5-Hydroxytryptamine Inhibits Glutamatergic Synaptic Transmission in Rat Corticostriatal Brain Slice

  • Cho, Hyeong-Seok (Department of Pharmacology, MRC for Cell Death Disease Research Center, College of Medicine, The Catholic University of Korea) ;
  • Choi, Se-Joon (Department of Pharmacology, MRC for Cell Death Disease Research Center, College of Medicine, The Catholic University of Korea) ;
  • Kim, Ki-Jung (Department of Pharmacology, MRC for Cell Death Disease Research Center, College of Medicine, The Catholic University of Korea) ;
  • Lee, Hyun-Ho (Department of Pharmacology, MRC for Cell Death Disease Research Center, College of Medicine, The Catholic University of Korea) ;
  • Kim, Seong-Yun (Department of Pharmacology, MRC for Cell Death Disease Research Center, College of Medicine, The Catholic University of Korea) ;
  • Cho, Young-Jin (Department of Pharmacology, MRC for Cell Death Disease Research Center, College of Medicine, The Catholic University of Korea) ;
  • Sung, Ki-Wug (Department of Pharmacology, MRC for Cell Death Disease Research Center, College of Medicine, The Catholic University of Korea)
  • Published : 2005.10.21

Abstract

Striatum is involved in the control of movement and habitual memory. It receives glutamatergic input from wide area of the cerebral cortex as well as an extensive serotonergic (5-hydroxytryptamine, 5-HT) input from the raphe nuclei. In our study, the effects of 5-HT on synaptic transmission were studied in the rat corticostriatal brain slice using in vitro whole-cell recording technique. 5-HT inhibited the amplitude as well as frequency of spontaneous excitatory postsynaptic currents (sEPSC) significantly, and neither ${\gamma}-aminobutyric$ acid (GABA)A receptor antagonist bicuculline (BIC), nor $N-methyl-_{D}-aspartate$ (NMDA) receptor antagonist, $_{DL}-2-amino-5-phosphonovaleric$ acid (AP-V) could block the effect of 5-HT. In the presence non-NMDA receptor antagonist, 2,3-dioxo-6-nitro-1,2,3,4-tetrahydrobenxo[f] quinoxaline-7-sulfonamide (NBQX), the inhibitory effect of 5-HT was blocked. We also figured out that 5-HT change the channel kinetics of the sEPSC. There was a significant increase in the rise time during the 5-HT application. Our results suggest that 5-HT has an effect on both pre- and postsynaptic site with decreasing neurotransmitter release probability of glutamate and decreasing the sensitivity to glutamate by increasing the rise time of non-NMDA receptor mediated synaptic transmission in the corticostriatal synapses.

Keywords

References

  1. Aghajanian GK, Marek GJ. Serotonin induces excitatory postsynaptic potentials in apical dendrites of neocortical pyramidal cells. Neuropharmacology 36: 589-599, 1997 https://doi.org/10.1016/S0028-3908(97)00051-8
  2. Barnes NM, Sharp T. A review of central 5-HT receptors and their function. Neuropharmacology 38: 1083-1152, 1999 https://doi.org/10.1016/S0028-3908(99)00010-6
  3. Bennett MR, Kearns JL. Statistics of transmitter release at nerve terminals. Prog Neurobiol 60: 545-606, 2000 https://doi.org/10.1016/S0301-0082(99)00040-4
  4. Bouryi VA, Lewis DI. The modulation by 5-HT of glutamatergic inputs from the raphe pallidus to rat hypoglossal motoneurones, in vitro. J Physiol 553: 1019-1031, 2003 https://doi.org/10.1113/jphysiol.2003.053843
  5. Bubser M, Backstrom JR, Sanders-Bush E, Roth BL, Deutch AY. Distribution of serotonin 5-HT (2A) receptors in afferents of the rat striatum. Synapse 39: 297-304, 2001 https://doi.org/10.1002/1098-2396(20010315)39:4<297::AID-SYN1012>3.0.CO;2-Q
  6. Cai X, Gu Z, Zhong P, Ren Y, Yan Z. Serotonin 5-HT1A receptors regulate AMPA receptor channels through inhibiting $Ca^{2+}$/ calmodulin-dependent kinase II in prefrontal cortical pyramidal neurons. J Biol Chem 277: 36553-36562, 2002 https://doi.org/10.1074/jbc.M203752200
  7. Cherubini E, Herrling PL, Lanfumey L, Stanzione P. Excitatory amino acids in synaptic excitation of rat striatal neurones in vitro. J Physiol 400: 677-690, 1988
  8. Choi SJ, Chung WS, Kim KJ, Sung KW. Inhibitory modulation of 5-hydroxytryptamine on corticostriacal synaptic transmission in rat brain slice. Korean J Physiol Pharmacol 7: 295-301, 2003
  9. Herrling PL. Pharmacology of the corticocaudate excitatory postsynaptic potential in the cat: evidence for its mediation by quisqualate- or kainate-receptors. Neuroscience 14: 417-426, 1985 https://doi.org/10.1016/0306-4522(85)90301-X
  10. Hu WP, Guan BC, Ru LQ, Chen JG, Li ZW. Potentiation of 5-HT3 receptor function by the activation of coexistent 5-HT2 receptors in trigeminal ganglion neurons of rats. Neuropharmacology 47: 833-840, 2004 https://doi.org/10.1016/j.neuropharm.2004.06.015
  11. Jiang ZG, Teshima K, Yang Y, Yoshioka T, Allen CN. Pre- and postsynaptic actions of serotonin on rat suprachiasmatic nucleus neurons. Brain Res 866: 247-256, 2000 https://doi.org/10.1016/S0006-8993(00)02294-0
  12. Jones BJ, Blackburn TP. The medical benefit of 5-HT research. Pharmacol Biochem Behav 71: 555-568, 2002 https://doi.org/10.1016/S0091-3057(01)00745-6
  13. Laurent A, Goaillard JM, Cases O, Lebrand C, Gaspar P, Ropert N. Activity-dependent presynaptic effect of serotonin 1B receptors on the somatosensory thalamocortical transmission in neonatal mice. J Neurosci 22: 886-900, 2002
  14. Lovinger DM, Tyler EC, Merritt A. Short- and long-term synaptic depression in rat neostriatum. J Neurophysiol 70: 1937-1949, 1993
  15. Muramatsu M, Lapiz MD, Tanaka E, Grenhoff J. Serotonin inhibits synaptic glutamate currents in rat nucleus accumbens neurons via presynaptic 5-HT1B receptors. Eur J Neurosci 10: 2371-2379, 1998 https://doi.org/10.1046/j.1460-9568.1998.00248.x
  16. Nayak SV, Ronde P, Spier AD, Lummis SC, Nichols RA. Nicotinic receptors co-localize with 5-HT (3) serotonin receptors on striatal nerve terminals. Neuropharmacology 39: 2681-2690, 2000 https://doi.org/10.1016/S0028-3908(00)00109-X
  17. Querejeta E, Oviedo-Chavez A, Araujo-Alvarez JM, Quinones-Cardenas AR, Delgado A. In vivo effects of local activation and blockade of 5-HT1B receptors on globus pallidus neuronal spiking. Brain Res 1043: 186-194, 2005 https://doi.org/10.1016/j.brainres.2005.02.055
  18. Rainnie DG. Serotonergic modulation of neurotransmission in the rat basolateral amygdala. J Neurophysiol 82: 69-85, 1999
  19. Ronesi J, Lovinger DM. Induction of striatal long-term synaptic depression by moderate frequency activation of cortical afferents in rat. J Physiol 562: 245-256, 2005
  20. Sung KW, Choi S, Lovinger DM. Activation of group I mGluRs is necessary for induction of long-term depression at striatal synapses. J Neurophysiol 86: 2405-2412, 2001
  21. Svenningsson P, Nishi A, Fisone G, Girault JA, Nairn AC, Greengard P. DARPP-32: an integrator of neurotransmission. Annu Rev Pharmacol Toxicol 44: 269-296, 2004 https://doi.org/10.1146/annurev.pharmtox.44.101802.121415
  22. Yakel JL, Trussell LO, Jackson MB. Three serotonin responses in cultured mouse hippocampal and striatal neurons. J Neurosci 8: 1273-1285, 1988
  23. Zhong P, Yan Z. Chronic antidepressant treatment alters serotonergic regulation of GABA transmission in prefrontal cortical pyramidal neurons. Neuroscience 129: 65-73, 2004 https://doi.org/10.1016/j.neuroscience.2004.06.072
  24. Zhou FM, Hablitz JJ. Activation of serotonin receptors modulates synaptic transmission in rat cerebral cortex. J Neurophysiol 82: 2989-2999, 1999