Chemical Anatomy of the Basal Ganglia in Primates

  • A. Parent
  • Y. Smith
  • M.-Y. Arsenault
Part of the Advances in Behavioral Biology book series (ABBI, volume 32)


This paper summarizes the results of our recent studies of the cellular localization of different neurotransmitters or neurotransmitter-related substances within the basal ganglia of the squirrel monkey (Saimiri sciureus). Although most of these results pertained to the primate striatum, other components of the basal ganglia in monkeys as well as some data obtained in rats and cats will also be considered. The distribution and morphological characteristics of cholinergic neurons such as visualized by means of a pharmacohistochemical technique to reveal the acetylcholinesterase (AChE) or the immunohistochemical identification of choline acetyltransferase (ChAT) will be described first. This will be followed by a survey of the immunohistochemical localization of three different neuropeptides: (1) neuropeptide Y (NPY) belonging to the pancreatic polypeptide family, (2) enkephalins (ENK), a member of the abundant and highly diversified family of opiate peptides, and (3) substance P (SP) belonging to the tachykinin family. Then, a summary of the distribution of gamma-aminobutyric acid (GABA)-immunoreactive cell bodies and terminals in the basal ganglia and of dopamine (DA)-immunoreactive cell bodies in the midbrain of the squirrel monkey will be provided. Finally, the significance of all these findings will be discussed in the light of the wealth of information presently available on the complex organization of the various chemospecific neuronal systems involved in the functional organization of the primate basal ganglia.


Substantia Nigra Ventral Tegmental Area Caudate Nucleus Cholinergic Neuron Globus Pallidus 
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. Araki, M., McGeer, P.L. and McGeer, E.G., 1984, Retrograde HRP tracing combined with a pharmacohistochemical method for GABA Transaminase for the identification of presumptive GABAergic projections to the habenula, Brain Res., 304: 271–277.PubMedCrossRefGoogle Scholar
  2. Araki, M., McGeer, P.L. and McGeer, E.G., 1985a, Striatonigral and pallidonigral pathways studied by a combination of retrograde horseradish peroxidase tracing and a pharmacohistochemical method for γ-aminobutyric acid transaminase, Brain Res., 331: 17–24.PubMedCrossRefGoogle Scholar
  3. Araki, M., McGeer, P.L. and McGeer, E.G., 1985b, Presumptive γ-aminobutyric acid pathways from the midbrain to the superior colliculus studied by combined horseradish peroxidase-γ-aminobutyric acid transaminase pharmacohistochemical method, Neuroscience, 13: 433–439.CrossRefGoogle Scholar
  4. Armstrong, D.M., Saper, C.B., Levey, A.I., Wainer, B.H. and Terry, R.D., 1983, Distribution of cholinergic neurons in rat brain: demonstrated by the immunocytochemical localization of choline acetyltransferase, J. Comp. Neurol., 216: 53–68.PubMedCrossRefGoogle Scholar
  5. Aronin, N., DiFiglia, M., Graveland, G.A., Schwartz, W.J. and Wu, J.-Y., 1984, Localization of immunoreactive enkephalins in GABA synthesizing neurons in the rat neostriatum, Brain Res., 300: 376–380.PubMedCrossRefGoogle Scholar
  6. Beach, T.G. and McGeer, E.G., 1984, The distribution of substance P in the primate basal ganglia: An immunohistochemical study of baboon and human brain, Neuroscience, 13: 29–52.PubMedCrossRefGoogle Scholar
  7. Beal, M.F., Frank, R.C., Ellison, D.W. and Martin, J.B., 1986, The effect of neuropeptide Y on striatal catecholamines, Neurosci. Lett., 71: 118–123.PubMedCrossRefGoogle Scholar
  8. Beal, M.F. and Martin, J.B., 1984, The effect of somatostatin on striatal catecholamines, Neurosci. Lett., 44: 271–276.PubMedCrossRefGoogle Scholar
  9. Beckstead, R.M. and Cruz, C.J., 1986, Striatal axons to the globus pallidus, entopeduncular nucleus and substantia nigra come mainly from separate cell populations in cat, Neuroscience, 19: 147–158.PubMedCrossRefGoogle Scholar
  10. Beckstead, R.M. and Kersey, K.S., 1985, Immunohistochemical demonstration of differential substance P-, met-enkephalin-, and glutamic-acid-decarboxylase-containing cell body and axon distributions in the corpus striatum of the cat, J. Comp. Neurol., 232: 481–498.PubMedCrossRefGoogle Scholar
  11. Benoit, R., Bohlen, P., Ling, N., Briskin, A., Esch, F., Brazeau, P., Ying, S.-Y. and Guillemin, R., 1982, Presence of somatostatin-28 (1–12) in hypothalamus and pancreas, Proc. Natl Acad. Sci. (USA), 79: 917–921.CrossRefGoogle Scholar
  12. Bishop, G.A., Chang, H.T. and Kitai, S.T., 1982, Morphological and physiological properties of neostriatal neurons: An intracellular horseradish peroxidase study in the rat, Neuroscience, 7: 179–191.PubMedCrossRefGoogle Scholar
  13. Björklund, A. and Lindvall, O., 1984, Dopamine-containing systems in the CNS, in: “Handbook of Chemical Neuroanatomy: Classical Transmitters in the CNS”, Vol. 2, Part I, A. Björklund and T. Hökfelt, eds., Elsevier, Amsterdam.Google Scholar
  14. Bolam, J.P., Clark, D.J., Smith, A.D., and Somogyi, P., 1983, A type of aspiny neuron in the rat neostriatum accumulates [3H]-γ-aminobutyric acid: Combination of Golgi-staining, autoradiography, and electron microscopy, J. Comp. Neurol., 213: 121–134.PubMedCrossRefGoogle Scholar
  15. Bolam, J.P., Ingham, C.A. and Smith, A.D., 1984a, The section-Golgiimpregnation procedure. 3. Combination of Golgi impregnation with enzyme histochemistry and electron microscopy to characterize acetylcholinesterase-containing neurons in the rat neostriatum, Neuroscience, 12: 687–709.PubMedCrossRefGoogle Scholar
  16. Bolam, J.P., Powell, J.F., Totterdell, S. and Smith, A.D., 1981, The proportion of neurons in the rat neostriatum that project to the substantia nigra demonstrated using horseradish peroxidase conjugated with wheat-germ agglutinin, Brain Res., 220: 339–343.PubMedCrossRefGoogle Scholar
  17. Bolam, J.P., Powell, J.F., Wu, J.-Y. and Smith, A.D., 1985, Glutamate decarboxylase-immunoreactive structures in the rat neostriatum: A correlated light and electron microscopic study including a combination of Golgi impregnation with immunohistochemistry, J. Comp. Neurol., 237: 1–20.PubMedCrossRefGoogle Scholar
  18. Bolara, J.P., Wainer, B.H. and Smith, A.D., 1984b, Characterization of cholinergic neurons in the rat neostriatum. A combination of choline acetyltransferase immunocytochemistry, Golgiimpregnation and electron microscopy, Neuroscience, 12: 711–718.CrossRefGoogle Scholar
  19. Bouras, C., Taban, C.H. and Constantinidis, J., 1984, Mapping of enkephalin in human brain. An immunofluorescence study on brains from patients with senile and presenile dementia, Neuroscience, 12: 179–190.PubMedCrossRefGoogle Scholar
  20. Brann, M.R. and Emson, P.C., 1980, Microiontophoretic injection of fluorescent tracer combined with simultaneous immunofluorescent histochemistry for the demonstration of efferents from the caudate-putamen projecting to the globus pallidus, Neurosci. Lett., 16: 61–65.PubMedCrossRefGoogle Scholar
  21. Brownstein, M.J., Mroz, E.A., Tappaz, M.L. and Leeman, S.E., 1977, On the origin of substance P and glutamic acid decarboxylase (GAD) in the substantia nigra, Brain Res., 135: 315–323.PubMedCrossRefGoogle Scholar
  22. Butcher, L.L., Talbot, K. and Bilezikjian, L., 1975, Acetylcholinesterase neurons in dopamine-containing regions of the brain, J. Neural Transm., 37: 127–153.PubMedCrossRefGoogle Scholar
  23. Butcher, L.L. and Woolf, N.J., 1984, Histochemical distribution of acetylcholinesterase in the central nervous system: Clues to the localization of cholinergic neurons,in: “Handbook of Chemical Neuroanatomy: Classical Transmitters in the CNS”, Vol. 3, Part II, A. Björklund, T. Hökfelt and M.J. Kuhar, eds., Elsevier, Amsterdam.Google Scholar
  24. Cajal, S. Ramon y, 1895, Sur le corps strié, Bibl. Anat. (Basel), 3: 58–62.Google Scholar
  25. Cheramy, A., Leviel, V. and Glowinski, J., 1981, Dendritic release of dopamine in the substantia nigra, Nature, 289: 537–542.PubMedCrossRefGoogle Scholar
  26. Chesselet, M.F. and Graybiel, A.M., 1986, Striatal neurons expressing somatostatin-like immunoreactivity: Evidence for a peptidergic interneuronal system in the cat, Neuroscience, 17: 547–571.PubMedCrossRefGoogle Scholar
  27. Chevalier, G., Thierry, A.M., Shibazaki, T. and Féger, J., 1981, Evidence for a gabaergic inhibitory nigrotectal pathway in the rat, Neurosci. Lett., 21: 67–70.PubMedCrossRefGoogle Scholar
  28. Childs, J.A. and Gale, K., 1983, Neurochemical evidence for a nigrotegmental GABAergic projection, Brain Res., 258: 109–114.CrossRefGoogle Scholar
  29. Christensson-Nylander, I., Herrera-Marschitz, M., Staines, W., Hökfelt, T., Terenius, L., Ungerstedt, U., Cuello, C., Oertel, W. and Goldstein, M., 1986, Striato-nigral dynorphin and substance P pathways in the rat. I. Biochemical and immunohistochemical studies, Exp. Brain Res., 64: 169–192.PubMedCrossRefGoogle Scholar
  30. Chronwall, B.M., Dimaggio, D.A., Massari, V.J., Pickel, V.M., Ruggiero, D.A. and O’Donohue, T.L., 1985, The anatomy of neuropeptide-Y-containing neurons in rat brain, Neuroscience, 15: 1159–1181.PubMedCrossRefGoogle Scholar
  31. Coons, A.H., 1958, Fluorescent antibody methods, in: “General Cytochemical Methods”, J.F. Danielli, ed., Academic Press, New York.Google Scholar
  32. Cuello, A.C. and Kanazawa, I., 1978, The distribution of substance P immunoreactive fibers in the rat central nervous system, J. Comp. Neurol., 178: 129–150.PubMedCrossRefGoogle Scholar
  33. Cuello, A.C., and Paxinos, G., 1978, Evidence for a long leu-enkephalin striopallidal pathway in rat brain, Nature, 271: 178–180.PubMedCrossRefGoogle Scholar
  34. Dalhström, A. and Fuxe, K., 1964, Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brainstem neurons, Acta Physiol. Scand., Suppl. 232: 1–55.Google Scholar
  35. Dawbarn, D., De Quidt, M.E. and Emson, P.C., 1985, Survival of basal ganglia neuropeptide Y-somatostatin neurones in Huntington’s disease, Brain Res., 340: 251–260.PubMedCrossRefGoogle Scholar
  36. Dawbarn, D., Hunt, S.P. and Emson, P.C., 1984, Neuropeptide Y: regional distribution, chromatographic characterization and immunohistochemical demonstration in post-mortem human brain, Brain Res., 296: 168–173.PubMedCrossRefGoogle Scholar
  37. Del Fiacco, M., Dessi, M.L. and Levanti, M.C., 1984, Topographical localization of substance P in the human post-mortem brainstem. An immunohistochemical study in the newborn and adult tissue, Neuroscience, 12: 591–611.PubMedCrossRefGoogle Scholar
  38. Del Fiacco, M., Paxinos, G. and Cuello, A.C., 1982, Neostriatal enkephalin-immunoreactive neurones project to the globus pallidus, Brain Res., 231: 1–17.PubMedCrossRefGoogle Scholar
  39. Deniau, J.M., Lackner, D. and Féger, J., 1978, Effect of substantia nigra stimulation on identified neurons in the VL-VA thalamic complex: comparison between intact and chronically decorticated cats, Brain Res., 145: 27–35.PubMedCrossRefGoogle Scholar
  40. De Quidt, M.E. and Emson, P.C., 1986, Distribution of neuropeptide Y-like immunoreactivity in the rat central nervous system — II. Immunohistochemical analysis, Neuroscience, 18: 545–618.PubMedCrossRefGoogle Scholar
  41. DiCarlo, V., Hubbard, J.E. and Pate, P., 1973, Fluorescence histochemistry of monoamine-containing cell bodies in the brainstem of the squirrel monkey, J. Comp. Neurol., 152: 347–372.CrossRefGoogle Scholar
  42. DiChiara, G., Morelli, M., Porceddu, M.L., Mulas, M. and Del Fiacco, M., 1980, Effect of discrete kainic acid-induced lesions of the corpus caudatus and globus pallidus on glutamic acid decarboxylase or rat substantia nigra, Brain Res., 189: 193–208.CrossRefGoogle Scholar
  43. DiChiara, G., Porceddu, M.L., Morelli, M., Mulas, M.L. and Gessa, G.L., 1979, Evidence for gabaergic projection from the substantia nigra to the ventromedial thalamus and to the superior colliculus of the rat, Brain Res., 176: 273–284.CrossRefGoogle Scholar
  44. DiFiglia, M. and Aronin, N., 1982, Ultrastructural features of immunoreactive somatostatin neurons in the rat caudate nucleus, J. Neurosci., 2: 1267–1274.PubMedGoogle Scholar
  45. DiFiglia, M., Aronin, N. and Martin, J.B., 1982, Light and electron microscopic localization of immunoreactive leu-enkephalin in the monkey basal ganglia, J. Neurosci., 2: 303–320.PubMedGoogle Scholar
  46. DiFiglia, M., Aronin, N. and Leeman, S.E., 1981, Immunoreactive substance P in the substantia nigra of the monkey: light and electron microscopic localization, Brain Res., 233: 381–388.CrossRefGoogle Scholar
  47. DiFiglia, M., Pasik, P. and Pasik, T., 1976, A Golgi study of neuronal types in the neostriatum of monkeys, Brain Res., 114: 245–256.PubMedCrossRefGoogle Scholar
  48. Dimova, R., Vuillet, J. and Seite, R., 1980, Study of the rat neostriatum using a combined Golgi- electron microscope technique and serial sections, Neuroscience, 5: 1581–1596.PubMedCrossRefGoogle Scholar
  49. Domesick, V.B., Stinus, L. and Paskevitch, P.A., 1983, The cytology of dopaminergic and nondopaminergic neurons in the substantia nigra and ventral tegmental area of the rat: A light and electron-microscpic study, Neuroscience, 8: 743–765.PubMedCrossRefGoogle Scholar
  50. Eckenstein, F. and Sofroniew, M.V., 1983, Identification of central cholinergic neurons containing both choline acetyltransferase and acetylcholinesterase and of central neurons containing only acetylcholinesterase, J. Neurosci., 3: 2286–2291.PubMedGoogle Scholar
  51. Elde, R., Hökfelt, T., Johansson, O. and Terenius, L., 1976, Immunohistochemical studies using antibodies to leucine-enkephalin: Initial observations on the nervous system of the rat, Neuroscience, 1: 349–351.PubMedCrossRefGoogle Scholar
  52. Emson, P.C., Arregui, A., Clement-Jones, V., Sandberg, B.E. and Rossor, M., 1980, Regional distribution of met-enkephalin and substance P immunoreactivity in normal human brain and in Huntington’s disease, [Brain Res., 199: 147–160.PubMedCrossRefGoogle Scholar
  53. Fallon, J.H. and Leslie, F.M., 1986, Distribution of dynorphin and enkephalin peptides in the rat brain, J. Comp. Neurol., 249: 293–336.PubMedCrossRefGoogle Scholar
  54. Feiten, D.L., Laties, A.M. and Carpenter, M.B., 1974, Monoaminecontaining cell bodies in the squirrel monkey brain, Amer. J. Anat., 139: 153–166.CrossRefGoogle Scholar
  55. Felten, D.L. and Sladek Jr., J.R., 1983, Monoamine distribution in primate brain. V. Monoaminergic nuclei: Anatomy, pathways and local organization, Brain Res. Bull., 10: 171–284.PubMedCrossRefGoogle Scholar
  56. Ferrante, R.J., Kowall, N.W., Beal, M.F., Richardson Jr., E.P., Bird, E.D. and Martin, J.B., 1985, Selective sparing of a class of striatal neurons in Huntington’s disease, Science, 230: 561–563.PubMedCrossRefGoogle Scholar
  57. Finley, J.C.W., Maderdrut, J.L. and Petrusz, P., 1981, The Immunocytochemical localization on enkephalin in the central nervous system of the rat, J. Comp. Neurol., 198: 541–565.PubMedCrossRefGoogle Scholar
  58. Fisher, R.S., Buchwald, N.A., Hull, C.D. and Levine, M.S., 1986, The GABAergic striatonigral neurons of the cat: demonstration by double peroxidase labeling, Brain Res., 398: 148–156.PubMedCrossRefGoogle Scholar
  59. Fonnum, F., Gottesfeld, Z. and Grofova, I., 1978a, Distribution of glutamate decarboxylase, choline acetyltransferase and aromatic amino acid decarboxylase in the basal ganglia of normal and operated rats. Evidence for striatopallidal, striatoento-peduncular and striatonigral gabaergic fibers, Brain Res., 143: 125–138.PubMedCrossRefGoogle Scholar
  60. Fonnum, F., Grofova, I. and Rinvik, E., 1978b, Origin and distribution of glutamate decarboxylase in the nucleus subthalamicus of the cat, Brain Res., 153: 370–374.PubMedCrossRefGoogle Scholar
  61. Fonnum, F., Grofova, I., Rinvik, E., Storm-Mathisen, J. and Walberg, F., 1974, Origin and distribution of glutamate decarboxylase in the substantia nigra of the cat, Brain Res., 71: 77–92.PubMedCrossRefGoogle Scholar
  62. Fuxe, K., Agnati, L.F., Kalia, M., Goldstein, M., Andersson, K. and Härfstrand, A., 1985, Dopaminergic systems in the brain and pituitary,in: “The Dopaminergic System”, E. Flückiger, E.E. Müller and M.O. Thorner, eds., Springer-Verlag, Heidelberg.Google Scholar
  63. Gale, K., Hong, J.-S. and Guidotti, A., 1977, Presence of substance P and GABA in separate striatonigral neurons, Brain Res., 136: 371–375.PubMedCrossRefGoogle Scholar
  64. Garver, D.L. and Sladek, Jr., J.R., 1975, Monoamine distribution in primate brain. I. Catecholamine-containing perikarya in the brainstem of Macaca speciosa, J. Comp. Neurol., 159: 289–304.PubMedCrossRefGoogle Scholar
  65. Gaspar, P., Berger, B., Gay, M., Hamon, M., Cesselin, F., Vigny, A., Javoy-Agid, F. and Agid, Y., 1983, Tyrosine hydroxylase and methionine-enkephalin in the human mesencephalon, J. Neurol. Sci., 58: 247–267.PubMedCrossRefGoogle Scholar
  66. Gauchy, C., Beajouan, J.C., Besson, M.J., Kerdelhue, B., Glowinski, J. and Michelot, R., 1979, Topographical distribution of substance P in cat substantia nigra, Neurosci. Lett., 12: 127–131.PubMedCrossRefGoogle Scholar
  67. Geffard, M., Buijs, R.M., Séguéla, P., Pool, C.W. and LeMoal, M., 1984, First demonstration of highly specific and sensitive antibodies against dopamine, Brain Res., 294: 161–165.PubMedCrossRefGoogle Scholar
  68. Gottesfeld, Z., Brandon, C. and Wu, J.-Y., 1981, Immunocytochemistry of glutamate decarboxylase in the deafferented habenula, Brain Res., 208: 181–186.PubMedCrossRefGoogle Scholar
  69. Graybiel, A.M. and Ragsdale Jr., C.W., 1983, Biochemical Anatomy of the striatum,in: “Chemical Neuroanatomy”, P.C. Emson, ed., Raven Press, New York.Google Scholar
  70. Groenewegen, H.-J. and Russchen, F.T., 1984, Organization of the efferent projections of the nucleus accumbens to pallidal, hypothalamic and mesencephalic structures. A tracing and immunohistochemical study in the cat, J. Comp. Neurol., 223: 347–367.PubMedCrossRefGoogle Scholar
  71. Grofova, I., 1975, Identification of striatal and pallidal neurons projecting to substantia nigra. An experimental study by means retrograde axonal transport of horseradish peroxidase, Brain Res., 91: 286–291.PubMedCrossRefGoogle Scholar
  72. Gulley, R.L. and Wood, R.L., 1971, The fine structure of the neurons in the rat substantia nigra, Tissue and Cell, 3: 675–690.PubMedCrossRefGoogle Scholar
  73. Haber, S. and Elde, R., 1981, Correlation between met-enkephalin and substance P immunoreactivity in the primate globus pallidus, Neuroscience, 6: 1291–1297.PubMedCrossRefGoogle Scholar
  74. Haber, S. and Elde, R., 1982, The distribution of enkephalin immunoreactive fibers and terminals in the monkey central nervous system: An immunohistochemical study, Neuroscience, 7: 1049– 1095.PubMedCrossRefGoogle Scholar
  75. Haber, S.N. and Nauta, W.J.H., 1983, Ramifications of the globus pallidus in the rat as indicated by patterns of immunohistochemistry, Neuroscience, 9: 245–260.PubMedCrossRefGoogle Scholar
  76. Haber, S.N. and Watson, S.J., 1985, The comparative distribution of enkephalin, dynorphin and substance P in the human globus pallidus and basal forebrain, Neuroscience, 14: 1011–1024.PubMedCrossRefGoogle Scholar
  77. Hattori, T., McGeer, 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 Res., 54: 103–114.PubMedCrossRefGoogle Scholar
  78. Hedreen, J.C., Bacon, S.J., Cork, L.C., Kitt, C.A., Crawford, G.D., Salvaterra, M. and Price, D.L., 1983, Immunocytochemical identification of cholinergic neurons in the monkey central nervous system using monoclonal antibodies against choline acetyltransferase, Neurosci. Lett., 43: 173–177.PubMedCrossRefGoogle Scholar
  79. Henderson, Z., 1981, Ulstrastructure and acetylcholinesterase content of neurons forming connections between the striatum and substantia nigra of rat, J. Comp. Neurol., 197: 185–196.PubMedCrossRefGoogle Scholar
  80. Hendry, S.H.C, Jones, E.G. and Emson, P.C., 1984, Morphology, distribution, and synaptic relations of somatostatin- and neuropeptide Y-immunoreactive neurons in rat and monkey neocortex, J. Neurosci., 4: 2497–2517.PubMedGoogle Scholar
  81. Hökfelt, T., Johansson, O., Fuxe, K., Goldstein, M. and Park, D., 1976, Immunohistochemical studies on the localization and distribution of monoamine neuron systems in the rat brain. I. Tyrosine hydroxylase in the mes- and diencephalon, Med. Biol., 54: 427– 453.PubMedGoogle Scholar
  82. Hökfelt, T., Martensson, R., Björklund, A., Kleinau, S. and Goldstein, M., 1984, Distributional maps of tyrosine-hydroxylase immunoreactive neurons in the rat brain,in: “Handbook of Chemical Neuroanatomy: Classical Transmitters in the CNS”, Vol. 2, Part I, A. Björklund and T. Hökfelt, eds., Elsevier, Amsterdam.Google Scholar
  83. Holstein, G.R., Pasik, P. and Hamori, J., 1986, Synapses between GABA-immunoreactive axonal and dendritic elements in monkey substantia nigra, Neurosci. Lett., 66: 316–323.PubMedCrossRefGoogle Scholar
  84. Hong, J.-S., Yang, H.Y., Racagni, G. and Costa, E., 1977, Projections of substance P containing neurons from neostriatum to substantia nigra, Brain Res., 122: 541–544.PubMedCrossRefGoogle Scholar
  85. Houser, C.R., Crawford, G.D., Barber, R.P., Salvaterra, P.M. and Vaughn, J.E., 1983, Organization and morphological characteristics of cholinergic neurons: An immunocytochemical study with a monoclonal antibody to choline acetyltransferase, Brain Res., 266: 97–119.PubMedCrossRefGoogle Scholar
  86. Hsu, S.M., Raine, L. and Fanger, H., 1981, Use of avidin-biotinperoxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures, J. Histochem. Cytochem., 29: 577–580.PubMedCrossRefGoogle Scholar
  87. Ichikawa, T. and Hirata, Y., 1986, Organization of choline acetyltransferase-containing structures in the forebrain of the rat, J. Neurosci., 6: 281–292.PubMedGoogle Scholar
  88. Inagaki, S. and Parent, A., 1984, Distribution of substance P and enkephalin-like immunoreactivity in the substantia nigra of rat, cat and monkey, Brain Res. Bull., 13: 319–329.PubMedCrossRefGoogle Scholar
  89. Inagaki, S. and Parent, A., 1985, Distribution of enkephalin-immunoreactive neurons in the forebrain and upper brainstem of the squirrel monkey, Brain Res., 359: 267–280.PubMedCrossRefGoogle Scholar
  90. Inagaki, S., Sakanaka, M., Shiosaka, J., Senba, E., Takatsuki, K., Takagi, H., Kawai, T., Minagawa, H. and Tohyama, M., 1981, Ontogeny of substance-P-containing neuron system of the rat. Immunohistochemical analysis. I. Forebrain and upper brainstem, Neuroscience, 7: 639–645.CrossRefGoogle Scholar
  91. Jacobowitz, D.M. and MacLean, P.D., 1978, A brainstem atlas of catecholaminergic neurons and serotonergic perikarya in a pygmy primate (Cebuella pygmaea), J. Comp. Neurol., 177: 397–416.PubMedCrossRefGoogle Scholar
  92. Jayaraman, A., 1980, Anatomical evidence for cortical projections from the striatum in the cat, Brain Res., 195: 29–36.PubMedCrossRefGoogle Scholar
  93. Jessell, T.M., Emson, P.C., Paxinos, G. and Cuello, A.C., 1978, Topographic projections of substance P and GABA pathways in the striato- and pallido-nigral system: A biochemical and immunohistochemical study, Brain Res., 152: 487–498.PubMedCrossRefGoogle Scholar
  94. Juraska, J.M., Wilson, C.J. and Grover, P.M., 1977, The substantia nigra of the rat: A Golgi study, J. Comp. Neurol., 172: 585–600.PubMedCrossRefGoogle Scholar
  95. Kaiya, H., Kreutzberg, G.W. and Namba, M., 1980, Ultrastructure of acetylcholinesterase synthesizing neurons in the neostriatum, Brain Res., 187: 369–382.PubMedCrossRefGoogle Scholar
  96. Kanazawa, I., Emson, P.C. and Cuello, A.C., 1977, Evidence for the existence of substance P-containing fibers in the striato-nigral and pallido-nigral pathways in rat brain, Brain Res., 119: 447–453.PubMedCrossRefGoogle Scholar
  97. Kanazawa, I., Mogaki, S., Muramoto, O. and Kuzuhara, S., 1980, On the origin of substance P-containing fibres in the entopeduncular nucleus and the substantia nigra of the rat, Brain Res., 184: 481–485.PubMedCrossRefGoogle Scholar
  98. Karabelas, A.B. and Moschovakis, A.K., 1985, Nigral inhibitory termination on efferent neurons of the superior colliculus: An intracellular horseradish peroxidase study in the cat, J. Comp. Neurol., 239: 309–329.PubMedCrossRefGoogle Scholar
  99. Karnovsky, M.J. and Roots, L., 1964, A “direct-coloring” thiocholine method for Cholinesterase, J. Histochem. Cytochem., 12: 219–221.PubMedCrossRefGoogle Scholar
  100. Kataoka, K., Bak, 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 strio-nigral fibres of the baboon, Exp. Brain Res., 19: 217–227.PubMedCrossRefGoogle Scholar
  101. Kerkérian, L., Bosler, O., Pelletier, G. and Nieoullon, A., 1986, Striatal neuropeptide Y neurones are under the influence of the nigrostriatal dopaminergic pathway: immunohistochemical evidence, Neurosci. Lett., 66: 106–112.PubMedCrossRefGoogle Scholar
  102. Khachaturian, H., Lweis, M.E., Hollt, V. and Watson, S.J., 1983, Telencephalic enkephalinergic systems in the rat brain, J. Neurosci., 3: 844–855.PubMedGoogle Scholar
  103. Kilpatrick, I.C, Starr, M.S., Fletcher, A., James, T.A. and MacLeod, N.K., 1980, Evidence for a GABAergic nigrothalamic pathway in the rat. I. Behavioural and biochemical studies, Exp. Brain Res., 40: 45–54.PubMedCrossRefGoogle Scholar
  104. Kim, J.S., Bak, I.J., Hassler, R. and Okada, Y., 1971, 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.PubMedCrossRefGoogle Scholar
  105. Kimura, H., McGeer, P.L., Peng, J.H. and McGeer, E.G., 1981, The central cholinergic system studied by choline acetyltransferase immunohistochemistry in the cat, J. Comp. Neurol., 200: 151–201.PubMedCrossRefGoogle Scholar
  106. Kohno, J., Shiosaka, S., Shinoda, K., Inagaki, S. and Tohyama, M., 1984, Two distinct strio-nigral substance P pathways in the rat: An experimental immunohistochemical study, Brain Res., 308: 309– 317.PubMedCrossRefGoogle Scholar
  107. Levey, A.I., Wainer, B.H., Mufson, E.J. and Mesulam, M.-M., 1983, Colocalization of acetylcholinesterase and choline acetyltransferase in the rat cerebrum, Neuroscience, 9: 9–22.PubMedCrossRefGoogle Scholar
  108. Ljungdahl, A., Hökfelt, T. and Nilsson, G., 1978, Distribution of substance P-like immunoreactivity in the central nervous system of the rat. I. Cell bodies and nerve terminals, Neuroscience, 3: 861–943.PubMedCrossRefGoogle Scholar
  109. Llinas, R., Greenfield, S.A. and Jahsen, H., 1984, Electrophysiology of pars compacta cells in the in vitro substantia nigra — A possible mechanism for dentritic release, Brain Res., 294: 127–132.PubMedCrossRefGoogle Scholar
  110. Loughlin, S.E. and Fallon, J.H., 1984, Substantia nigra and ventral tegmental area projections to cortex: Topography and collateralization, Neuroscience, 11: 425–435.PubMedCrossRefGoogle Scholar
  111. MacLeod, N.K., James, T.A., Kilpatrick, I.C. and Starr, M.S., 1980, Evidence for a GABAergic nigrothalamic pathway in the rat. II. Electrophysiological studies, Exp. Brain Res., 40: 55–61.PubMedCrossRefGoogle Scholar
  112. Marshall, P.E., Landis, D.M.D. and Zalneraitis, E.L., 1983, Immunocytochemical studies of substance P and leucine-enkephalin in Huntington’s disease, Brain Res., 289: 11–26.PubMedCrossRefGoogle Scholar
  113. McLean, S., Skirboll, L.R. and Pert, C., 1985, Comparison of substance P and enkephalin distribution in rat brain: An overview using radioimmunohistochemistry, Neuroscience, 14: 837–852.PubMedCrossRefGoogle Scholar
  114. Mesulam, M.-M., 1976, A horseradish peroxidase method for the identification of the efferents of acetylcholinesterase-containing neurons, J. Histochem. Cytochem., 24: 1281–1286.PubMedCrossRefGoogle Scholar
  115. Mesulam, M.-M., Mufson, E.J., Levey, A.I. and Wainer, B.H., 1984, Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry, Neuroscience, 12: 669–686.PubMedCrossRefGoogle Scholar
  116. Mesulam, M.-M., Mufson, E.J., Wainer, B.H. and Levey, A.I., 1983, Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Chl-Ch6), Neuroscience, 10: 1185–1201.PubMedCrossRefGoogle Scholar
  117. Morelli, M., Del Fiacco, M., Wu, J.-Y. and DiChiara, G., 1983, Immunohistochemical localization of Leu-enkephalin and Glutamicacid-decarboxylase in the nucleus caudatus of the rat, in: “Neuromodulation and Brain Function”, G. Biggio, P.F. Spano, G. Toffano and G.L. Gessa, eds., Pergamon Press, New York.Google Scholar
  118. Mugnaini, E. and Oertel, W.H., 1985, An atlas of the distribution of GABAergic neurons and terminals in the rat CNS as revealed by GAD immnunohistochemistry,in: “Handbook of Chemical Neuroanatomy: GABA and Neuropeptides in the CNS”, Vol. 4, Part I, A. Björklund and T. Hökfelt, eds., Elsevier, Amsterdam.Google Scholar
  119. Nagai, T., McGeer, P.L. and McGeer, E.G., 1983, Distribution of GABA-T-intensive neurons in the rat forebrain and midbrain, J. Comp. Neurol., 218: 220–238.PubMedCrossRefGoogle Scholar
  120. Nagy, J.I., Carter, D.A. and Fibiger, H.C., 1978a, Anterior striatal projections to the globus pallidus, entopeduncular nucleus and substantia nigra in the rat: the GABA connection, Brain Res., 158: 15–29.PubMedCrossRefGoogle Scholar
  121. Nagy, J.I., Carter, D.A., Lehman, J. and Fibiger, H.C., 1978b, Evidence for a GABA-containing projection from the entopeduncular nucleus to the lateral habenula in the rat, Brain Res., 145: 360–364.PubMedCrossRefGoogle Scholar
  122. Nagy, J.I. and Fibiger, H.C., 1980, A striatal source of glutamic acid decarboxylase activity in the substantia nigra, Brain Res., 187: 237–242.PubMedCrossRefGoogle Scholar
  123. Nakagawa, Y., Shiosaka, S., Emson, P.C. and Tohyama, M., 1985, Distribution of neuropeptide Y in the forebrain and diencephalon: an immunohistochemical analysis, Brain Res., 361: 52–60.PubMedCrossRefGoogle Scholar
  124. Nobin, A. and Björklund, A., 1973, Topography of monoamine neurons systems in the human brain as revealed in fetuses, Acta Physiol. Scand., 388: 1–40.Google Scholar
  125. Oertel, W.H. and Mugnaini, E., 1984, Immunocytochemical studies of gabaergic neurons in rat basal ganglia and their relations to other neuronal systems, Neurosci. Lett., 47: 233–238.PubMedCrossRefGoogle Scholar
  126. Oertel, W.H., Nitsch, C. and Mugnaini, E., 1984, Immuunocytochemical demonstration of the GABA-ergic neurons in rat globus pallidus and nucleus entopeduncularis and their GABA-ergic innervation, in: “Advances in Neurology”, R.G. Hassler and J.F. Christ, eds., Raven Press, New York, 40: 91–98.Google Scholar
  127. Oertel, W.H., Tappaz, M.L., Berod, A. and Mugnaini, E., 1982, Two-color immunohistochemistry for dopamine and GABA neurons in rat substantia nigra and zona incerta, Brain Res. Bull., 9: 463–474.PubMedCrossRefGoogle Scholar
  128. Olson, L., Boreus, L.O. and Seiger, A., 1973, Histochemical demonstration and mapping of 5-hydroxytryptamine and catecholaminecontaining neuron systems in the human fetal brain, Zeit. für Anat. und Entwickl., 139: 259–282.CrossRefGoogle Scholar
  129. Ottersen, O.P. and Storm-Mathisen, J., 1984, Neurons containing or accumulating transmitter amino acid,in: “Handbook of Chemical Neuroanatomy: Classical Transmitters and Transmitter receptors in CNS”, Vol. 3, Part II, A. Björklund, T. Hökfelt and M.J. Kuhar, eds., Elsevier, Amsterdam.Google Scholar
  130. Panula, P., Wu, J.-Y. and Emson, P., 1981, Ultrastructure of GABA-neurons in cultures of rat neostriatum, Brain Res., 219: 202– 207.PubMedCrossRefGoogle Scholar
  131. Parent, A., 1986, “Comparative Neurobiology of the Basal Ganglia”, John Wiley & Sons, New York, pp. 335.Google Scholar
  132. Parent, A., Boucher, R. and O’Reilly-Fromentin, J., 1981, Acetylcholinesterase-containing neurons in cat pallidal complex: morphological characteristics and projection towards the neocortex, Brain Res., 230: 356–361.PubMedCrossRefGoogle Scholar
  133. Parent, A. and De Bellefeuille, L., 1983, The pallidointralaminar and pallidonigral projections in primate as studied by retrograde double-labeling method, Brain Res., 278: 11–27.PubMedCrossRefGoogle Scholar
  134. Parent, A., Gravel, S. and Olivier, A., 1979, The extrapyramidal and limbic systems relationship at the globus pallidus level: A comparative histochemical study in the rat, cat and monkey, in: “Advances in Neurology”, L.J. Poirier, T.L. Sourkes and P.J. Bédard, eds., Raven Press, New York, 24: 1–11.Google Scholar
  135. Parent, A., Mackey, A., Smith, Y. and Boucher, R., 1983, The output organization of the substantia nigra in primate as revealed by retrograde double labeling method, Brain Res. Bull., 10: 529–537.PubMedCrossRefGoogle Scholar
  136. Parent, A., O’Reilley-Fromentin, J. and Boucher, R., 1980, Acetylcholinesterase-containing neurons in cat neostriatum: a morphological and quantitative analysis, Neurosci. Lett., 20: 271–276.PubMedCrossRefGoogle Scholar
  137. Parent, A., Smith, Y. and De Bellefeuille, L., 1984, The output organization of the pallidum and substantia nigra in primate as revealed by a retrograde double-labeling method,in: “The Basal Ganglia”, J.S. McKenzie, R.E. Kemm and L.N. Wilcock, eds., Plenum Press, New York.Google Scholar
  138. Pasik, P., Pasik, T., Hamori, J. and Holstein, G.R., 1986, Light and electron microscopic visualization of GABAergic elements in the monkey brain by means of a direct GABA antibody,in: “GABA and endocrine function”, G. Racagni and A.O. Donoso, eds., Raven Press, New York.Google Scholar
  139. Pearson, J., Goldstein, M., Markey, K. and Brandeis, L., 1983, Human brainstem catecholamine neuronal anatomy as revealed by immunocytochemistry with antibodies to tyrosine hydroxylase, Neuroscience, 8: 3–32.PubMedCrossRefGoogle Scholar
  140. Pelletier, G., Désy, L., Kerkérian, L. and Côté, J., 1984, Immunocytochemical localization of Neuropeptide Y (NPY) in the human hypothalamus, Cell tissue Res., 238: 203–205.PubMedCrossRefGoogle Scholar
  141. Penney, J.B. and Young, A.B., 1981, GABA as the pallidothalamic neurotransmitter: implications for basal ganglia function, Brain Res., 207: 195–199.PubMedCrossRefGoogle Scholar
  142. Penny, G.R., Afsharpour, S. and Kitai, S.T., 1986, The glutamate decarboxylase-, leucine enkephalin-, methionine enkephalin- and substance P-immunoreactive neurons in the neostriatum of the rat and cat: evidence for partial population overlap, Neuroscience, 17: 1011–1045.PubMedCrossRefGoogle Scholar
  143. Pérez de 1a Mora, M., Possani, L.D., Tapia, R., Teran, L., Palacios, R., Fuxe, K., Hökfelt, T. and Ljungdahl, A., 1981, Demonstration of central γ-aminobutyrate-containing nerve terminals by means of antibodies against glutamate decarboxylase, Neuroscience, 6: 875–895.PubMedCrossRefGoogle Scholar
  144. Petrusz, P., Merchenthaler, I. and Maderdrut, J.L., 1985, Distribution of enkephalin-containing neurons in the central nervous system, in: “Handbook of Chemical Neuroanatomy: GABA and Neuropeptides in the CNS”, Vol., 4, Part I, A. Björklund and T. Hökfelt, eds., Elsevier, Amsterdam.Google Scholar
  145. Phelps, P.E., Houser, C.R. and Vaughn, J.E., 1985, Immunocytochemical localization of choline acetyltransferase within the rat neostriatum: A correlated light and electron microscopic study of cholinergic neurons and synapses, J. Comp. Neurol., 238: 286–307.PubMedCrossRefGoogle Scholar
  146. Pickel, V.M., Khushdev, K.S., Beckley, S.C., Miller, R.J. and Reis, D.J., 1980a, Immunocytochemical localization of enkephalin in the neostriatum of rat brain: A light and electron microscopic study, J. Comp. Neurol., 189: 721–740.PubMedCrossRefGoogle Scholar
  147. Pickel, V.M., Specht, L.A., Sumai, K.K., Joh, T.H., Reis, D.J. and Hervonen, A., 1980b, Immunocytochemical localization of tyrosine-hydroxylase in the human fetal neuron systems, J. Comp. Neurol., 194: 465–474.PubMedCrossRefGoogle Scholar
  148. Pioro, E.P.J., Hugues, J.T. and Cuello, A.C., 1984, Loss of substance P and enkephalin immunoreactivity in the human substantia nigra after striato-pallidal infarction, Brain Res., 292: 339–347.PubMedCrossRefGoogle Scholar
  149. Poirier, L.J., Giguère, M. and Marchand, R., 1983, Comparative morphology of the substantia nigra and ventral tegmental area on the monkey, cat, and rat, Brain Res. Bull., 11: 371–397.PubMedCrossRefGoogle Scholar
  150. Poirier, L.J., Parent, A., Marchand, R. and Butcher, L.L., 1977, Morphological characteristics of the acetylcholinesterase-containing neurons in the CNS of DFP-treated monkeys. Part I. Extrapyramidal and related structures, J. Neurol. Sci., 31: 181–198.PubMedCrossRefGoogle Scholar
  151. Poitras, D. and Parent, A., 1978, Atlas of the distribution of monoamine-containing nerve cell bodies in the brain stem of the cat, J. Comp. Neurol., 179: 699–718.PubMedCrossRefGoogle Scholar
  152. Reinoso-Suarez, F., Llamas, A. and Avendano, C., 1982, Pallido-cortical projections in the cat studied by means of horseradish peroxidase retrograde transport technique, Neurosci. Lett., 29: 255–259.CrossRefGoogle Scholar
  153. Ribak, C.E. and Kramer, W.G. III, 1982, Cholinergic neurons in the basal forebrain of the cat have direct projections to the sensorimotor cortex, Exp. Neurol., 75: 453–465.PubMedCrossRefGoogle Scholar
  154. Ribak, C.E., Vaughn, J.E. and Roberts, E., 1979, The GABA neurons and their axon terminals in the rat corpus striatum as demonstrated by GAD immunocytochemistry, J. Comp. Neurol., 187: 261–284.PubMedCrossRefGoogle Scholar
  155. Ribak, C.E., Vaughn, J.E. and Roberts, E. 1980, Gabaergic nerve terminals decrease in the substantia nigra following hemitransections of the striatonigral and pallidonigral pathways, Brain Res., 192: 413–420.PubMedCrossRefGoogle Scholar
  156. Ribak, C.E., Vaughn, J.E., Saito, K., Barber, R. and Roberts, E., 1976, Immunocytochemical localization of glutamate decarboxylase in rat substantia nigra, Brain Res., 116: 287–298.PubMedCrossRefGoogle Scholar
  157. Rouzaire-Dubois, B., Hammond, C., Hamon, B. and Féger, J., 1980, Pharmacological blockade of the globus pallidus-induced inhibitory response of subthalamic cells in the rat, Brain Res., 200: 321–329.PubMedCrossRefGoogle Scholar
  158. Royce, G.J. and Laine, E., 1984, Efferent connections of the caudate nucleus, including cortical projections of the striatum and other basal ganglia: An autoradiographic and horseradish peroxidase investigation in the cat, J. Comp. Neurol., 226: 28–49.PubMedCrossRefGoogle Scholar
  159. Sandell, J.H., Graybiel, A.M. and Chesselet, M.-F., 1986, A new marker for striatal compartmentalization: NADPH diaphorase activity in the caudate nucleus and putamen of the cat, J. Comp. Neurol., 243: 326–334.PubMedCrossRefGoogle Scholar
  160. Sar, M., Stumpf, W.E., Miller, R.S., Chang, K.-J. and Cuatrecasas, P., 1978, Immunohistochemical localization of enkephalin in rat brain and spinal cord, J. Comp. Neurol., 182: 17–38.PubMedCrossRefGoogle Scholar
  161. Satoh, K., Armstrong, D.M. and Fibiger, E.G., 1983a, A comparison of the distribution of central cholinergic neurons as demonstrated by acetylcholinesterase pharmacohistochemistry and choline acetyltransferase immunohistochemistry, Brain Res. Bull., 11: 693–720.PubMedCrossRefGoogle Scholar
  162. Satoh, K. and Fibiger, H.C., 1985a, Distribution of central cholinergic neurons in the baboon (Papio papio) I. General morphology, J. Comp. Neurol., 236: 197–214.PubMedCrossRefGoogle Scholar
  163. Satoh, K. and Fibiger, H.C., 1985b, Distribution of central cholinergic neurons in the baboon (Papio papio) II. A topographic atlas correlated with catecholamine neurons, J. Comp. Neurol., 236: 215–233.PubMedCrossRefGoogle Scholar
  164. Satoh, K., Staines, W.A., Atmadja, S. and Fibiger, H.C., 1983b, Ultrastructural observations of the cholinergic neurons in the rat striatum as identified by acetylcholinesterase pharmacohistochemistry, Neuroscience, 10: 1121–1136.PubMedCrossRefGoogle Scholar
  165. Schofield, S.P.M. and Everitt, B.J., 1981, The organization of catecholamine-containing neurons in the brain of the rhesus monkey (Macaca mulatta), J. Anat., 132: 391–418.PubMedGoogle Scholar
  166. Schwyn, R.C. and Fox, C.A., 1974, The primate substantia nigra: A Golgi and electron microscopic study, J. Hirnforsch., 15: 95–126.PubMedGoogle Scholar
  167. Séguéla, P., Geffard, M., Buijs, R.M. and LeMoal, M., 1984, Antibodies against γ-aminobutyric acid: Specificity studies and immunocytochemical results, Proc. Natl Acad. Sci. (USA), 81: 3888–3892.CrossRefGoogle Scholar
  168. Smith, Y. and Parent, A., 1986, Neuropeptide Y-imraunoreactive neurons in striatum of cat and monkey: morphological characteristics, intrinsic organization and co-localization with somatostatin, Brain Res., 372: 241–253.PubMedCrossRefGoogle Scholar
  169. Smith, Y. and Parent, A., 1984, Distribution of acetylcholinesterase-containing neurons in the basal forebrain and upper brainstem of the squirrel monkey (Saimiri sciureus), Brain Res. Bull., 12: 95–104.PubMedCrossRefGoogle Scholar
  170. Smith, Y., Parent, A., Kerkérian, L. and Pelletier, G., 1985, Distribution of neuropeptide Y-immunoreactivity in the basal forebrain and upper brainstem of the squirrel monkey (Saimiri sciureus), J. Comp. Neurol., 236: 71–89.PubMedCrossRefGoogle Scholar
  171. Somogyi, P., Bolam, J.P. and Smith, A.D., 1981, Monosynaptic cortical input and local axon collaterals of identified striatonigral neurons. A light and electron microscopic study using the Golgi-peroxidase transport-degeneration procedure, J. Comp. Neurol., 195: 567–584.PubMedCrossRefGoogle Scholar
  172. Somogyi, P. and Smith, A.D., 1979, Projection of neostriatal spiny neurons to the substantia nigra. Application of a combined Golgi-staining and horseradish peroxidase transport procedure at both light and electron microscopic levels, Brain Res., 178: 3–15.PubMedCrossRefGoogle Scholar
  173. Staines, W.A., Nagy, J.I., Vincent, S.R. and Fibiger, H.C., 1980, Neurotransmitters contained in the efferents of the striatum, Brain Res., 194: 391–402.PubMedCrossRefGoogle Scholar
  174. Sternberger, L.A., 1974, “Immunocytochemistry”, John Wiley & Sons, New York.Google Scholar
  175. Streit, P., 1980, Selective retrograde labeling indicating the transmitter of neuronal pathways, J. Comp. Neurol., 191: 429–463.PubMedCrossRefGoogle Scholar
  176. Swanson, L.W., 1982, The projections of the ventral tegmental area and adjacent regions: A combined fluorescent retrograde tracer and immunofluorescence study in the rat, Brain Res. Bull., 9: 321–353.PubMedCrossRefGoogle Scholar
  177. Tanaka, C., Ishikawa, M. and Shimada, S., 1982, Histochemical mapping of catecholaminergic neurons and their ascending fiber pathways in the rhesus monkey brain, Brain Res. Bull., 9: 255–270.PubMedCrossRefGoogle Scholar
  178. Tramu, G., Pillez, A. and Leonardell, J., 1978, An effective method of antibody elution for the successive or simultaneous localization of two antigens by immunocytochemistry, J. Histochem. Cytochem., 26: 322–324.PubMedCrossRefGoogle Scholar
  179. Tsubokawa, T. and Sutin, J., 1972, Pallidal and tegmental inhibition of oscillatory slow waves and unit activity in the subthalamic nucleus, Brain Res., 41: 101–118.PubMedCrossRefGoogle Scholar
  180. Ueki, A., 1983, The mode of nigro-thalamic transmission investigated with intracellular recording in the cat, Exp. Brain Res., 49: 116–124.PubMedCrossRefGoogle Scholar
  181. Uno, M., Ozawa, N. and Yoshida, M., 1978, The mode of pallido-thalamic transmission investigated with intracellular recording from the cat thalamus, Exp. Brain Res., 33: 493–507.PubMedCrossRefGoogle Scholar
  182. Van del Pol, A.N., Smith, A.D. and Powell, J.F., 1985, GABA axons in synaptic contact with dopamine neurons in the substantia nigra: double immunocytochemistry with biotin-peroxidase and protein A-colloidal gold, Brain Res., 348: 146–154.PubMedCrossRefGoogle Scholar
  183. Vincent, S.R., Hattori, T. and McGeer, E.G., 1978, The nigrotectal projection: a biochemical and ultrastructural characterization, Brain Res., 151: 159–164.PubMedCrossRefGoogle Scholar
  184. Vincent, S.R. and Johansson, O., 1983, Striatal neurons containing both somatostatin- and avian pancreatic polypeptide (APP)-like immunoreactivities and NADPH-Diaphorase activity: A light and electron microscopic study, J. Comp. Neurol., 217: 264–270.PubMedCrossRefGoogle Scholar
  185. Vincent, S.R., Kimura, H. and McGeer, E.G., 1981, The histochemical localization of GABA-transaminase in the efferents of the striatum, Brain Res., 222: 198–203.PubMedCrossRefGoogle Scholar
  186. Vincent, S.R., Kimura, H. and McGeer, E.G., 1982, A histochemical study of GABA-transaminase in the efferents of the pallidum, Brain Res., 241: 162–165.PubMedCrossRefGoogle Scholar
  187. Wainer, B.H., Levey, A.I., Mufson, E.J. and Mesulam, M.-M., 1984, Cholinergic systems in mammalian brain identified with antibodies against choline acetyltransferase, Neurochem. Int., 6: 163–182.PubMedCrossRefGoogle Scholar
  188. Wainer, B.H. and Rye, D.B., 1984, Retrograde horseradish peroxidase tracing combined with localization of choline acetyltransferase immunoreactivity, J. Histochem. Cytochem., 32: 439–443.PubMedCrossRefGoogle Scholar
  189. Wamsley, J.K., Young, W.S. III and Kuhar, M.J., 1980, Immunohistochemical localization of enkephalin in rat forebrain, Brain Res., 190: 153–174.PubMedCrossRefGoogle Scholar
  190. Wiklund, L., Léger, L. and Persson, M., 1981, Monoamine cell distribution in the rat brain stem. A fluorescence histochemical study with quantification of indolaminergic and locus coeruleus cell groups, J. Comp. Neurol., 203: 613–647.PubMedCrossRefGoogle Scholar
  191. Williams, R.G. and Dockray, G.J., 1983, Distribution of enkephalinrelated peptides in rat brain: Immunohistochemical studies using antisera to met-enkephalin and met-enkephalin-Arg 6Phe 7, Neuroscience, 9: 563–586.PubMedCrossRefGoogle Scholar
  192. Woodhams, P.L., Allen, Y.S., McGovern, J., Allen, J.M., Bloom, S.R., Balazs, R. and Polak, J.M., 1985, Immunohistochemical analysis of the early ontogeny of the neuropeptide Y system in rat brain, Neuroscience, 15: 173–202.PubMedCrossRefGoogle Scholar
  193. Woolf, N. and Butcher, L.L., 1981, Cholinergic neurons in the caudateputamen complex proper are intrinsically organized: A combined Evans blue and acetylcholinesterase analysis, Brain Res. Bull., 7: 487–507.PubMedCrossRefGoogle Scholar
  194. Yoshida, M. and Omata, S., 1979, Blocking by picrotoxin of nigra-evoked inhibition of neurons of ventromedial nucleus of the thalamus, Experientia, 35: 794.PubMedCrossRefGoogle Scholar
  195. Yoshida, M. and Precht, W., 1971, Monosynaptic inhibition of neurons of the substantia nigra by caudato-nigral fibers, Brain Res., 32: 225–228.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1987

Authors and Affiliations

  • A. Parent
    • 1
  • Y. Smith
    • 1
  • M.-Y. Arsenault
    • 1
  1. 1.Laboratoire de Neurobiologie Faculté de MédecineUniversité LavalQuébecCanada

Personalised recommendations