Abstract
1. The actions of 5-hydroxytryptamine (5-HT) on rat dentate gyrus neurones were measured with conventional intracellular recording techniques in brain slices maintained in vitro at 32 degrees C. 2. Bath application of 5-HT (0.3-100 microM) hyperpolarized the membrane potential and reduced the input resistance; these effects persisted in tetrodotoxin (1 microM) and were abolished by MDL 73,005EF, a 5-HT1A receptor antagonist. 3. Local application of 5-HT via a pressure pipette also elicited a hyperpolarization and a reduction in resistance, and evoked a transient 'burst' of spontaneous inhibitory postsynaptic potentials (IPSPs) which were blocked by tetrodotoxin or bicuculline. 4. The 'burst' of IPSPs was subject to desensitization. It was completely abolished in the presence of the 5-HT3 receptor antagonist dolasetron. 5. In some cells, a longer lasting increase in spontaneous IPSP frequency was observed during application of 5-HT; this effect was blocked by the 5-HT2 receptor antagonist MDL 100,907. 6. 5-HT (30 microM) shortened the decay time constants of the glutamatergic and GABAergic evoked EPSPs and IPSPs without changing their amplitudes. 7. It is concluded that 5-HT hyperpolarizes granule cells via postsynaptic 5-HT1A receptors and increases spontaneous GABA release from inhibitory interneurones via the activation of 5-HT3 receptors and/or 5-HT2 receptors.
Full text
PDF










Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Akasu T., Hasuo H., Tokimasa T. Activation of 5-HT3 receptor subtypes causes rapid excitation of rabbit parasympathetic neurones. Br J Pharmacol. 1987 Jul;91(3):453–455. doi: 10.1111/j.1476-5381.1987.tb11236.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Alger B. E., Nicoll R. A. Spontaneous inhibitory post-synaptic potentials in hippocampus: mechanism for tonic inhibition. Brain Res. 1980 Oct 27;200(1):195–200. doi: 10.1016/0006-8993(80)91108-7. [DOI] [PubMed] [Google Scholar]
- Alhaider A. A., Lei S. Z., Wilcox G. L. Spinal 5-HT3 receptor-mediated antinociception: possible release of GABA. J Neurosci. 1991 Jul;11(7):1881–1888. doi: 10.1523/JNEUROSCI.11-07-01881.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Andrade R., Nicoll R. A. Pharmacologically distinct actions of serotonin on single pyramidal neurones of the rat hippocampus recorded in vitro. J Physiol. 1987 Dec;394:99–124. doi: 10.1113/jphysiol.1987.sp016862. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Azami J., Fozard J. R., Round A. A., Wallis D. I. The depolarizing action of 5-hydroxytryptamine on rabbit vagal primary afferent and sympathetic neurones and its selective blockade by MDL 72222. Naunyn Schmiedebergs Arch Pharmacol. 1985 Feb;328(4):423–429. doi: 10.1007/BF00692911. [DOI] [PubMed] [Google Scholar]
- Azmitia E. C., Segal M. An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol. 1978 Jun 1;179(3):641–667. doi: 10.1002/cne.901790311. [DOI] [PubMed] [Google Scholar]
- Bliss T. V., Goddard G. V., Riives M. Reduction of long-term potentiation in the dentate gyrus of the rat following selective depletion of monoamines. J Physiol. 1983 Jan;334:475–491. doi: 10.1113/jphysiol.1983.sp014507. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Corradetti R., Ballerini L., Pugliese A. M., Pepeu G. Serotonin blocks the long-term potentiation induced by primed burst stimulation in the CA1 region of rat hippocampal slices. Neuroscience. 1992;46(3):511–518. doi: 10.1016/0306-4522(92)90140-w. [DOI] [PubMed] [Google Scholar]
- Costall B., Naylor R. J. Astra Award Lecture. The psychopharmacology of 5-HT3 receptors. Pharmacol Toxicol. 1992 Dec;71(6):401–415. doi: 10.1111/j.1600-0773.1992.tb00570.x. [DOI] [PubMed] [Google Scholar]
- Derkach V., Surprenant A., North R. A. 5-HT3 receptors are membrane ion channels. Nature. 1989 Jun 29;339(6227):706–709. doi: 10.1038/339706a0. [DOI] [PubMed] [Google Scholar]
- Elliott P., Wallis D. I. Analysis of the actions of 5-hydroxytryptamine on the rabbit isolated vagus nerve. Naunyn Schmiedebergs Arch Pharmacol. 1990 Jun;341(6):494–502. doi: 10.1007/BF00171728. [DOI] [PubMed] [Google Scholar]
- Greenshaw A. J. Behavioural pharmacology of 5-HT3 receptor antagonists: a critical update on therapeutic potential. Trends Pharmacol Sci. 1993 Jul;14(7):265–270. doi: 10.1016/0165-6147(93)90128-7. [DOI] [PubMed] [Google Scholar]
- Higashi H., Nishi S. 5-Hydroxytryptamine receptors of visceral primary afferent neurones on rabbit nodose ganglia. J Physiol. 1982 Feb;323:543–567. doi: 10.1113/jphysiol.1982.sp014091. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hornung J. P., Celio M. R. The selective innervation by serotoninergic axons of calbindin-containing interneurons in the neocortex and hippocampus of the marmoset. J Comp Neurol. 1992 Jun 22;320(4):457–467. doi: 10.1002/cne.903200404. [DOI] [PubMed] [Google Scholar]
- Johnson S. W., Mercuri N. B., North R. A. 5-hydroxytryptamine1B receptors block the GABAB synaptic potential in rat dopamine neurons. J Neurosci. 1992 May;12(5):2000–2006. doi: 10.1523/JNEUROSCI.12-05-02000.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kawa K. Distribution and functional properties of 5-HT3 receptors in the rat hippocampal dentate gyrus: a patch-clamp study. J Neurophysiol. 1994 May;71(5):1935–1947. doi: 10.1152/jn.1994.71.5.1935. [DOI] [PubMed] [Google Scholar]
- Kidd E. J., Laporte A. M., Langlois X., Fattaccini C. M., Doyen C., Lombard M. C., Gozlan H., Hamon M. 5-HT3 receptors in the rat central nervous system are mainly located on nerve fibres and terminals. Brain Res. 1993 May 28;612(1-2):289–298. doi: 10.1016/0006-8993(93)91674-h. [DOI] [PubMed] [Google Scholar]
- Laporte A. M., Koscielniak T., Ponchant M., Vergé D., Hamon M., Gozlan H. Quantitative autoradiographic mapping of 5-HT3 receptors in the rat CNS using [125I]iodo-zacopride and [3H]zacopride as radioligands. Synapse. 1992 Apr;10(4):271–281. doi: 10.1002/syn.890100402. [DOI] [PubMed] [Google Scholar]
- North R. A., Uchimura N. 5-Hydroxytryptamine acts at 5-HT2 receptors to decrease potassium conductance in rat nucleus accumbens neurones. J Physiol. 1989 Oct;417:1–12. doi: 10.1113/jphysiol.1989.sp017786. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Oleskevich S., Lacaille J. C. Reduction of GABAB inhibitory postsynaptic potentials by serotonin via pre- and postsynaptic mechanisms in CA3 pyramidal cells of rat hippocampus in vitro. Synapse. 1992 Nov;12(3):173–188. doi: 10.1002/syn.890120302. [DOI] [PubMed] [Google Scholar]
- Paudice P., Raiteri M. Cholecystokinin release mediated by 5-HT3 receptors in rat cerebral cortex and nucleus accumbens. Br J Pharmacol. 1991 Jul;103(3):1790–1794. doi: 10.1111/j.1476-5381.1991.tb09864.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pazos A., Palacios J. M. Quantitative autoradiographic mapping of serotonin receptors in the rat brain. I. Serotonin-1 receptors. Brain Res. 1985 Nov 4;346(2):205–230. doi: 10.1016/0006-8993(85)90856-x. [DOI] [PubMed] [Google Scholar]
- Ropert N., Guy N. Serotonin facilitates GABAergic transmission in the CA1 region of rat hippocampus in vitro. J Physiol. 1991 Sep;441:121–136. doi: 10.1113/jphysiol.1991.sp018742. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sanger G. J. New antiemetic drugs. Can J Physiol Pharmacol. 1990 Feb;68(2):314–324. doi: 10.1139/y90-046. [DOI] [PubMed] [Google Scholar]
- Schwartzkroin P. A., Scharfman H. E., Sloviter R. S. Similarities in circuitry between Ammon's horn and dentate gyrus: local interactions and parallel processing. Prog Brain Res. 1990;83:269–286. doi: 10.1016/s0079-6123(08)61256-x. [DOI] [PubMed] [Google Scholar]
- Sheldon P. W., Aghajanian G. K. Serotonin (5-HT) induces IPSPs in pyramidal layer cells of rat piriform cortex: evidence for the involvement of a 5-HT2-activated interneuron. Brain Res. 1990 Jan 1;506(1):62–69. doi: 10.1016/0006-8993(90)91199-q. [DOI] [PubMed] [Google Scholar]
- Sprouse J. S., Aghajanian G. K. Electrophysiological responses of serotoninergic dorsal raphe neurons to 5-HT1A and 5-HT1B agonists. Synapse. 1987;1(1):3–9. doi: 10.1002/syn.890010103. [DOI] [PubMed] [Google Scholar]
- Sugita S., Shen K. Z., North R. A. 5-hydroxytryptamine is a fast excitatory transmitter at 5-HT3 receptors in rat amygdala. Neuron. 1992 Jan;8(1):199–203. doi: 10.1016/0896-6273(92)90121-s. [DOI] [PubMed] [Google Scholar]
- Tecott L. H., Maricq A. V., Julius D. Nervous system distribution of the serotonin 5-HT3 receptor mRNA. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1430–1434. doi: 10.1073/pnas.90.4.1430. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Van den Hooff P., Galvan M. Electrophysiology of the 5-HT1A ligand MDL 73005EF in the rat hippocampal slice. Eur J Pharmacol. 1991 Apr 24;196(3):291–298. doi: 10.1016/0014-2999(91)90442-s. [DOI] [PubMed] [Google Scholar]
- Vanderwolf C. H., Baker G. B. Evidence that serotonin mediates non-cholinergic neocortical low voltage fast activity, non-cholinergic hippocampal rhythmical slow activity and contributes to intelligent behavior. Brain Res. 1986 May 28;374(2):342–356. doi: 10.1016/0006-8993(86)90428-2. [DOI] [PubMed] [Google Scholar]
- Vanner S., Surprenant A. Effects of 5-HT3 receptor antagonists on 5-HT and nicotinic depolarizations in guinea-pig submucosal neurones. Br J Pharmacol. 1990 Apr;99(4):840–844. doi: 10.1111/j.1476-5381.1990.tb13017.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Winson J. Influence of raphe nuclei on neuronal transmission from perforant pathway through dentate gyrus. J Neurophysiol. 1980 Nov;44(5):937–950. doi: 10.1152/jn.1980.44.5.937. [DOI] [PubMed] [Google Scholar]
- Yakel J. L., Jackson M. B. 5-HT3 receptors mediate rapid responses in cultured hippocampus and a clonal cell line. Neuron. 1988 Sep;1(7):615–621. doi: 10.1016/0896-6273(88)90111-0. [DOI] [PubMed] [Google Scholar]
- Yakel J. L., Trussell L. O., Jackson M. B. Three serotonin responses in cultured mouse hippocampal and striatal neurons. J Neurosci. 1988 Apr;8(4):1273–1285. doi: 10.1523/JNEUROSCI.08-04-01273.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yang J., Mathie A., Hille B. 5-HT3 receptor channels in dissociated rat superior cervical ganglion neurons. J Physiol. 1992 Mar;448:237–256. doi: 10.1113/jphysiol.1992.sp019039. [DOI] [PMC free article] [PubMed] [Google Scholar]
