Electrophysiological and immunocytochemical characterization of GABA and dopamine neurons in the substantia nigra of the rat

Neuroscience

Volumn 80, Issue 2, 1997, Pages 545-557

  Richards, C D ^a   Shiroyama, T ^a,b   Kitai, S T ^a  

^a UNIVERSITY OF TENNESSEE COLLEGE OF MEDICINE   (United States)

^b MIE UNIVERSITY   (Japan)

Author keywords

Glutamate decarboxylase; Neurobiotin; Tyrosine hydroxylase

Indexed keywords

4 AMINOBUTYRIC ACID; BIOTIN DERIVATIVE; CALCIUM; DOPAMINE; GLUTAMATE DECARBOXYLASE; TYROSINE 3 MONOOXYGENASE;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ELECTROPHYSIOLOGY; GABAERGIC SYSTEM; IMMUNOCYTOCHEMISTRY; MALE; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SUBSTANTIA NIGRA;

ANIMALS; BIOTIN; COLORING AGENTS; DOPAMINE; ELECTROPHYSIOLOGY; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE POTENTIALS; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SUBSTANTIA NIGRA; TYROSINE 3-MONOOXYGENASE;

EID: 0030879450     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00093-6     Document Type: Article

References (94)

1. Agid Y. (1991) Parkinson's disease: pathophysiology. Lancet 337, 1321-1324.
2. Andén N.-E., Dahlström A., Fuxe K., Larsson K., Olson L. and Ungerstedt U. (1966) Ascending monoamine neurons to the telencephalon and diencephalon. Acta physiol. scand. 67, 313-326.
3. Beckstead R. M., Domesick V. B. and Nauta W. J. H. (1979) Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res. 175, 191-217.
4. Bentivoglio M., Van der Kooy D. and Kuypers H. G. J. M. (1979) The organization of the efferent projections of the substantia nigra in the rat. A retrograde fluorescent double labeling study. Brain Res. 174, 1-17.
5. Björklund A. and Lindvall O. (1975) Dopamine in dendrites of substantia nigra neurons: suggestions for a role in dendritic terminals. Brain Res. 83, 531-537.
6. Bunney B. S., Walters J. R., Roth R. H. and Aghajanian G. K. (1973) Dopaminergic neurons: effect of antipsychotic drugs and amphetamine on single cell activity. J. Pharmac. exp. Ther. 185, 560-571.
7. Chang H. T., Kita H. and Kitai S. T. (1984) The ultrastructural morphology of the subthalamic-nigral axon terminals intracellularly labeled with horseradish peroxidase. Brain Res. 299, 182-185.
8. Charara A., Smith Y. and Parent A. (1996) Glutamatergic inputs from the pedunculopontine nucleus to midbrain dopaminergic neurons in primates: Phaseolus vulgaris-leucoagglutinin anterograde labeling combined with postembedding glutamate and GABA immunohistochemistry. J. comp. Neurol. 364, 254-266.
9. Chèramy A., Leviel V. and Glowinski J. (1981) Dendritic release of dopamine in the substantia nigra. Nature 289, 537-542.
10. Chergui K., Akaoka H., Charlety P. J., Saunier C. F., Buda M. and Chouvet G. (1994) Subthalamic nucleus modulates burst firing of nigral dopamine neurones via NMDA receptors. NeuroReport 5, 1185-1188.
11. Deniau J. M., Hammond C., Chevalier G. and Féger J. (1978) Evidence for branched subthalamic nucleus projections to substantia nigra, entopeduncular nucleus and globus pallidus. Neurosci. Lett. 9, 117-121.
12. Deniau J. M., Kitai S. T., Donoghue J. P. and Grofová I. (1982) Neuronal interactions in the substantia nigra pars reticulata through axon collaterals of the projection neurons. An electrophysiological and morphological study. Expl Brain Res. 47, 105-113.
13. Domesick V. B., Stinus L. and Paskevich 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 microscopic study. Neuroscience 8, 743-765.
14. Fallon J. H. (1988) Topographic organization of ascending dopaminergic projections. Ann. N.Y. Acad. Sci. 537, 1-9.
15. Faull R. L. M. and Mehler W. R. (1978) The cells of origin of nigrotectal, nigrothalamic and nigrostriatal projections in the rat. Neuroscience 3, 989-1002.
16. Freeman A. S., Meltzer L. T. and Bunney B. S. (1985) Firing properties of substantia nigra dopaminergic neurons in freely moving rats. Life Sci. 36, 1983-1994.
17. Freund T. F., Powell J. F. and Smith A. D. (1984) Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neruons, with particular reference to dendritic spines. Neuroscience 13, 1189-1215.
18. Fujimoto K. and Kita H. (1993) Response characteristics of subthalamic neurons to the stimulation of the sensorimotor cortex in the rat. Brain Res. 609, 185-192.
19. Futami T., Takakusaki K. and Kitai S. T. (1995) Glutamatergic and cholinergic inputs from the pedunculopontine tegmental nucleus to dopamine neurons in the substantia nigra pars compacta. Neurosci. Res. 21, 331-342.
20. Galarraga E. and Bargas J. (1995) Firing patterns in substantia nigra compacta identified neurons in vitro. Archs Med. Res. 26, 191-199.
21. Gariano R. F. and Groves P. M. (1988) Burst firing induced in midbrain dopamine neurons by stimulation of the medial prefrontal and anterior cingulate cortices. Brain Res. 462, 194-198.
22. Gerfen C. R., Herkenham M. and Thibault J. (1987) The neostriatal mosaic: II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems. J. Neurosci. 7, 3915-3934.
23. Gerfen C. R., Staines W. A., Arbuthnott G. W. and Fibiger H. C. (1982) Crossed connections of the substantia nigra in the rat. J. comp. Neurol. 207, 283-303.
24. Gibb W. R. and Lees A. J. (1991) Anatomy, pigmentation, ventral and dorsal subpopulations of the substantia nigra, and differential cell death in Parkinson's disease. J. Neurol. Neurosurg. Psychiat. 54, 388-396.
25. Grace A. A. and Bunney B. S. (1983) Intracellular and extracellular electrophysiology of nigral dopaminergic neurons - 1. Identification and characterization. Neuroscience 10, 301-315.
26. Grace A. A. and Bunney B. S. (1984) The control of firing pattern in nigral dopamine neurons: burst firing. J. Neurosci. 4, 2877-2890.
27. Grace A. A. and Onn S.-P. (1989) Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J. Neurosci. 9, 3463-3481.
28. Granata A. R. and Kitai S. T. (1991) Inhibitory substantia nigra inputs to the pedunculopontine neurons. Expl Brain Res. 86, 459-466.
29. Graybiel A. M. (1978) Organization of the nigrotectal connection: an experimental tracer study in the cat. Brain Res. 143, 339-348.
30. Graybiel A. M., Hirsch E. C. and Agid Y. A. (1987) Differences in tyrosine hydroxylase-like immunoreactivity characterize the mesostriatal innervation of striosomes and extrastriosomal matrix at maturity. Proc. natn. Acad. Sci. U.S.A. 84, 303-307.
31. Grofová I., Deniau J. M. and Kitai S. T. (1982) Morphology of the substantia nigra pars reticulata projection neurons intracellularly labeled with HRP. J. comp. Neurol. 208, 352-368.
32. Grofová I., Ottersen O. P. and Rinvik E. (1978) Mesencephalic and diencephalic afferents to the superior colliculus and periaqueductal gray substance demonstrated by retrograde axonal transport of horseradish peroxidase in the cat. Brain Res. 146, 205-220.
33. Groves P. M., Wilson C. J., Young S. J. and Rebec G. V. (1975) Self-inhibition by dopaminergic neurons. Science 190, 522-529.
34. Gulley R. L. and Wood R. L. (1971) The fine structure of the neurons in the rat substantia nigra. Tiss. Cell 3, 675-690.
35. Hajdu F., Hassler R. and Bak I. J. (1973) Electron microscopic study of the substantia nigra and the strio-nigral projection in the rat. Z. Zellforsch 146, 207-221.
36. Hajós M. and Greenfield S. A. (1993) Topographic heterogeneity of substantia nigra neurons: diversity in intrinsic membrane properties and synaptic inputs. Neuroscience 55, 919-934.
37. Hajós M. and Greenfield S. A. (1994) Synaptic connections between pars compacta and pars reticulata neurones: electrophysiological evidence for functional modules within the substantia nigra. Brain Res. 660, 216-224.
38. Hammond C., Deniau J. M., Rizk A. and Fegér J. (1978) Electrophysiological demonstration of an excitatory subthalamonigral pathway in the rat. Brain Res. 151, 235-244.
39. Hammond C., Shibazaki T. and 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.
40. Häusser M., Stuart G., Racca C. and Sakmann B. (1995) Axonal initiation and active dendritic propagation of action potentials in substantia nigra neurons. Neuron 15, 637-647.
41. Herkenham M. (1979) The afferent and efferent connections of the ventromedial thalamic nucleus in the rat. J. comp. Neurol. 183, 487-517.
42. Horikawa K. and Armstrong W. E. (1988) A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates. J. Neurosci. Meth. 25, 1-11.
43. Jayaraman A., Batton R. R. III and Carpenter M. B. (1977) Nigrotectal projections in the monkey: an autoradiographic study. Brain Res. 135, 147-152.
44. Juraska J. M., Wilson C. J. and Groves P. M. (1977) The substantia nigra of the rat: a Golgi study. J. comp. Neurol. 172, 585-600.
45. Kang Y. and Kitai S. T. (1993) Calcium spike underlying rhythmic firing in dopaminergic neurons of the rat substantia nigra. Neurosci. Res. 18, 195-207.
46. Kang Y. and Kitai S. T. (1993) A whole-cell patch-clamp study on the pacemaker potential in dopaminergic neurons of rat substantia nigra compacta. Neurosci. Res. 18, 209-221.
47. Kita H. and Armstrong W. (1991) A biotin-containing compound N-(2-aminoethyl)biotinamide for intracellular labeling and neuronal tracing studies: comparison with biocytin. J. Neurosci. Meth. 37, 141-150.
48. Kita H., Chang H. T. and Kitai S. T. (1983) The morphology of intracellularly labeled rat subthalamic neurons: a light microscopic analysis. J. comp. Neurol. 215, 245-257.
49. Kita H. and Kitai S. T. (1987) Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. J. comp. Neurol. 260, 435-452.
50. Kita T., Kita H. and Kitai S. T. (1986) Electrical membrane properties of rat substantia nigra compacta neurons in an in vitro slice preparation. Brain Res. 372, 21-30.
51. Kitai S. T. and Deniau J. M. (1981) Cortical inputs to the subthalamus: intracellular analysis. Brain Res. 214, 411-415.
52. Kultas-Ilinsky K., Ilinsky I. A., Massopust L. C., Young P. A. and Smith K. R. (1978) Nigrothalamic pathway in the cat demonstrated by autoradiography and electron microscopy. Expl Brain Res. 33, 481-492.
53. Lacey M. G., Calabresi P. and North R. A. (1990) Muscarine depolarizes rat substantia nigra zona compacta and ventral tegmental neurons in vitro through M1-like receptors. J. Pharmac. exp. Ther. 253, 395-400.
54. Lavoie B. and Parent A. (1994) Pedunculopontine nucleus in the squirrel monkey: cholinergic and glutamatergic projections to the substantia nigra. J. comp. Neurol. 344, 232-241.
55. Marsden C. D. (1990) Parkinson's disease. Lancet 335, 948-952.
56. 1 receptors on striatonigral terminals via a pertussis toxin-sensitive coupling pathway. J. Neurosci. 14, 4494-4506.
57. Matsuda Y., Fujimura K. and Yoshida S. (1987) Two types of neurons in the substantia nigra pars compacta studied in a slice preparation. Neurosci. Res. 5, 172-179.
58. Naito A. and Kita H. (1994) The cortico-nigral projection in the rat: an anterograde tracing study with biotinylated dextran amine. Brain Res. 637, 317-322.
59. Nakanishi H., Kita H. and Kitai S. T. (1987) Electrical membrane properties of rat subthalamic neurons in an in vitro slice preparation. Brain Res. 437, 35-44.
60. Nakanishi H., Kita H. and Kitai S. T. (1987) Intracellular study of rat substantia nigra pars reticulata neurons in an in vitro slice preparation: electrical membrane properties and response characteristics to subthalamic stimulation. Brain Res. 437, 45-55.
61. Nakanishi H., Kita H. and Kitai S. T. (1988) An N-methyl-D-aspartate receptor mediated excitatory postsynaptic potential evoked in subthalamic neurons in an in vitro slice preparation of the rat. Neurosci. Lett. 95, 130-136.
62. Nedergaard S. and Greenfield S. A. (1992) Sub-populations of pars compacta neurons in the substantia nigra: the significance of qualitatively and quantitatively distinct conductances. Neuroscience 48, 423-437.
63. Nieoullon A., Chèramy A. and Glowinski J. (1977) Release of dopamine in vivo from cat substantia nigra. Nature 266, 375-377.
64. Overton P. G. and Greenfield S. A. (1995) Determinants of neuronal firing pattern in the guinea-pig subthalamic nucleus: an in vivo and in vitro comparison. J. neural Transm. 10, 41-54.
65. Overton P. G., O'Callaghan J. F. X. and Greenfield S. A. (1995) Possible intermixing of neurons from the subthalamic nucleus and substantia nigra pars compacta in the guinea-pig. Expl Brain Res. 107, 151-165.
66. Paden C., Wilson C. J. and Groves P. M. (1976) Amphetamine-induced release of dopamine from the substantia nigra in vitro. Life Sci. 19, 1499-1506.
67. Poirier L. J., Giguère M. and Marchand R. (1983) Comparative morphology of the substantia nigra and ventral tegmental area in the monkey, cat and rat. Brain Res. Bull. 11, 371-397.
68. Preston R. J., McCrea R. A., Chang H. T. and Kitai S. T. (1981) Anatomy and physiology of substantia nigra and retrorubral neurons studied by extra- and intracellular recording and by horseradish peroxidase labeling. Neuroscience 6, 331-344.
69. Ricardo J. A. (1980) Efferent connections of the subthalamic region in the rat. I. The subthalamic nucleus of Luys. Brain Res. 202, 257-271.
70. Rice M. E., Richards C. D., Nedergaard S., Hounsgaard J., Nicholson C. and Greenfield S. A. (1994) Direct monitoring of dopamine and 5-HT release in substantia nigra and ventral tegmental area in vitro. Expl Brain Res. 100, 395-406.
71. 2C receptors. Neuroscience 69, 903-913.
72. Rinvik E. (1975) Demonstration of nigrothalamic connections in the cat by retrograde axonal transport of horseradish peroxidase. Brain Res. 90, 313-318.
73. Rinvik E. and Grofová I. (1970) Observations on the fine structure of the substantia nigra in the cat. Expl Brain Res. 11, 229-248.
74. Rinvik E., Grofová I. and Ottersen O. P. (1976) Demonstration of nigrotectal and nigroreticular projections in the cat by axonal transport of proteins. Brain Res. 112, 388-394.
75. Rouzaire-Dubois B. and Scarnati E. (1987) Pharmacological study of the cortical-induced excitation of subthalamic nucleus neurons in the rat: evidence for amino acids as putative neurotransmitters. Neuroscience 21, 429-440.
76. Scarnati E., Campana E. and Pacitti C. (1984) Pedunculopontine-evoked excitation of substantia nigra neurons in the rat. Brain Res. 304, 351-361.
77. Schwyn R. C. and Fox C. A. (1974) The primate substantia nigra: A Golgi and electron microscopic study. J. Hirnforsch. 15, 95-126.
78. Shepard P. D. and Bunney B. S. (1988) Effects of apamin on the discharge properties of putative dopamine-containing neurons in vitro. Brain Res. 463, 380-384.
79. + conductance. Expl Brain Res. 86, 141-150.
80. Specht L. A., Pickel V. M., Joh T. H. and Reis D. J. (1981) Light-microscopic immunocytochemical localization of tyrosine hydroxylase in prenatal rat brain. I. Early ontogeny. J. comp. Neurol. 199, 233-253.
81. Takakusaki K., Shiroyama T., Yamamoto T. and Kitai S. T. (1996) Cholinergic and noncholinergic tegmental pedunculopontine projection neurons in rats revealed by intracellular labeling. J. comp. Neurol. 371, 345-361.
82. A receptor-mediated inhibition of rat substantia nigra dopaminergic neurons by pars reticulata projection neurons. J. Neurosci. 15, 3092-3103.
83. Tepper J. M., Sawyer S. F. and Groves P. M. (1987) Electrophysiologically identified nigral dopaminergic neurons intracellularly labeled with HRP: light-microscopic analysis. J. Neurosci. 7, 2794-2806.
84. Voorn P., Kalsbeek A., Jorritsma-Byham B. and Groenewegen H. J. (1988) The pre- and postnatal development of the dopaminergic cell groups in the ventral mesencephalon and the dopaminergic innervation of the striatum of the rat. Neuroscience 25, 857-887.
85. Walsh J. P., Cepeda C., Buchwald N. A. and Levine M. S. (1991) Neurophysiological maturation of cat substantia nigra neurons: evidence from in vitro studies. Synapse 7, 291-300.
86. 2 dopamine receptor agonists on substantia nigra pars reticulata neurons. Brain Res. 513, 125-135.
87. Waszczak B. L., Eng N. and Walters J. R. (1980) Effects of muscimol and picrotoxin on single unit activity of substantia nigra neurons. Brain Res. 188, 185-197.
88. Waszczak B. L. and Walters J. R. (1983) Dopamine modulation of the effects of g-aminobutyric acid on substantia nigra pars reticulata neurons. Science 220, 218-221.
89. Waszczak B. L. and Walters J. R. (1984) A physiological role for dopamine as modulator of GABA effects in substantia nigra: supersensitivity in 6-hydroxydopamine-lesioned rats. Eur. J. Pharmac. 105, 369-373.
90. Waszczak B. L. and Walters J. R. (1986) Endogenous dopamine can modulate inhibition of substantia nigra pars reticulata neurons elicited by GABA iontophoresis or striatal stimulation. J. Neurosci. 6, 120-126.
91. Wilson C. J., Young S. J. and Groves P. M. (1977) Statistical properties of neuronal spike trains in the substantia nigra: cell types and their interactions. Brain Res. 136, 243-260.
92. Wu J.-Y. (1982) Purification and characterization of cysteic/cysteine sulfinic acids decarboxylase and L-glutamate decarboxylase in bovine brain. Proc. natn. Acad. Sci. U.S.A. 79, 4270-4274.
93. Wu J.-Y., Lin C.-T., Brandon C., Chan T.-S., Möhler H. and Richards J. G. (1982) Regulation and immunocytochemical characterization of glutamic acid decarboxylase. In Cytochemical Methods in Neuroanatomy (eds Palay S. L. and Chan-Palay V.), pp. 279-296. Alan R. Liss, New York.
94. Yung W. H., Häusser M. A. and Jack J. J. B. (1991) Electrophysiology of dopaminergic and non-dopaminergic neurones of the guinea-pig substantia nigra pars compacta in vitro. J. Physiol., Lond. 436, 643-667.