Excitatory actions of serotonin on GABAergic neurons of the medial septum and diagonal band of Broca

Synapse

Volumn 22, Issue 1, 1996, Pages 15-27

  Alreja, Meenakshi ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Yale University School of Medicine   (United States)

Author keywords

5 HT(2A) receptor; Cholinergic; GABAergic; MDL 100,907; Septohippocampal; Synaptic potentials

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ALPHA (2,3 DIMETHOXYPHENYL) 1 [2 (4 FLUOROPHENYL)ETHYL] 4 PIPERIDINEMETHANOL; BICUCULLINE; MIANSERIN; PICROTOXIN; POTASSIUM CHLORIDE; RECEPTOR SUBTYPE; SEROTONIN; SEROTONIN 2 ANTAGONIST; SEROTONIN 2A RECEPTOR; SEROTONIN 3 ANTAGONIST; SEROTONIN 3 RECEPTOR; SEROTONIN 4 RECEPTOR; SEROTONIN CREATININE SULFATE; TETRODOTOXIN; TROPISETRON;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DRUG MECHANISM; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIAL; INTRACELLULAR RECORDING; MALE; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SEPTUM PELLUCIDUM; SEROTONINERGIC NERVE CELL; SYNAPTIC POTENTIAL;

ANIMALS; BICUCULLINE; BRAIN; ELECTROPHYSIOLOGY; EVOKED POTENTIALS; EXTRACELLULAR SPACE; FLUOROBENZENES; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; MALE; NEURONS; PATCH-CLAMP TECHNIQUES; PIPERIDINES; POTASSIUM CHLORIDE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, SEROTONIN; SEROTONIN; SEROTONIN AGONISTS; SEROTONIN ANTAGONISTS; SYNAPSES; TETRODOTOXIN; VISUAL PATHWAYS;

EID: 0030040404     PISSN: 08874476     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-2396(199601)22:1<15::AID-SYN2>3.0.CO;2-L     Document Type: Article

References (84)

1. Aghajanian, G.K., and Rasmussen, K. (1989) Intracellular studies illustrating a simple new method for obtaining viable motoneurons in adult brain slices. Synapse, 3:331-338.
2. Alonso, A., and Köhler, C. (1982) Evidence for separate projections of hippocampal pyramidal and non-pyramidal neurons to different parts of the septum in the rat brain. Neurosci. Lett., 31:209-214.
3. Amaral, D.G., and Kurz, J. (1985) An analysis of the origins of the cholinergic and noncholinergic septal projections to the hippocampal formation of the rat. J. Comp. Neurol., 240.37-59.
4. Assaf, S.Y., and Miller, J.J. (1978) The role of a raphe serotonin system in the control of septal unit activity and hippocampal desynchronization. Neuroscience, 3:539-550.
5. Azmitia, E.C., and Segal, M. (1978) An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J. Comp. Neurol., 179:641-668.
6. Bland, B.H. (1986) The physiology and pharmacology of hippocampal formation theta rhythms Prog. Brain. Res., 26:1-54.
7. 2- conductance. Synapse, 1:582-588.
8. Celio, M.R. (1986) Parvalbumin in most γ-aminobutyric acid-containing neurons of the rat cerebral cortex. Science, 231:995-997.
9. Conn, J.P., Sanders-Bush, E., Hoffman, B.J., and Hartig, P.R. (1986) A unique serotonin receptor in choroid plexus is linked to phosphatidylinositol turnover. Proc. Natl. Acad. Sci. USA, 83:4086-4088.
10. Conrad, L.C.A., Leonard, C.M., and Pfaff, D.W. (1974) Connections of the median and dorsal raphe nuclei in the rat: An autoradiographic and degeneration study. J. Comp. Neurol., 156:179-206.
11. 7 serotonin receptors. Soc. Neurosci Abst., 19:217.
12. Crunelh, V., and Segal, M. (1985) An electrophysiological study of neurons in the rat median raphe and their projections to septum and hippocampus. Neuroscience, 15:47-60.
13. Dinopoulos, A., Dori, I., and Parnavelas, J.G. (1993) Serotonergic innervation of the mature and developing lateral septum of the rat: A light and electron microscopic immunocytochemical analysis. Neuroscience, 55:209-222.
14. Freund, T.F. (1989) GABAergic septohippocampal neurons contain parvalbumin. Brain Res., 478:375-381.
15. Freund, T.F., and Antal, M. (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature, 336:170-173.
16. Frotscher, M., and Leranth, C. (1985) Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunoreactivity: A combined light and electron microscopic study. J. Comp. Neurol., 239:237-246
17. Frotscher, M., and Leranth, C. (1986) The cholinergic innervation of the rat fascia dentata: Identification of target structures on granule cell by combining choline acetyltransferase immunocytochemistry and Golgi impregnation. J. Comp. Neurol., 243:58-70.
18. Gall, C., and Moore, R. Y. (1994) Distribution of enkephalin, substance P, tyrosine hydroxylase, and 5-hydroxytryptamine immunoreactivity in the septal region of the rat. J. Comp. Neurol., 225: 212-227.
19. Gao, B., Hornung, J.P., and Fritschy, J.M. (1995) Identification of distinct GABAA-receptor subtypes in cholinergic and parvalbumin-positive neurons of the rat and marmoset medial-septum diagonal band complex. Neuroscience, 65:101-117.
20. 2 receptor-mediated excitation of interneurons in piriform cortex: Antagonism by atypical antipsychotic drugs. Neuroscience, 58:515-525.
21. Green, J.D., Maxwell, D.S , Schindler, WJ., and Stumpf, C. (1960) Rabbit EEG "theta" rhythm: Its anatomical source and relation to activity in single neurons. J. Neurophysiol., 23:403-420.
22. Griffith, W.H. (1988) Membrane properties of cell types within guinea pig basal forebrain nuclei in vitro. J. Neurophysiol., 59:1590-1612.
23. Griffith, W.H., and Matthews, R.T. (1986) Electrophysiology of AChE-positive neurons in basal forebrain slices. Neurosci. Lett., 71: 169-174.
24. Gritti, I, Mainville, L., and Jones, B.E. (1993) Codistribution of GABA-with acetylcholine-synthesizing neurons in the basal forebrain of the rat. J. Comp. Neurol., 329:438-457.
25. Gulyás, A.I., Seress, L., Tóth, K., Acsády, L., Antal, M., and Freund, T.F. (1991) Septal GABAergic neurons innervate inhibitory interneurons in the hippocampus of the macaque monkey. Neuroscience, 41:381-390.
26. Herz, A., and Gogolak, G. (1965) Mikroelektrophoretische untersuchungen am septum des kaninchens. Pflugers Arch., 285:317-330.
27. Honda, T., and Semba, K. (1993) Serotonergic synaptic input to GABAergic septohippocampal neurons in the rat: A pre-embedding triple-label electron microscopic study. Soc. Neurosci. Abst., 1442.
28. Joels, M., and Gallagher, J.P. (1988) Actions of serotonin recorded intracellularly in rat dorsal lateral septal neurons. Synapse, 2: 45-53.
29. Joels, M., Shinnick-Gallagher, P., and Gallagher, J.P. (1987) Effects of serotonin and serotonin analogues on passive membrane properties of lateral septal neurons in vitro. Brain Res., 417:99-107.
30. Kawaguchi, Y., Katsumaru, H., Kosaka, T., Heizmann, C.W., and Hama, K. (1987) Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin. Brain Res., 416: 369-374.
31. Kohler, C., Chan-Palay, V., and Steinbush, H. (1982) The distribution and origin of serotonin-containing fibers in the septal area: A combined immunohistochemical and fluorescent retrograde tracing study in the rat. J. Comp. Neurol., 209:91-111.
32. Kohler, C , Chan-Palay, V., and Wu, J.Y. (1984) Septal neurons containing glutamatic acid decarboxylase immunoreactivity project to the hippocampal region in the rat brain. Anat. Embryol., 169: 41-44.
33. Larson, J., Wong, D., and Lynch, G. (1986) Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res., 368:347-350.
34. Leranth, C., and Frotscher, M. (1989) Organization of the septal region in the rat brain: cholinergic GABAergic interconnections and the termination of hippocampo-septal fibers. J. Comp. Neurol., 289: 304-314.
35. Leranth, C., Deller, T., and Buzsaki, G. (1992) Intraseptal connections redefined: Lack of a lateral septum to medial septum path. Brain Res., 583:1-11.
36. Lewis, P.R., and Shute, C.C.D. (1967) The cholinergic limbic system: Projections to hippocampal formation, medial cortex nuclei of the ascending cholinergic reticular system and the subfornical organ and supra-optic crest. Brain, 90:521-537.
37. Liu, W., and Alreja, M. (1995) Atypical antipsychotics block 5-HT-mediated excitations in septohippocampal GABAergic neurons. Soc. Neurosci. Abs., abstract 443.15.
38. Lorens, S.A., and Guldberg, H.C. (1974) Regional 5-hydroxytryptamine following selective midbrain raphe lesions in the rat. Brain Res., 78:45-56.
39. Madison, D.V., Malenka, R.C., and Nicoll, R.A., (1986) Phorbol esters block a voltage-sensitive chloride current in hippocampal pyramidal cells Nature, 321:695-697.
40. 2A antagonist. Eur. J. Pharmacol., 259:137-141.
41. Marek, G. J., McDougle, C.J., Price, L.H., and Seiden, L.S. (1992) A comparison of trazodone and fluoxetine: Implications for a serotonergic mechanisms of antidepressant action. Psychopharmacology, 109:2-11.
42. Markram, H., and Segal, H. (1990) Electrophysiological characteristics of cholinergic and non-cholinergic neurons in the rat medial septum-diagonal band complex. Brain Res., 513:171-174.
43. Marrosu, F., Portas, C., Mascia, M.S., Casu, M.A., Fa, M., Giagheddu, M., Imperato, A., and Gessa, G.L. (1995) Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats. Brain Res., 671:329-332.
44. McCormick, D.A., and Wang, Z. (1991) Serotonin and noradrenaline excite GABAergic neurones of the guinea-pig and cat nucleus reticularis thalami. J. Physiol., 442:235-255.
45. 2 pK, values. J Pharmacol. Exp. Ther., 251:238-246.
46. Miettinen, R., and Freund, T.F. (1992) Convergence and segregation of septal and median raphe inputs onto different subsets of hippocampal inhibitory interneurons. Brain Res., 594:263-272.
47. Milner, T.A., and Veznedaroglu, E. (1993) Serotonin-containing terminals synapse on septohippocampal neurones in the rat. J. Neurosci. Res., 36:260-271.
48. Monsma, F.J., Jr, Shen, Y., Ward, R.P., Hamblin, M.W., and Sibley, D.R. (1993) Cloning and expression of a novel serotonin receptor with high affinity for tricyclie psychotropic drugs. Mole C. Pharmacol., 43:320-327.
49. Montone, K.T., Fass, B., and Hamill, G.S. (1988) Serotonergic and nonserotonergic projections from the rat interpeduncular nucleus to the septum, hippocampal formation and raphe: A combined immunocytochemical and fluorescent retrograde labelling study of neurons in the apical subnucleus. Brain Res Bull., 20:233-240.
50. Moore, R.Y., Halans, A.E., and Jones, B.E. (1978) Serotonin neurons of the midbrain raphe: Ascending projections. J. Comp. Neurol., 180:417-438
51. Nilsson, O.G., Strecker, R.E., Daszuta, A., and Bjorklund, A. (1988) Combined cholinergic and serotonergic denervation of the forebrain produces severe deficits in a spatial learning task in the rat. Brain Res., 453:235-246.
52. Onteniente, B., Geffard, M., Campistron, G., and Calas, A. (1987) An ultrastructural study of GABA-immunoreactive neurons and terminals in the septum of the rat, J. Neurosci., 7:48-54.
53. Palacios, J.M., Waeber, C., Hoyer, D., and Mengod, G. (1990) Distribution of serotonin receptors.: Ann. N.Y. Acad. Sci., 600:36-52.
54. 3 mediated control of dopaminergic function. Psychopharmacology, 112:S60.
55. Panula, P., Revuelta, A.V., Cheney, D.L., Wu. J.Y., and Costa, E. (1984) An immunohistochemical study on the locatior of GABAergic neurons in rat septum. J. Comp. Neurol., 222:69-80.
56. 3H-5-hydroxytryptamine. Neuroscience, 6:115-139.
57. Pavlides, C., Greenstein, Y.J., Grudman, M., and Winson, J. (1988) Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res., 439: 383-387.
58. Petsche, H., Stumpf, C., and Gogolak, G. (1962) The significance of the rabbit's septum as a relay station between the midbrain and the hippocampus. The control of hippocampal arousal activity by septum cells. Electroenceph. Clin. Neurophysiol., 14:202-211.
59. Piguet, P., and Galvan, M. (1994) Transient and long-lasting actions of 5-HT on rat dentate gyrus neurones in vitro. J. Physiol., 481.3: 629-640.
60. 2C receptors. Mole C. Brain Res., 23:163-178.
61. Raisman, G. (1966) The connexions of the septum Brain, 89:317-348.
62. Rascol, O., Dutar, P., and Lamour, Y. (1989) Involvement of a pertussis toxin-sensitive G-protein in the pharmacological properties of septohippocampal neurones. Br. J. Pharmacol., 96:956-960.
63. Ropert, N., and Guy, N. (1991) Serotonin facilitates GABAergic transmission in the CA1 region of rat hippocampal in vitro. J. Physiol. (Lond.), 441:121-136
64. 7 receptors. J. Pharmacol. Exp. Ther., 268: 1403-1410.
65. 7) activating cAMP formation. Proc. Natl. Acad. Sci. USA, 90:8547-8551.
66. Segal, M. (1974) Responses of septal nuclei neurons to microiontophoretically administered putative neurotransmitters. Life. Sci., 14: 1345-1351.
67. Segal, M. (1976) Brain stem afferents to the rat medial septum. J. Physiol. (Lond.), 261 617-631.
68. Segal, M. (1986) Properties of rat medial septal neurons recorded in vitro. J. Physiol. (Lond.), 379:309-330.
69. Segal, M., and Landis, S.C. (1974) Afferents to the septal area of the rat studied with the method of retrograde axonal transport of horseradish peroxidase. Brain Res., 82:263-268.
70. 2-activated interneuron. Brain Res., 506: 62-69.
71. Staiger, J.F., and Nurnberger, F. (1991) The efferent connections of the lateral septal nucleus in the guinea pig: Intrinsic connectivity of the septum and projections to other teleneephalic areas. Cell Tissues Res., 264:415-426.
72. Stefanis, C. (1964) Hippocampal neurons: Their responsiveness to microelectrophoretically administered endogenous amines. Pharmacologist, 6:171.
73. Steinbusch, H.W.M. (1981) Distribution of serotonin immunoreactivity in the central nervous system of the rat cell bodies and terminals. Neuroscience. 4:557-618.
74. Stewart, M., and Fox, S.E. (1990) Do septal neurons pace the hippocampal theta rhythm? TINS, 13:163-169.
75. 3 receptors in rat amygdala Neuron, 8:199-203.
76. Swanson, L.W., and Cowan, W.M. (1979) The connections of the septal region in the rat. J. Comp. Neurol., 186:621-656.
77. Tóth, K., Borhegyi, Z., and Freund, T.F. (1993) Postsynaptic targets of GABAergic hippocampal neurons in the medial septum-diagonal band of broca complex. J. Neurosci., 13:3712-3724.
78. 1A receptor ligands on rat dorso-lateral septal neurones in vitro. Br. J. Pharmacol , 106:893-899.
79. Van der Zee, E.A., and Luiten, P.G.M (1994) Cholinergic and GABAergic neurons in the rat medial septum express muscarinic acetylcholine receptors. Brain Res., 652:263-272.
80. Vertes, R.P. (1981) An analysis of ascending brain systems involved in hippocampal synchronization and desynchronization. J. Neurophysiol., 46:1140-1159.
81. Vertes, R P., and Martin, G.P. (1988) Autoradiographic analysis of ascending projections from the pontine and mesencephalic reticular formation of the median raphe nucleus in the rat. J. Comp. Neurol., 275:511-541.
82. 1A agonists, 8-OH-DPAT and buspirone, produces hippocampal theta rhythm in the rat. Neuroscience, 60:441-451
83. Wenk, G., Hughey, D., Boundy, V., Kim, A., Walter, L., and Olton, D (1987) Neurotransmitters and memory: Role of cholinergic, serotonergic and noradrenergic systems. Behav. Neurosci., 101: 325-332.
84. Zhadina, S.D., and Vinogradova, O.S. (1983) Effects of acetylcholine, norepinephrine, and serotonin on neurons of the septum in vitro. Neurosci. Behav. Physiol., 13:405-411.