Summary
Recent neurochemical evidence suggests that chemical or electrial stimulation of the subthalamic nucleus (STH) increases dopamine release in the substantia nigra (SN) with a subsequent decrease in the striatum. In a previous paper, we reported that bicuculline-induced activation of the STH increases neuronal activity in the substantia nigra pars reticulata (SNpr) and in the pallidal complex. In order to investigate the role played by the dopaminergic system in the observed activation, the neuronal responses of subthalamic nucleus target structures were studied in amine depleted rats following subthalamic stimulation. Amine depletion was accomplished by pretreating the rats with reserpine (2 mg/kg; S.C.) and with alpha-methyl-para-tyrosine (α-mpt; 50 mg/kg; I.P.).Following this treatment, dopamine levels were reduced by 94% in the striatum as measured by HPLC. Amine depletion significantly increased the spontaneous activity of subthalamic cells by 53%. In the SNpr, no significant changes in the spontaneous neuronal activity were observed, but the excitatory responses to bicuculline-induced stimulation of the STH were potentiated as compared to non-treated animals. In the pallidial complex (GP-EP), no potentiation was found. The data suggest that the spontaneous pattern of discharge of the STH is probably under monoaminergic control. They also suggest a reciprocal interaction between dopamine and glutamatergic afferent terminals from the STH within the SNpr, but not in the pallidal complex.
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Albin RL, Aldrige W, Young AB, Gilman S (1989) Feline subthalamic nucleus neurons contain glutamate-like but not GABA-like or glycine-like immunoreactivity. Brain Res 491: 185–188
Besson MJ, Graybiel AM, Nastuk MA (1988) (3H) SCH 23390 binding to D 1 dopamine receptors in the basal ganglia of the cat and primate: delineation of striosomal compartments and pallidal and nigral subdivisions. Neuroscience 26: 101–119
Bergman H, Wichmann T, De Long MR (1990) Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 249: 1436–1438
Bergstrom DA, Walters JR (1984) Dopamine attenuates the effects of GABA on single unit activity in the globus pallidus. Brain Res 310: 23–33
Brown LL, Makman MM, Wolfson LI, Dvorkin B, Warner C, Katzman R (1979) A direct role of dopamine in the rat subthalamic nucleus and intrapeduncular area. Science 206: 1416–1418
Campbell GA, Eckardt MJ, Weight FF (1985) Dopaminergic mechanisms in the subthalamic nucleus of rat: analysis using horseradish peroxydase and microiontophoresis. Brain Res 333: 261–270
Cheramy A, Leviel V, Glowinski J (1981) Dendritic release of dopamine in the substantia nigra. Nature 289: 537–542
Deniau JM, Hammond C, Chevalier G, Feger J (1978) Evidence for branched subthalamic nucleus projections to substantia nigra, entopeduncular nucleus and globus pallidus. Neurosci Lett 9: 117–121
Dray S, Gonye TJ, Oakley NR, Tanner T (1976) Evidence for the existence of a raphe projection to the substantia nigra in rats. Brain Res 113: 45–57
Filion M (1979) Effects of interruption of the nigrostriatal pathway and of dopaminergic agents on the spontaneous activity of globus pallidus neurons in the awake monkey. Brain Res 178: 425–441
Fonnum F, Grofova I, Rinvik E (1978) Origin and distribution of glutamate decarboxylase in the nucleus subthalamicus of the cat. Brain Res 153: 370–374
Hammond C, Hammond T, Rouzaire-Dubois B (1983) Branched output neurons of the rat subthalamic nucleus: electrophysiological study of the synaptic effects on identified cells in the two main target nuclei, the entopeduncular nucleus and the substantia nigra. Neuroscience 9: 511–520
Kerkerian L, Cupo A, Dusticier N, Epelbaum J, Errami M, Ettayebi K, Forni C, Jarry T, Kumar U, Salin P, Samuel LD, Vuillet J, Danger JM, Nieoullon A (1989) Regulation dopaminergique de l'activité de systèmes neuronaux peptidergiques, GABAergiques et glutamatergiques au niveau du striatum. Encéphale 15: 143–154
Kilpatrik IC, Jones MW, Phillipson OT (1986) A semi automated analysis method for catecholamines, indolamines and some prominent metabolites in microdissected regions on the nervous system: an isocratic HPLC technic and employing coulometric detection and minimal sample preparation. J Neurochem 46: 1865–1876
Kitai ST, Deniau JM (1981) Cortical inputs to the subthalamus: intracellular analysis. Brain Res 214: 411–415
Kitai ST, Kita H (1987) Anatomy and physiology of the subthalamic nucleus: a driving force of the basal ganglia. In: Carpenter MB, Jaraman A (eds) The basal ganglia II. Structure and function: current concepts. Plenum Press, New York, pp 357–373
Kornhuber J, Kornhuber KJS, Kornhuber HH (1984) The corticonigral projection: reduced glutamate content in the rat substantia nigra following frontal cortex ablation in the rat. Brain Res 322: 124–126
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1961) Protein measurement with the folin phenol reagent. J Biol Chem 193: 265–275
Madison DV, Nicoll RA (1982) Noreadrenaline blocks accommodation of pyramidal cell discharge in the hippocampus. Nature 299: 631–633
Martres M-P, Bouthenet M-L, Sales N, Sokoloff P, Schwartz J-C (1985) Widespread distribution of brain dopamine receptors evidenced with (125I) Iodosulpiride, a highly selective ligand. Science 228: 752–755
Mathews RT, German DC (1986) Evidence for a functional role of dopamine type D 1 receptors in the substantia nigra of rats. Eur J Pharmacol 120: 87–93
Meibach RC, Katzman R (1979) Catecholaminergic innervation of the subthalamic nucleus: evidence for a rostral continuation of A 9 (substantia nigra) dopaminergic group. Brain Res 173: 364–368
Miller WC, De Long MR (1987) Altered tonic activity of neurons in the globus pallidus and subthalamic nucleus in the primate MPTP model of parkinsonism. In: Carpenter MB, Jayaraman A (eds) The basal ganglia II, vol 32. Structure and function, current concepts. Plenum Press, New York, pp 415–427
Mintz I, Hammond C, Feger J (1986 a) Excitatory effect of iontophoretically applied dopamine on identified neurons of the rat subthalamic nucleus. Brain Res 375: 172–175
Mintz I, Hammond C, Guibert B, Leviel V (1986 b) Stimulation of the subthalamic nucleus enhances the release of dopamine in the rat substantia nigra. Brain Res 376: 406–408
Nakanishi H, Hori N, Kastuda N (1985) Neostriatal evoked inhibition and effects of dopamine on globus pallidus neurons in the rat slice preparations. Brain Res 358: 282–286
Nakanishi H, Kita H, Kita ST (1988) Electrophysiology of entopeduncular neurons and their responses to subthalamic stimulation in the rat brain slice preparations. Soc Neurosci Abstr 14: 408.14
Nieoullon A, Kerkerian L, Dusticier N (1983) Presynaptic controls in the neostriatum: reciprocal interactions between the nigrostriatal dopaminergic neurons and the cortico-striatal glutamatergic pathway. Exp Brain Res 7: 54–65
Pan HS, Penney JB, Young AB (1985) GABA and benzodiazepine receptor changes induced by unilateral 6-hydroxydopamine lesions of the medial forebrain bundle. J Neurochem 45: 1396–1404
Parent A, Hazrati LN, Smith Y (1989) The subthalamic nucleus in primates. A neuroan-atomical and immunohistochemical study. In: Crossman AR, Sambrook MA (eds) Neural mechanisms in disorders of movement. Current problems in neurology, vol 9. Libbey, London, pp 29–35
Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd ed. Academic Press, Australia
Richfield EK, Young AB, Penney JB (1987) Comparative distribution of D 1 and D 2 receptors in the basal ganglia of turtles, pigeons, rats, cats and monkeys. J Comp Neurol 262: 446–463
Robledo P, Feger J (1990) Excitatory influence of rat subthalamic nucleus to substantia nigra pars reticulata and the pallidal complex: electrophysiological data. Brain Res 518: 47–54
Rouzaire-Dubois B, Hammond C, Hamon B, Feger J (1980) Pharmacological blockade of the globus pallidus-induced inhibitory responses of the subthalamic cells in the rat. Brain Res 200: 321–329
Rouzaire-Dubois B, Scarnati E (1985) Bilateral corticosubthalamic nucleus projections: an electrophysiological study in rats with chronic cerebral lesions. Neuroscience 5: 69–79
Ruffieux A, Schultz W (1981) Influence de la dopamine sur les neurones de la pars réticulata de la substance noire. J Physiol (Paris) 77: 63–69
Segovia J, Tossman U, Herrera-Marschitz M, Garcia-Munoz M, Ungerstedt U (1986) Gamma-aminobutyric acid release in the globus pallidus in vivo after 6-hydroxydopamine lesion in the substantia nigra of the rat. Neurosci Lett 70: 364–368
Van Der Kooy D, Hattori T (1980) Single subthalamic neurons project to both the globus pallidus and the substantia nigra in the rat. J Comp Neurol 192: 751–790
Waszczak BL, Walters JR (1983) Dopamine modulation of the effects of gamma-aminobutyric acid on substantia nigra pars reticulata neurons. Science 220: 218–221
Waszczak BL, Walters JR (1986) Endogenous dopamine can modulate inhibition of substantia nigra reticulata neurons elicited by GABA iontophoresis or striatal stimulation. J Neurosci 6: 120–126
Yamamura T, Harada K, Okamura A, Kemmotsu O (1990) Is the site of action of ketamine anesthesia the N-methyl-D-aspartate receptor? Anesthesiology 72: 704–710
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Robledo, P., Feger, J. Acute monoaminergic depletion in the rat potentiates the excitatory effect of the subthalamic nucleus in the substantia nigra pars reticulata but not in the pallidal complex. J. Neural Transmission 86, 115–126 (1991). https://doi.org/10.1007/BF01250572
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DOI: https://doi.org/10.1007/BF01250572