova O.S. Expression, control, and probable functional significance of the neuronal theta-rhythm // Prog. Neurobiol. 1995. V. 45. P. 523-583.
80. Vinogradova O.S., Brazhnik E.S., Karanov A.M., Zhadina S.D. Analysis of neuronal activity in the rabbit's septum with various conditions of deafferentation // Brain Res. 1980. V. 187. P. 354-368.
81. Vinogradova O.S., Zhadina S.D., Brazhnik E.S. Organization of background activity of the septal neurons analyzed in vitro // Neurophysiologia (Kiev). 1987. V. 19. P. 586-595 (In Russian).
82. Walsh T.J., Stackman R.W., Emerich D.F., Taylor L.A. Intraseptal injection of GABA and benzodiazepine receptor ligands alters high-affinity choline transport in the hippocampus // Brain Res. Bull. 1993. V. 31. P. 267-271.
83. Wang X.J. Pacemaker neurons for the theta rhythm and their synchronization in the septohippocampal reciprocal loop // J. Neurophysiol. 2002. V. 87. P. 889-900.
84. Wang X.J., Buzsáki G. Gamma oscillations by synaptic inhibition in a hippocampal interneuronal network // J. Neurosci. 1996. V. 16. P. 6402-6413.
85. Wang X.J., Rinzel J. Spindle rhythmicity in the reticularis thalami nucleus: synchronization among mutually inhibitory neurons // Neuroscience. 1993. V. 53. P. 899-904.
86. White J.A., Banks M.I., Pearce R.A., Kopell N. Networks of interneurons with fast and slow γ-aminobutyric acid type A (GABAA) kinetics provide substrate for mixed gamma-theta rhythm // Proc. Nat. Acad. Sci. USA. 2000. V. 97. P. 8128-8133.
87. White J.A., Chow C.C., Soto-Trevino C., Kopell N. Synchronization and oscillatory dynamics in heterogeneous mutually inhibitory neurons // J. Comput. Neurosci. 1998. V. 5. P. 5-16.
88. Woolf N.J., Butcher L.L. Cholinergic systems in the brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain // Brain Res. Bull. 1986. V. 16. P. 603-637.
89. Wu N., Hsiao C.F., Chandler S.H. Membrane resonance and subthreshold membrane oscillations in mesencephalic V neurons: participants in burst generation // J. Neurosci. 2001. V. 21. P. 3729-3739.
90. Zaborszky L., Pang K., Somogyi J., Nadasdy Z., Kallo I. The basal forebrain corticopetal system revisited // Ann. N. Y. Acad. Sci. 1999. V. 877. P. 339-367.