Summary
This study investigated the effect of strio-nigral hemitransection on the enzymes necessary for the synthesis and cataboiism of γ-aminobutyric acid, acetylcholine and dopamine in the caudate nucleus, the putamen, the pallidum and the substantia nigra of the baboon. After transection, more than 70% of the L-glutamate decarboxylase activity was missing from the substantia nigra ipsilateral to the location of the lesions, leaving all remaining regions unchanged. Choline acetyltransferase, acetylcholinesterase and monoaminoxidase activities failed, however, to be affected by the lesions, while glutamic-γ-aminobutyric transaminase was slightly decreased in the substantia nigra. These results strongly support our previous view that the strio-nigral neuron system is primarily an inhibitory one, in which γ-aminobutyric acid plays the role of transmitter. Confirming earlier investigations, a marked reduction of L-DOPA decarboxylase activity was induced by the lesions in the caudate nucleus and the putamen, which indicates that the nigro-striatal neuron system in the baboon is also dopaminergic. Neither the striatum nor the substantia nigra had a markedly diminished acetylcholine content after hemitransection. This strongly suggests that the acetylcholine in the striatum does not depend on the integrity of the strio-nigral connexions.
Similar content being viewed by others
References
Albers, R.W., Brady, R.O.: The distribution of glutamic decarboxylase in the nerve system of rhesus monkey. J. biol. Chem. 234, 926–928 (1959)
Andén, N.E., Carlsson, A., Dahlström, A., Fuxe, K., Hillarp, N.A., Larsson, K.: Demonstrating and mapping out of nigro-neostriatal dopamine neurons. Life Sci. 3, 523–530 (1964)
—, Dahlström, A., Fuxe, K., Larsson, K.: Further evidences for the presence of nigro-striatal dopamine neurons in the rat. Amer. J. Anat. 116, 329–333 (1965)
—, Fuxe, K., Hamberger, B., Hökfelt, T.: A quantitative study on the nigro-neostriatal dopamine neuron system in the rat. Acta physiol. scand. 67, 306–312 (1966)
—, Dahlström, A., Fuxe, K., Larsson, K., Olson, L., Ungerstedt, U.: Ascending monoamine neurons to the telencephalon and diencephalon. Acta physiol. scand. 67, 313–326 (1966)
Bak, I.J., Hassler, R., Kim, J.S., Kataoka, K.: Amantadine actions on acetylcholine and GABA in striatum and substantia nigra of rat in relation to behavioral changes. J. Neurol. Transmis. 33, 45–61 (1972)
Bedard, P., Larochelle, L., Parent, A., Poirier, L.: The nigrostriatal pathway: a correlative study based on neuroanatomical and neurochemical criteria in the cat. Exp. Neurol. 25, 365–377 (1969)
Bertler, A., Falck, B., Gottfries, C.G., Ljundgren, L., Rosengren, E.: Some observations on adrenergic connections between mesencephalon and cerebral hemispheres. Acta pharmacol. (Kbh.) 21, 283–289 (1964)
Bonta, I.L., De Vos, C.J., Grijsen, H., Hillen, F.C., Noach, E.L., Sim, A.W.: 1-hydroxy-3-amino-pyrrolidon-2 (HA-966): A new GABA-like compound, with potential use in extrapyramidal diseases. Brit. J. Pharmacol. 43, 514–535 (1971)
Carlsson, A., Falck, B., Hillarp, A.: Cellular localization of monoamines by a fluorescence method. Acta physiol. scand. 56, Suppl. 196, 1–26 (1962)
Dahlström, A., Fuxe, K.: Evidence for the existence of monoamine containing neurons in the central nervous system. 1. Demonstration of monoamines in the cell bodies of brain stem neurons. Acta physiol. scand. 62, Suppl. 232, 1–55 (1964)
De Robertis, E., Rodriguez De Lores Arnaiz G., Salganicoff, L., Pelegrino De Iraldi, A., Zieher, L.M.: Isolation of synaptic vesicles and structural organization of the acetylcholine system within nerve endings. J. Neurochem. 10, 225–235 (1963)
Eccles, J.C., Schmidt, R., Willis, W.D.: Pharmacological studies on presynaptic inhibition. J. Physiol. (Lond.) 168, 500–530 (1963)
Ellman, G.L., Courtney, K.D., Andres, V., Jr., Faetherstone, R.M.: A new and rapid calorimetric determination of acetylcholine esterase activity. Biochem. Pharmacol. 7, 88–95 (1961)
Fahn, S., Côté, L.J.: Regional distribution of γ-aminobutyric acid (GABA) in brain of the Rhesus monkey. J. Neurochem. 15, 209–213 (1968)
Faull, R.L.M., Laverty, R.: Changes in dopamine levels in the corpus striatum following lesions in the substantia nigra. Exp. Neurol. 23, 332–340 (1969)
Feltz, P.: γ-aminobutyric acid and a caudato-nigral inhibition. Can. J. Physiol. Pharmacol. 49, 1113–1115 (1971)
Fonnum, F.: The distribution of glutamate decarboxylase, and aspartate transaminase in subcellular fractions of rat and guinea pig brain. Biochem. J. 106, 401–412 (1968)
Fuxe, K., Hökfelt, T., Nilsson, O.: Observations on the cellular localization of dopamine in the caudate nucleus of the rat. Z. Zellforsch. 63, 701–706 (1964)
Gessa, G.L., Spano, P.F., Vargiu, L., Crabai, F., Tagliamonte, A., Mameli, L.: Effect of 1,4-butanediol and other butyric acid congeners on brain catecholamines. Life Sci. 7, 289–298 (1968)
Goldstein, M., Anagnoste, B., Battista, A.F., Owen, W.S., Nakatani, S.: Studies of amines in striatum in monkeys with nigral lesions —disposition, biosynthesis and metabolism of [H3]-dopamine and [14C]-serotonin in the striatum. J. Neurochem. 16, 645–653 (1969)
Grofová, I., Rinvik, E.: An experimental electron-microscopic study on the strionigral projection in the cat. Exp. Brain Res. 11, 249–262 (1970)
Gumulka, W., Ramirez del Angel, A., Samanin, R., Valzelli, L.: Lesion of the substantia nigra: biochemical and behavioral effects in rats. Europ. J. Pharmacol. 10, 79–82 (1970)
Gray, E.G., Whittaker, V.P.: The isolation of nerve endings from brain: an electron microscopic study of cell fragments derived by homogenization and centrifugation J. Anat. (Lond.) 96, 79–88 (1962)
Hassler, R.: Über die afferente Leitung und Steuerung des striären Systems. Nervenarzt 20, 537–541 (1949)
Hassler, R. Kim, J.S., Okada, Y., and, Bak, I.J.: A type of strio-nigral neurons with high GABA content in rat and monkey. Abstr. Third Intern. Meet. Intern. Soc. Neurochem., p. 398. Budapest: 1971
— Physiopathology of Rigidity. In: Parkinson's Disease; Rigidity, Akinesia, Behavior, Vol. 1, pp. 20–45. Ed. by J. Siegfried. Bern: H. Huber 1972
Hassler, R. Hajdu, F., Bak, I.J.: Über die 6 verschiedenen Typen von Synapsen im elektronenmikroskopischen Längsschnitt der Substantia nigra bei der Ratte. Anat. Anz. (in press, 1973)
Hebb, C.O., Whittaker, V.P.: Intracellular distributions of acetylcholine and choline acetylase. J. Physiol. (Lond.) 142, 187–196 (1958)
Hökfelt, T., Johnson, G., Ljungdahl, A.: Regional uptake and subcellular localization of H3-gamma-aminobutyric acid (GABA) in rat brain slices. Life Sci. 9, 203–212 (1970)
Hornykiewicz, O.: Dopamine (3-hydroxytyramine) and brain function. Pharmacol. Rev. 18, 925–964 (1966)
Jerusalem, F.: Doppeltblindstudie über den antispastischen Effekt von β-(4-Chlorphenyl-) γ-Aminobuttersäure (CIBA) bei multipler Sklerose. Nervenarzt 39, 515–517 (1968)
Kataoka, K., Bak, I. J., Hassler, R., Kim, J.S., Wagner, A.: Effect of strio-nigral interruption on the activities of glutamic decarboxylase (GAD), GABA-transaminase (GABA-T), DOPA decarboxylase and monoamine oxidase (MAO) in the substantia nigra and the corpus striatum of the baboon. Vth Internat. Congress Pharmacol., San Fransisco abst. 121 (1972)
Kim, J.S., Bak, I.J., Hassler, R., Okada, Y.: Role of γ-aminobutyric acid (GABA) in the extrapyramidal motor system. 2. Some evidence for the existence of a type of GABA-rich strio-nigral neurons. Exp. Brain Res. 14, 95–104 (1971)
Kuriyama, K., Roberts, E., Kakefuda, T.: Association of the γ-aminobutyric acid system with a synaptic vesicle fraction from mouse brain. Brain Res. 8, 132–152 (1968)
Lewis, P.R., Shute, C.C.D., Silber, A.: Confirmation from choline acetylase analyses of a massive cholinergic innervation to the rat hippocampus. J. Physiol. (Lond.) 191, 215–224 (1967)
Lloyd, K., Hornykiewicz, O.: Occurrence and distribution of L-DOPA decarboxylase in the human brain. Brain Res. 22, 426–428 (1970)
Lowe, I.P., Robins, E., Eyerman, G.S.: The fluorimetric measurement of the glutamic acid decarboxylase and its distribution in brain. J. Neurochem. 3, 8–18 (1958)
McCaman, R.E., Hunt, J.M.: Microdetermination of choline acetylase in nervous tissue. J. Neurochem. 12, 253–259 (1965)
Moore, R.Y., Heller, A.: Subcortical systems participating in the control of caudate nucleus dopamine content. In: Progress in Neurogenetics, pp. 276–282. Ed. by A. Barbeau and J.R. Brunette. Amsterdam: Excerpta Medica 1969
—, Bhatuagar, R.K., Heller, A.: Anatomical and chemical studies of a nigro-neostriatal projection in the cat. Brain Res. 30, 119–135 (1971)
Müller, P.B., Langemann, H.: Distribution of glutamic acid decarboxylase activity in human brain. J. Neurochem. 9, 399–401 (1962)
Niimi, K., Ikeda, T., Kawamura, S., Inoshita, H.: Efferent projections of the head of the caudate in the cat. Brain Res. 21, 327–344 (1970)
Nybäck, H., Sedvall, G.: Effect of nigral lesion of chlorpromazine-induced acceleration of dopamine synthesis from [14C]tyrosine. J. Pharm. Pharmacol. 23, 322–326 (1971)
Okada, Y., Nitsch-Hassler, C., Kim, J.S., Bak, I.J., Hassler, R.: Role of γ-aminobutyric acid (GABA) in the extrapyramidal motor system. Exp. Brain Res. 13, 514–518 (1971)
—, Hassler, R.: Uptake and release of γ-aminobutyric acid (GABA) in slices of substantia nigra of rat. Brain Res. 49, 214–217 (1973)
Olivier, A., Parent, A., Simard, H., Poirier, L.J.: Cholinesteratic striopallidal and strionigral efferents in the cat and the monkey. Brain Res. 18, 273–282 (1970)
Poirier, L.J., Sourkes, T.R.: Influence of the substantia nigra on the catecholamine content of the striatum. Brain 88, 181–192 (1965)
—, Singh, P., Boucher, R., R., Bouvier, G., Olivier, A., Larochelle, P.: Effect of brain lesions on striatal monoamines in the cat. Arch. Neurol. (Chic.) 17, 601–608 (1967)
—, Sourkes, T.L., Boucher, R.: Effect of amine precursors on the concentration of striatal dopamine and serotonin in cats with and without unilateral brain stem lesion. Brain Res. 6, 654–666 (1967)
Precht, W., Yoshida, M.: Blockade of caudate-evoked inhibition of neurons in the substantia nigra by picrotoxin. Brain Res. 32, 229–233 (1971)
Riese, W.: Zur vergleichenden Anatomie der striofugalen Faserung. Anat.Anz. 57, 487–494 (1924)
Rundles, R.W., Papez, J.W.: Connections between the striatum and the substantia nigra in a human brain. Arch. Neurol. Psychiat. (Chic.) 38, 550–562 (1937)
Salganicoff, L., De Robertis, E.: Subcellular distribution of the enzymes of the glutamic acid, glutamine and γ-aminobutyric acid cycles in rat brain. J. Neurochem. 12, 287–309 (1965)
Salvador, R.A., Albers, R.W.: The distribution of glutamic-γ-aminobutyric transaminase in the nervous system of rhesus monkey. J. biol. Chem. 234, 922–925 (1959)
Szabo, J.: Topical distribution of the striatal efferents in the monkey. Exp. Neurol. 5, 21–36 (1962)
Van Kempen, G.M.I., Van der Berg, G.I., Van der Helm, H.I., Veldstra, H.: Intracellular localization of glutamate decarboxylase, γ-aminobutyric transaminase and some other enzymes in brain tissue. J. Neurochem. 7, 581–589 (1965)
Vogt, C., Vogt, O.: Sitz und Wesen der Krankheiten im Lichte der topistischen Hirnforschung und des Variierens der Tiere. I. J. Psychol. (Lpz.), 47, 237–457 (1937)
Voneida, T.: An experimental study of the course and destination of fibres arising in the head of the caudate nucleus in the cat and the monkey. J. comp. Neurol. 115, 78–87 (1960)
Whittaker, V.P.: The application of subcellular fractionation techniques to the study of brain function. Progress in Biophysics and Molecular Biology, vol. 15, pp. 41–96. London: Pergamon Press 1965
Wagner, A.: Veränderungen der Gamma-Aktivität durch Reizungen im Zwischen-und Mittelhirn bei der Katze. In: Progress in Brain Research-Vol. 5, Lectures on the Diencephalon, p. 67–73. Ed. by W. Bargmann and J.P. Schadé. Amsterdam: 1964
Wurtman, R.J., Axelrod, J.: A sensitive and specific assay for the estimation of monoamine oxidase. Biochem. Pharmacol. 12, 1439–1441 (1963)
Yoshida, M., Precht, W.: Monosynaptic inhibition of neurons of the substantia nigra by caudato-nigral fibers. Brain Res. 32, 225–228 (1971)
Author information
Authors and Affiliations
Additional information
Visiting scientist from Department of Physiology, Kyoto University School of Medicine, 606 Kyoto (Japan)
Rights and permissions
About this article
Cite this article
Kataoka, K., Bak, I.J., Hassler, R. et al. L-glutamate decarboxylase and Choline acetyltransferase activity in the substantia nigra and the striatum after surgical interruption of the strio-nigral fibres of the baboon. Exp. Brain Res. 19, 217–227 (1974). https://doi.org/10.1007/BF00238536
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00238536