In vivo presynaptic control of dopamine release in the cat caudate nucleus—II. Facilitatory or inhibitory influence ofl-glutamate

The local effects of various concentrations of L-glutamate (from 10(-8) M up to 10(-3) M) on the release of [3H]dopamine synthesized continuously from [3H]tyrosine were examined in the caudate nucleus of halothane-anaesthetized cats implanted with push-pull cannulae. When used at a concentration of 10(-8) M or 10(-7) M, L-glutamate stimulated the release of [3H]dopamine from nerve terminals of the nigrostriatal dopamine neurons. This effect was still observed in the presence of tetrodotoxin (5 X 10(-7) M) but it was antagonized by 2-amino 6-trifluoromethoxy benzothiazole (PK 26124) (10(-5) M), an antagonist dopamine nerve terminals. While no significant change in the release of [3H]dopamine was observed with 10(-6) M L-glutamate, higher concentrations (from 10(-5) M to 10(-3) M) of the amino acid produced a long-lasting reduction in the [3H]transmitter release. This latter effect was also antagonized by PK 26124 (10(-5) M) but, unlike that observed with 10(-8) M L-glutamate, it did not persist in the presence of tetrodotoxin (5 X 10(-7) M). On the contrary, a marked stimulation of the release of [3H]dopamine was seen in the presence of this neurotoxin. The reduction in the release of [3H]dopamine produced by 10(-4) M L-glutamate was also antagonized by bicuculline (10(-5) M) and moreover a marked stimulation of [3H]dopamine release took place in the presence of this gamma-aminobutyric acid (GABA) antagonist. Therefore, high concentrations of L-glutamate exerted an inhibitory presynaptic control on [3H]dopamine release which seemed to be indirect and mediated partly by GABAergic neurons. Since a sustained reduction in the spontaneous release of [3H]dopamine was seen in the presence of PK 26124, the corticostriatal glutamatergic neurons appeared to exert a tonic facilitatory presynaptic influence on dopamine release. This effect was important since it represented 40% of the tetrodotoxin-sensitive release of the [3H]transmitter. The direct (stimulatory) and indirect (inhibitory) presynaptic controls on dopamine release mediated by corticostriatal glutamatergic fibres are discussed in light of previous findings and of the anatomical organization of the caudate nucleus.

[1]  J. Bolam.  Synapses of identified neurons in the neostriatum. , 1984, Ciba Foundation symposium.

[2]  I. Divac,et al.  High affinity uptake of glutamate in terminals of corticostriatal axons , 1977, Nature.

[3]  A. Dray,et al.  Caudate stimulation and substantia nigra activity in the rat. , 1976, The Journal of physiology.

[4]  A. Graybiel.  Correspondence between the Dopamine islands and striosomes of the mammalian striatum , 1984, Neuroscience.

[5]  A. Zharikova,et al.  Role of presynaptic dopamine receptors in regulation of the glutamatergic neurotransmission in rat neostriatum , 1984, Neuroscience.

[6]  P. Herrling,et al.  Iontophoretically applied dopamine depolarizes and hyperpolarizes the membrane of cat caudate neurons , 1980, Brain Research.

[7]  J. Glowinski,et al.  Release of dopamine evoked by electrical stimulation of the motor and visual areas of the cerebral cortex in both caudate nuclei and in the substantia nigra in the cat , 1978, Brain Research.

[8]  G. Bernardi,et al.  The action of acetylcholine and L-glutamic acid on rat caudate neurons , 1976, Brain Research.

[9]  J. Coyle,et al.  Dipeptides of glutamate and aspartate may be endogenous neuroexcitants in the rat hippocampal slice , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  T E Salt,et al.  Effects of excitatory amino acids and their antagonists on membrane and action potentials of cat caudate neurones. , 1983, The Journal of physiology.

[11]  S. Snyder,et al.  Dopamine receptors localised on cerebral cortical afferents to rat corpus striatum , 1978, Nature.

[12]  A. Grace,et al.  Dopamine auto- and postsynaptic receptors: electrophysiological evidence for differential sensitivity to dopamine agonists. , 1979, Science.

[13]  P. Spano,et al.  Dopamine receptors: pharmacological and anatomical evidences indicate that two distinct dopamine receptor populations are present in rat striatum. , 1978, Life sciences.

[14]  J. Brown,et al.  The electrophysiology of dopamine (D2) receptors: A study of the actions of dopamine on corticostriatal transmission , 1983, Neuroscience.

[15]  M. Cuénod,et al.  Glutamate release in vitro from corticostriatal terminals , 1979, Brain Research.

[16]  A M Graybiel,et al.  Neurochemically specified subsystems in the basal ganglia. , 2008, Ciba Foundation symposium.

[17]  P. Roberts,et al.  STIMULATORY EFFECT OF l‐GLUTAMATE AND RELATED AMINO ACIDS ON [3H]DOPAMINE RELEASE FROM RAT STRIATUM: AN IN VITRO MODEL FOR GLUTAMATE ACTIONS , 1979, Journal of neurochemistry.

[18]  J. Coyle,et al.  N‐Acetyl‐Aspartyl‐Glutamate: Regional Levels in Rat Brain and the Effects of Brain Lesions as Determined by a New HPLC Method , 1984, Journal of neurochemistry.

[19]  B. Meldrum,et al.  2-Amino-6-trifluoromethoxy benzothiazole, a possible antagonist of excitatory amino acid neurotransmission—I Anticonvulsant properties , 1985, Neuropharmacology.

[20]  M. Chesselet,et al.  Presynaptic regulation of neurotransmitter release in the brain: Facts and hypothesis , 1984, Neuroscience.

[21]  J. Glowinski,et al.  AN ADAPTATION OF THE PUSH‐PULL CANNULA METHOD TO STUDY THE IN VIVO RELEASE OF [3H]DOPAMINE SYNTHESIZED FROM [3H]TYROSINE IN THE CAT CAUDATE NUCLEUS: EFFECTS OF VARIOUS PHYSICAL AND PHARMACOLOGICAL TREATMENTS , 1977, Journal of neurochemistry.

[22]  R. Hassler,et al.  Effect of frontal cortex ablation on striatal glutamic acid level in rat , 1977, Brain Research.

[23]  L. Kerkérian,et al.  Presynaptic dopaminergic control of high affinity glutamate uptake in the striatum , 1983, Neuroscience Letters.

[24]  H. Bradford,et al.  Presynaptic Control of the Synthesis and Release of Dopamine from Striatal Synaptosomes: A Comparison Between the Effects of 5‐Hydroxytryptamine, Acetylcholine, and Glutamate , 1980, Journal of neurochemistry.

[25]  P. Mcgeer,et al.  A glutamatergic corticostriatal path? , 1977, Brain Research.

[26]  L. Kerkérian,et al.  Topographic changes in high-affinity glutamate uptake in the cat red nucleus, substantia nigra, thalamus, and caudate nucleus after lesions of sensorimotor cortical areas , 1983, Experimental Neurology.

[27]  M. Kemel,et al.  Presynaptic effect of L-glutamic acid on the release of dopamine in rat striatal slices , 1977, Neuroscience Letters.

[28]  J. Coyle,et al.  N-Acetylaspartylglutamate: possible role as the neurotransmitter of the lateral olfactory tract. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[29]  M. Kemel,et al.  Stimulation of dopamine release by GABA in rat striatal slices , 1978, Brain Research.

[30]  P. Jenner,et al.  Kainic acid lesions of striatum and decortication reduce specific [3H]sulpiride binding in rats, so D‐2 receptors exist post‐synaptically on corticostriate afferents and striatal neurons , 1981, The Journal of pharmacy and pharmacology.

[31]  K. Fuxe,et al.  Effects of bromocriptine on 3H-spiroperidol binding sites in rat striatum. Evidence for actions of dopamine receptors not linked to adenylate cyclase. , 1978, Life sciences.

[32]  G. F. Rowlands,et al.  Activation of dopamine receptors inhibits calcium-dependent glutamate release from cortico--striatal terminals in vitro. , 1980, European journal of pharmacology.

[33]  R. Romo,et al.  Distinct commissural pathways are involved in the enhanced release of dopamine induced in the contralateral caudate nucleus and substantia nigra by unilateral application of GABA in the cat thalamic motor nuclei , 1984, Brain Research.

[34]  T. F. Freund,et al.  Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines , 1984, Neuroscience.

[35]  J. Girault,et al.  In Vivo Release of Endogenous Amino Acids from the Rat Striatum: Further Evidence for a Role of Glutamate and Aspartate in Corticostriatal Neurotransmission , 1986, Journal of neurochemistry.

[36]  R. Romo,et al.  In vivo presynaptic control of dopamine release in the cat caudate nucleus—I. Opposite changes in neuronal activity and release evoked from thalamic motor nuclei , 1986, Neuroscience.

[37]  J. Bouyer,et al.  Chemical and structural analysis of the relation between cortical inputs and tyrosine hydroxylase-containing terminals in rat neostriatum , 1984, Brain Research.

[38]  P. Campochiaro,et al.  GABA receptor binding in rat striatum: Localization and effects of denervation , 1977, Brain Research.

[39]  J. Glowinski,et al.  Gabaergic processes involved in the control of dopamine release from nigrostriatal dopaminergic neurons in the cat. , 1978, European journal of pharmacology.

[40]  M. Kemel,et al.  Attempts to localize the GABA receptors involved in the GABA-induced release of newly-synthesized [3H]dopamine in rat striatal slices , 1979, Brain Research.

[41]  P R Mitchell,et al.  Modulation of striatal [3H]-glutamic acid release by dopaminergic drugs. , 1980, Life sciences.

[42]  J. Glowinski,et al.  Stimulating effects of gamma-hydroxybutyrate on dopamine release from the caudate nucleus and the substantia nigra of the cat. , 1977, The Journal of pharmacology and experimental therapeutics.

[43]  S. Snyder,et al.  Neurotransmitter receptor localizations: Brain lesion induced alterations in benzodiazepine, GABA, β-adrenergic and histamine H1-receptor binding , 1980, Brain Research.

[44]  Hugh J. Spencer.  Antagonism of cortical excitation of striatal neurons by glutamic acid diethyl ester: Evidence for glutamic acid as an excitatory transmitter in the rat striatum , 1976, Brain Research.

[45]  N. Sharif,et al.  Striatal glutamatergic function: Modifications following specific lesions , 1982, Brain Research.

[46]  L. Kerkérian,et al.  Inhibitory effects of dopamine on high affinity glutamate uptake from rat striatum. , 1982, Life sciences.

[47]  N. Sharif,et al.  Effects ofl-glutamate and related amino acids upon the release of [3H]dopamine from rat striatal slices , 1978, Brain Research.