Role of Gabaergic and Glycinergic Transmissions in the Substantia Nigra in the Regulation of Dopamine Release in the Cat Caudate Nucleus

  • A. Chéramy
  • A. Nieoullon
  • J. Glowinski
Part of the NATO Advanced Study Institutes Series book series (NSSA, volume 16)


It is well known that the substantia nigra contains numerous GABAergic terminals (Fonnum et al., 1974; Kataoka et al., 1974; Bak et al., 1975; Ribak et al., 1976). Most of these originate from the striatum (Feltz, 1971; Precht and Yoshida, 1971; Crossman et al., 1973; Fonnum et al., 1974; Kataoka et al.,1974; Bak et al., 1975; Dray et al.,1976) and/or the globus pallidus (Hattori et al.,1973,1975). According to electrophysiological studies, some of the striato-nigral inhibitory neurons projecting into the substantia nigra are involved in the regulation of the activity of an important nigro-thalamic pathway (Albe-Fessard et al., 1975; Deniau et al.,1976). It is also generally assumed that descending GABAergic neurons contribute to the control of the activity of the nigro-striatal dopaminergic neurons. Several electrophysiological (Aghajanian and Bunney, 1975), biochemical (Anden and Stock, 1973; Lloyd et al., 1977) and pharmacological (Tarsy et al., 1975) studies have suggested that these GABAergic neurons exert a direct inhibitory action on the dopaminergic neurons. Besides this direct inhibitory input on dopaminergic neurons, other GABAergic neurons projecting into the pars reticulata could indirectly exert a facilitatory control on dopaminergic neurons by inhibiting nigral inhibitory interneurons (Dray and Straughan, 1976; Fahn, 1976; Chéramy et al., 1977c).


Substantia Nigra Dopaminergic Neuron Caudate Nucleus Brain Research GABAergic Neuron 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aghajanian, G.K., and Bunney, B.S., 1975, Dopaminergic and non-dopaminergic neurons of the substantia nigra: differential responses to putative transmitters, in: “Neuropsychopharmacology”, pp 442–452 ( J.R. Boissier, H. Hippius, & P. Pichot, eds) Excerpta Medica, Amsterdam & American Elsevier Pub.Co. Inc. N.Y.Google Scholar
  2. Alber-Fessard, D., Deniau, J.P., Feger, J., LacKner, D., Jacquemin, J., and Ohye, C., 1975, Reciprocal connections between the striatum, the substantia nigra and the ventrolateral nucleus of the thalamus, in: “Neuropsychopharmacology” pp 434–443 ( J.R. Boissier, H. Hippius and P. Pichot, eds),Excerpta Pledica, Amsterdam & American Elsevier Pub.Co.Inc. N.Y.Google Scholar
  3. Anden, N.E., and Stock, G., 1973, Inhibitory effect of gamma-hydroxybutyric acid and gamma-aminobutyric acid on the dopamine cells in the substantia nigra. Naunyn-Schmiedeberg’s Arch. Pharmacol. 279: 89–92Google Scholar
  4. Bak, I.J., Choi, W.B., Hassler, R., Usunoff, K.G., and Wagner, A., 1975, Fine structural synaptic organization of the corpus striatum and substantia nigra in rat and cat, in: “Advances Neurol”. Vol. 9, pp 25–41 ( D. B. Calne, T.N. Chase & A. Barbeau, eds) Raven Press, N.Y.Google Scholar
  5. Chan-Palay, V., 1977, Cerebellar dentate nucleus: organization, cytology and transmitters, p. 202, Springer Verlag, BerlinGoogle Scholar
  6. Chéramy, A., Nieoullon, A., and Glowinski, J., 1977a, Effects of peripheral and local administration of Picrotoxin on the release of newly synthesized 3H-dopamine in the caudate nucleus of the cat. Naunyn Schmiedeberg’s Arch.Pharmacol. 297: 31–37PubMedCrossRefGoogle Scholar
  7. Chéramy, A., Nieoullon, A., and Glowinski, J., 1977b, Blockade of the picrotoxin-induced in vivo release of dopamine in the cat caudate nucleus by diazepam, Life Sciences, 20: 811–816PubMedCrossRefGoogle Scholar
  8. Chéramy, A., Nieoullon, A., and Glowinski, J., 1977c, In vivo changes in dopamine release in the caudate nucleus and the substantia nigra of the cat induced by nigral application of various drugs including GABAergic agonists and antagonists, in: “Interactions among putative neurotransmitters in the brain” CS. Garattini, J.F. Pujol & R. Samanin, eds) Raven Press, N.Y. (in press)Google Scholar
  9. Chéramy, A., Nieoullon A., and Glowinski, J., 1977d, Stimulating effects of gamma-hydroxybutyrate on dopamine release from the caudate nucleus and the substantia nigra of the cat. J. Pharmacol, exp. Ther. (in press)Google Scholar
  10. Chéramy, A., Nieoullon, A., Michelot, R.,and Glowinski, J., 1977e, Effects of intranigral applications of dopamine and substance P. on the in vivo release of newly synthesized 3H-dopamine in the ispilateral caudate nucleus of the cat. Neurosci.Letters, 4: 105–109CrossRefGoogle Scholar
  11. Costa, E., Guidotti, A., Mao, C.C., and Suria, A., 1975, New concepts on the mechanism of action of benzodiazepines, Life Sci. 17: 167–186PubMedCrossRefGoogle Scholar
  12. Crossman, A.R., Walker, R.J.,and Woodruff, G.N., 1973, Picrotoxin antagonism of gamma-aminobutyric acid inhibitory responses and synaptic inhibition in the rat substantia nigra. Brit.J. Pharmacol. 49: 696–698Google Scholar
  13. Curtis, D.R., and Johnston, G.A.R., 1974, Amino acid transmitters in the mammalian central nervous system, Rev. Physiol., 69: 96–188Google Scholar
  14. Davies, J., and Dray, A., 1976, Substance P in the substantia nigra, Brain Research, 107: 623–627PubMedCrossRefGoogle Scholar
  15. Deniau, J.N., Feger, J., and Le Guyader, C., 1976, Striatal evoked inhibition of identified nigro-thalamic neurons, Brain Research, 104: 152–156PubMedCrossRefGoogle Scholar
  16. DiChiara, G., Porceddu, M.L., Spano, P.F., and Gessa, G.L., 1977, Haloperidol increases and apomorphine decreases striatal dopamine metabolism after destruction of striatal dopamine-sensitive-adenylate cyclase by kainic acid, Brain Research, 130: 374–382CrossRefGoogle Scholar
  17. Divac, I., Fonnum, F., and Storm-Mathisen, J., 1977, High affinity uptake of glutamate in terminals of cortico-striatal axons, Nature, 266: 377–378PubMedCrossRefGoogle Scholar
  18. Dray, A., and Gonye, T.J.,1975, Effects of caudate stimulation and microiontophoretically applied substances on neurons in the rat substantia nigra.J.Physiol.(Lond.) 246: 88–89Google Scholar
  19. Dray, A., Gonye, T.J., and Oakley, N.R., 1976, Caudate stimulation and substantia nigra activity in the rat. J. Physio 1.(Lond.,) 259: 825–849Google Scholar
  20. Dray, A., and Straughan, D.W., 1976, Synaptic mechanisms in the substantia nigra, J. Pharm. Pharmacol., 28: 400–405PubMedCrossRefGoogle Scholar
  21. Edwards, C., and Kuffler, S.W., 1959, The blocking effect of aminobutyric acid (GABA) and the action of related compounds on single nerve cells. J. Neurochem. 4: 19–30PubMedCrossRefGoogle Scholar
  22. Fahn, S., 1976, Biochemistry of the basal ganglia, in:”Advances in Neurology’,’ Vol. 14, pp 59–88 ( R. Eldridge & S. Fahn, eds) Raven Press, N.Y.Google Scholar
  23. Feltz, P., 1971, Gamma-aminobutyric acid and a caudate-nigral inhi¬bition, Can. J.Physiol.Pharmacol. 49: 1113–1115CrossRefGoogle Scholar
  24. Fonnum, F., Grofova, I., Rinvik, E., Storm-Nathisen, J., and Walberg, F., 1974, Origin and distribution of glutamate decarboxylase in substantia nigra of the cat, Brain Research, 71: 77–92PubMedCrossRefGoogle Scholar
  25. Garcia-Nunoz, M., Nicolaou, N. N., Tulloch, I.F, Wright, A.K. and Arbuthnott, G.W., 1977, Feedback loop or output pathway in striato-nigral fibers ? Nature, 265: 363–365CrossRefGoogle Scholar
  26. Giorguieff, M.F., Le Floc’h, N.L., Westfall, T.C., Glowinski, J., and Besson, M.J., 1976, Nicotinic effect of acetylcholine on the release of newly synthesized 3H-dopamine in rat slices and cat caudate nucleus, Brain Research, 106: 117–131PubMedCrossRefGoogle Scholar
  27. Giorguieff, M.F., Kemel, H.L., and Glowinski, J., 1977, Presynaptic effect of L-glutamic acid on the reLease of dopamine in rat striatal slices. Neurosci.Lett. (in press)Google Scholar
  28. Haefely, W., Kulcsar, A., Möhler, H., Pieri, L., Pole, P., and Schaffner, R., 1975, Possible involvement of the central actions of benzodiazepines, Adv. Biochem. Psychopharmacol. 10: 131–152Google Scholar
  29. Hattori, T., HcGeer, P.L., Fibiger, H.C., and McGeer, E.G, 1973, On the source of GABA containing terminals in the substantia nigra: electron microscopic autoradiographic and biochemical studies, Brain Research, 54: 103–114PubMedCrossRefGoogle Scholar
  30. Hattori, T., Fibiger, H.C., and McGeer, P.L., 1975, Demonstration of a pallido-nigral projection innervating dopaminergic neurons, J. Comp. Neurol. 162: 487–504PubMedCrossRefGoogle Scholar
  31. Kataoka, K., Bäk, I.J., Hassler, R., Kim, J.S., and Wagner, A., 1974, L-glutamate decarboxylase and choline acetyltransferase activity in the substantia nigra and the striatum after surgical interruption of the striato-nigral fibers of the baboon, Exp. Brain Research, 19: 217–227Google Scholar
  32. Krnjevic, K., 1974, Chemical nature of synaptic transmission in vertebrates, Physiol.Rev. 54: 418–540Google Scholar
  33. Lloyd, K.G., Shemen, L., and Hornykiewicz, Q., 1977, Distribution of high affinity sodium-independent (3H)-gamma-aminobutyric acid ((3H)GABA) binding in the human brain: alterations in Parkinson’s disease, Brain Research, 127: 269–278CrossRefGoogle Scholar
  34. McGeer, E.G., Innanen, V.T., and McGeer, P.L., 1976, Evidence on the cellular localization of adenyl cyclase in the neostriatum Brain Research, 118: 356–358Google Scholar
  35. McLennan, H., 1964, The release of acetylcholine and,3-hydroxy-tyramine from the caudate nucleus, J. Physiol.(Lond.) 174: 152–161Google Scholar
  36. Nieoullon, A., Cheramy, A., and Glowinski, J., 1977a, 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. J. Neurochem. 28: 819–828PubMedCrossRefGoogle Scholar
  37. Nieoullon, A., Cheramy, A., and Glowinski, J., 1977b, Release of dopamine evoked under punctate electrical stimulations of the motor and visual areas of the cerebral cortex in both caudate nucleus and in the substantia nigra in the cat. Brain Research, (in press)Google Scholar
  38. Perry, T.L., Berry, K., Hansen, S., Diamond, S., and Mok, C., 1971, Regional distribution of amino-acids in human brain obtained at autopsy, J. Neurochem. 18: 513–519PubMedCrossRefGoogle Scholar
  39. Pole, P., Mohler, H., and Haefely, W., 1974, The effect of diazepam on spinal cord activities: possible site and mechanisms of action. Naunyn Schmiedeberg’s Arch. Pharmacol. 284: 319–337Google Scholar
  40. Pole, P., and Haefely, W., 1976, Effects of two benzodiazepines, phenobarbitone, and baclofen on synaptic transmission in the cat cuneate nucleus, Naunyn Schmiedeberg’s Arch.Pharmaco1. 294: 121–131CrossRefGoogle Scholar
  41. Precht, W. and Yoshida, M., 1971, Blockade of caudate-evoked inhibition of neurons in the substantia nigra by picrotoxin, Brain Research, 32: 229–233PubMedCrossRefGoogle Scholar
  42. Racagni, G., Bruno, F., Maggi, A., Cattabeni, F., and Groppetti, A., 1977, Functional interactions between dopamine and GABA in the nigro-striatal system. 6th International meeting of the International Society for Neurochemistry, Satellite Symposium on dopamine, Southampton.Google Scholar
  43. Ribak, C.E., Vaughn, I.E., Saito, K., Barker, R., and Roberts, E., 1976, Immunocytochemical localization of glutamate decarboxylase in rat substantia nigra, Brain Research, 116: 287–298PubMedCrossRefGoogle Scholar
  44. Schaffner, R., and Haefely, W., 1975, The effects of diazepam and bicuculline on the strio-nigral evoked potentials, Experientia (Basel) 31: 732Google Scholar
  45. Simke, J.P., and Saelens, J.K., 1977, Evidence for a cholinergic fiber tract connecting the thalamus with the head of the striatum of the rat. Brain Research, 126: 487–495PubMedCrossRefGoogle Scholar
  46. Tarsy, D., Pycock, C., Meldrum, B., and Marsden, C.D., 1975, Rotatio nal behavior induced in rats by intranigral picrotoxin, Brain Research, 89: 160–165PubMedCrossRefGoogle Scholar
  47. Tebecis, A.K., 1974, Transmitters and identified neurons in the mammalian central nervous system, Scientechnica Ltd, BristolGoogle Scholar
  48. Usunoff, K.G., Hassler, R., Romansky, K., Usunova, P., and Wagner, A., 1976, The nigrostriatal projection in the cat, Part 1, Silver impregnation method. J. Neurol. Sci. 28: 265–288PubMedCrossRefGoogle Scholar
  49. Wagner, A., Hassler, R., and Kim, J.S., 1975, Striatal cholinergic enzyme activities following discrete centromedian nucleus lesion in cat thalamus, Trans, int. Soc. Neurochem. (Barcelona) abst. 59, p. 116Google Scholar

Copyright information

© Plenum Press, New York 1978

Authors and Affiliations

  • A. Chéramy
    • 1
  • A. Nieoullon
    • 1
  • J. Glowinski
    • 1
  1. 1.Groupe NB, INSERM U.114Collège de FranceParis 5eF

Personalised recommendations