Skip to main content
Log in

Glutamate receptor activation induces carrier mediated release of endogenous GABA from rat striatal slices

  • Published:
Journal of Neural Transmission Aims and scope Submit manuscript

Summary

The regulation of striatonigral and striatopallidal GABAergic neurons by glutamatergic afferents is thought to play a critical role in normal basal ganglia function. Here we report that in striatal slices about 17% of K+-induced endogenous GABA release was Ca2+-independent and this could be blocked by a GABA transport inhibitor. Activation of N-methyl-D-aspartate (NMDA)- and quisqualate-sensitive receptors induced endogenous GABA efflux only in the presence of a GABA transaminase inhibitor; this efflux was inhibited by 60–80% with a GABA transport inhibiter. NMDA-induced GABA release was blocked by phencyclidine, Mg2+ and CGS 19755. Quisqualate-induced GABA release was blocked completely by a combination of the metabotropic antagonist, L-AP3 and CNQX, a non-NMDA receptor antagonist. These data indicate that excitatory amino acid agonists-induced GABA release is distinct from that induced by high K+ depolarization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bonanno G, Pittaluga A, Fedele E, Fontana G, Raiteri M (1993) Glutamic acid and γ- aminobutytric acid modulate each other's release through heterocarriers sited on the axon terminals of rat brain. J Neurochem 61: 222–230

    Google Scholar 

  • Burke SP, Hablitz JJ (1994) Presynaptic depression of synaptic transmission mediated by activation of metabotropic glutamate receptors in rat neocortex. J Neurosci 14: 5120–5130

    Google Scholar 

  • Choi DW (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1: 623–634

    Google Scholar 

  • Clow DW, Jhamandas K (1989) Characterization of L-glutamate action on the release of endogenous dopamine from the rat caudate-putamen. J Pharmacol Exp Ther 248: 722–728

    Google Scholar 

  • Davies CH, Starkey SJ, Pozza MF, Collingridge GL (1991) GABAB autoreceptors regulate the induction of LTP. Nature 349: 609–611

    Google Scholar 

  • De Montigny P, Stobaugh JF, Givens RS, Carlson RG, Srinivasachar K, Sternson LA, Higuchi T (1987) Naphthalene-2,3-dicarboxaldehyde/cyanide ion: a rationally designed fluorogenic reagent for primary amines. Anal Chem 59: 1096–1101

    Google Scholar 

  • Di Chiara G, Morelli M, Consolo S (1994) Modulatory functions of neurotransmitters in the striatum: ACh/dopamine/NMDA interactions. Trends Neurosci 17: 228–233

    Google Scholar 

  • Drejer J, Honore T (1987) Phencyclidine analogues inhibit NMDA-stimulated [3H]GABA release from cultured cortex neurons. Eur J Pharmacol 143: 287–290

    Google Scholar 

  • Duarte CB, Ferreira IL, Santos PF, Oliveira CR, Carvalho AP (1993) Glutamate increases the [Ca2+]i but stimulates Ca2+-independent release of [3H]GABA in cultured chick retina cells. Brain Res 611: 130–138

    Google Scholar 

  • Girault JA, Spampinato U, Savaki HE, Glowinski SJ, Besson MJ (1986) In vivo release of [3H] τ-aminobutyric acid in the rat neostriatum. I. Characterization and topographical heterogeneity of the effects of dopaminergic and cholinergic agents. Neurosci 19: 1101–1108

    Google Scholar 

  • Gram L (1988) Experimental studies and controlled clinical testing of valproate and vigabatrin. Acta Neurol Scand 78: 241–270

    Google Scholar 

  • Graybiel AM (1990) Neurotransmitters and neuromodulators in the basal ganglia. Trends Neurosci 13: 244–254

    Google Scholar 

  • Graybiel AM, Ragsdale CW (1983) Biochemical anatomy of the striatum. In: Emson PC (eds) Chemical neuroanatomy, 1st edn. Raven Press, New York, pp 427–504

    Google Scholar 

  • Hammond EJ, Wilder BJ (1985) Gamma-vinyl GABA. Gen Pharmacol 16: 441–447

    Google Scholar 

  • Harris KM, Miller RJ (1989) Excitatory amino acid-evoked release of [3H]GABA from hippocampal neurons in primary culture. Brain Res 482: 23–33

    Google Scholar 

  • Jaffe EH, Cuello AC (1980) Release of τ-aminobutyric acid from the external plexiform layer of the rat olfactory bulb: possible dendritic involvement. Neuroscience 5: 1859–1869

    Google Scholar 

  • Jahr CE, Nicoll RA (1980) Dendrodendritic inhibition: demonstration with intracellular recording. Science 207: 1473–1475

    Google Scholar 

  • Janáky R, Saransaari P, Oja SS (1993) Release of GABA from rat hippocampal slices: involvement of quisqualate/N-methyl-D-aspartate-gated ionophores and extracellular magnesium. Neuroscience 53: 779–785

    Google Scholar 

  • Johansen FF, Diemer NH (1991) Enhancement of GABA neurotransmission after cerebral ischemia in the rat reduces loss of hippocampal CA1 pyramidal cells. Acta Neurol Scand 84: 1–6

    Google Scholar 

  • Johnson KM, Jeng YJ (1991) Pharmacological evidence for N-methyl-D-aspartate receptors on nigrostriatal dopaminergic nerve terminals. Can J Physiol Pharmacol 69: 1416–1421

    Google Scholar 

  • Johnson KM, Jones SM (1990) Neuropharmacology of phencyclidine: basic mechanisms and therapeutic potential. Annu Rev Pharmacol Toxicol 30: 707–750

    Google Scholar 

  • Jung MJ, Lippert B, Metcalf BW, Bohlen P, Schlechter PJ (1977) Gamma-vinyl GABA (4-amino-hex-5-enoic acid), a new selective irreversible inhibitor of GABA-T: effects on brain GABA metabolism in mice. J Neurochem 29: 787–802

    Google Scholar 

  • Lehamann J, Scatton B (1982) Characterization of the excitatory amino acid receptor-mediated release of [3H]-acetylcholine from rat striatal slices. Brain Res 252: 77–89

    Google Scholar 

  • Levi G, Raiteri M (1993) Carrier-mediated release of neurotransmitters. Trends Neurosci 16: 415–420

    Google Scholar 

  • Lipton SA (1992) Models of neuronal injury in AIDS: another role for the NMDA receptor? Trends Neurosci 15: 75–79

    Google Scholar 

  • Marchi M, Sanguineti P, Raiteri M (1990) Muscarinic receptors mediate direct inhibition of GABA release from rat striatal nerve terminals. Neurosci Lett 116: 347–351

    Google Scholar 

  • Meldrum B, Garthwaite J (1990) Excitatory amino acid neurotoxicity and neurodegenerative disease. Trends Pharmacol Sci 11: 379–387

    Google Scholar 

  • Mudrick LA, Heinemann U (1990) Quisqualate-induced changes in extracellular sodium and calcium concentrations persist in the combined presence of NMDA and non- NMDA receptor antagonists in rat hippocampus slices. Neurosci Lett 116: 172–178

    Google Scholar 

  • Pin J-P, Bockaert J (1989) Two distinct mechanisms, differentially affected by excitatory amino acids, trigger GABA release from fetal mouse striatal neurons in primary culture. J Neurosci 9: 648–656

    Google Scholar 

  • Salt TE, Eaton SA (1995) Distinct presynaptic metabotropic receptors for L-AP4 and CCG1 on gabaergic terminals: pharmacological evidence using novel α-methyl derivative mGluR antagonists, MAP4 and MCCG, in the rat thalamus in vivo. Neuroscience 65: 5–13

    Google Scholar 

  • Schoepp DD, Conn PJ (1993) Metabotropic glutamate receptors in brain function and pathology. Trends Pharmacol Sci 14: 13–20

    Google Scholar 

  • Shuaib A, Ijaz S, Hasan S, Kalra J (1992) Gamma-vinyl GABA prevents hippocampal and substantia nigra reticulata damage in repetitive transient forebrain ischemia. Brain Res 590: 13–17

    Google Scholar 

  • Snell LD, Johnson KM (1986) Characterization of the inhibition of excitatory amino acid-induced neurotransmitter release in the rat striatum by phencyclidine-like drugs. J Pharmacol Exp Ther 238: 938–946

    Google Scholar 

  • Sugita S, Uchimura N, Jiang ZG, North RA (1991) Distinct muscarinic receptors inhibit release of τ-aminobutyric acid and excitatory amino acids in mammalian brain. Proc Natl Acad Sci USA 88: 2608–2611

    Google Scholar 

  • Suzdak PD, Frederiksen K, Andersen KE, Sorensen PO, Knutsen LJS, Nielsen EB (1992) NNC-711, a novel potent and selective gamma-aminobutyric acid uptake inhibitor: pharmacological characterization. Eur J Pharmacol 224: 189–198

    Google Scholar 

  • Tihon C, Goren MB, Spitz E, Rickenberg HV (1977) Convenient elimination of trichloroacetic acid prior to radioimmunoassay of cyclic nucleotides. Anal Biochem 80: 652–653

    Google Scholar 

  • Watkins JC, Krogsgarrd-Larsen P, Honore T (1990) Structure-activity relationships in the development of excitatory amino acid receptor agonists and competitve antagonists. Trends Pharmacol Sci 11: 25–33

    Google Scholar 

  • Weiss S (1988) Excitatory amino acid-evoked release of γ-[3H] aminobutyric acid from striatal neurons in primary culture. J Neurochem 51: 435–441

    Google Scholar 

  • Williams S, Lacaille JC (1992) GABAB receptor-mediated inhibitory postsynaptic potentials evoked by electrical stimulation and by glutamate stimulation of interneurons in stratum lacunosum-moleculare in hippocampal CA1 pyramidal cells in vitro. Synapse 11: 249–258

    Google Scholar 

  • Wong EHF, Kemp JA (1991) Sites for antagonism on the N-methyl-D-aspartate receptor channel complex. Annu Rev Pharmacol Toxicol 31: 401–425

    Google Scholar 

  • Yazulla S, Kleinschmidt J (1983) Carrier-mediated release of GABA from retinal horizontal cells. Brain Res 263: 63–75

    Google Scholar 

  • Young AMJ, Bradford HF (1993) N-methyl-D-aspartate releases gamma-aminobutyric acid from rat striatum in vivo: a microdialysis study using a novel preloading method. J Neurochem 60: 487–492

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, J., Lonart, G. & Johnson, K.M. Glutamate receptor activation induces carrier mediated release of endogenous GABA from rat striatal slices. J. Neural Transmission 103, 31–43 (1996). https://doi.org/10.1007/BF01292614

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01292614

Keywords

Navigation