Heterogeneity of electrically evoked dopamine release and reuptake in substantia nigra, ventral tegmental area, and striatum

Journal of Neurophysiology

Volumn 77, Issue 2, 1997, Pages 863-873

  Cragg, S J ^a   Rice, M E ^a,b   Greenfield, S A ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DESIPRAMINE; DOPAMINE; DOPAMINE BETA MONOOXYGENASE; DOPAMINE UPTAKE INHIBITOR; NORADRENALIN; NORADRENALIN UPTAKE INHIBITOR; PAROXETINE; SEROTONIN UPTAKE INHIBITOR; TYROSINE 3 MONOOXYGENASE; VANOXERINE;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE RELEASE; DOPAMINE UPTAKE; ELECTROSTIMULATION; GUINEA PIG; MESENCEPHALON; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; SUBSTANTIA NIGRA; VENTRAL TEGMENTUM;

EID: 0031019286     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1997.77.2.863     Document Type: Article

References (83)

1. ANDERSEN, P. H. The dopamine uptake inhibitor GBR 12909: selectivity and molecular mechanism of action. Eur. J. Pharmacol. 166: 493-504, 1989.
2. BJÖRKLUND, A. AND LINDVALL, O. Dopamine in dendrites of substantia nigra neurons: suggestions for a role in dendritic terminals. Brain Res. 83: 531-537, 1975.
3. BLANCHARD, V., RAISMAN-VOZARI, R., VYAS, S., MICHEL, P. P., JAVOYAGID, F., UHL, G., AND AGID, Y. Differential expression of tyrosine hydroxylase and membrane dopamine transporter genes in subpopulations of dopaminergic neurons of the rat mesencephalon. Mol Brain Res. 22: 29-40, 1994.
4. BULL, D. R., PALIJ, P., SHEEHAN, M. J., MILLAR, J., STAMFORD, J. A., KRUK, Z. L., AND HUMPHREY, P. P. A. Application of FCV to measurement of electrically evoked DA overflow from brain slices in vitro. J. Neurosci. Methods 32: 37-44, 1990.
5. 1 receptors facilitate transmitter release. Nature Lond. 366: 344-347, 1993.
6. CARBONI, E., TANDA, G. L., FRAU, R., AND DI CHIARA, G. Blockade of the noradrenaline carrier increases extracellular dopamine concentrations in the prefrontal cortex: evidence that dopamine is taken up in vivo by noradrenergic terminals. J. Neurochem. 55: 1067-1070, 1990.
7. CHIODO, L. A., BANNON, M. J., GRACE, A. A., ROTH, R. H., AND BUNNEY, B. S. Evidence for the absence of impulse-regulating somatodendritic and synthesis-modulating nerve terminal autoreceptors on subpopulations of mesocortical dopamine neurons. Neuroscience 12: 1-16, 1984.
8. CILIAX, B. J., HEILMAN, C., DEMCHYSHYN, L. L., PRISTUPA, Z. B., INCE, E., HERSCH, S., NIZMK, H. B., AND LEVEY, A. I. The dopamine transporter: immunocytochemical characterisation and localisation in brain. J. Neurosci. 15: 1714-1723, 1995.
9. CLINE, E. J., SCHEFFEL, U., BOJA, J. W., MITCHELL, W. M., CARROLL, F. I., ABRAHAM, P., LEWIN, A. H., AND KUHAR, M. J. In vivo binding of [125I]RTI-55 to dopamine transporters: pharmacology and regional distribution. Synapse 12: 37-46, 1992.
10. CRAGG, S. J., RICE, M. E., AND GREENFIELD, S. A. Voltammetric characterization of electrically-stimulated somatodendritic release in mesencephalic slices. Soc. Neurosci. Abstr. 20: 1152, 1994.
11. DAHLSTRÖM, A. AND FUXE, K. Evidence for the existence of monamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brainstem neurons. Acta Physiol. Scand. 62, Suppl. 232: 1-31, 1964.
12. DONNAN, G. A., KACZMARCZYK, S. J., PAXINOS, G., CHILCO, P. J., KALNINS, R. M., WOODHOUSE, D. G., AND MENDELSOHN, F. A. Distribution of catecholamine uptake sites in human brain as determined by quantitative [3H] mazindol autoradiography. J. Comp. Neurol. 304: 19-34, 1991.
13. ELVERFORS, A., JONASON, J., AND NISSBRANDT, H. Effects of drugs interfering with sodium and calcium channels on the release of endogenous dopamine from superfused substantia nigra slices. Soc. Neurosci. Abstr. 20: 126.14, 1994.
14. ELVERFORS, A. AND NISSBRANDT, H. Reserpine-insensitive dopamine release in the substantia nigra? Brain Res. 557: 5-12, 1991.
15. ESHLEMAN, A. J., HENNINGSEN, R. A., NEVE, K. A., AND JANOWSKY, A. Release of dopamine via the human transporter. Mol. Pharmacol. 45: 312-316, 1994.
16. FALLON, J. H. AND MOORE, R. Y. Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J. Comp. Neurol. 180: 545-580, 1978.
17. FALLON, J. H., RILEY, J. N., AND MOORE, R. Y. Substantia nigra dopamine neurons: separate populations project to neostriatum and allocortex. Neurosci. Lett. 7: 157-162, 1978.
18. FEARNLEY, J. AND LEES, A. J. Aging and Parkinson's disease: substantia nigra regional selectivity. Brain 114: 2283-2301, 1991,
19. FREED, C., REVAY, R., VAUGHAN, R. A., KRIEK, E., GRANT, S., UHL, G. R., AND KUHAR, M. J. Dopamine transporter immunoreactivity in rat brain. J. Comp. Neurol. 359: 340-349, 1995.
20. FUXE, K. AND AGNATI, L. F. (Editors). Volume Transmission in the Brain. New York: Raven, 1991.
21. GARRIS, P. A. AND WIGHTMAN, R. M. Different kinetics govern dopaminergic transmission in the amygdala, prefrontal cortex, and striatum: an in vivo Voltammetric study. J. Neurosci. 14: 442-450, 1994.
22. GEFFEN, L. B., JESSELL, T. M., CUELLO, A. C., AND IVERSEN, L. L. Release of DA from dendrites in rat substantia nigra. Nature Lond. 260: 258260, 1976.
23. 3H]tomoxetine, an enantiomerically pure ligand for NA re-uptake sites. Neurosci. Lett. 157: 203-206, 1993.
24. GERFEN, C. R., BAIMBRIDGE, K. G., AND MILLER, J. J. The neostriatal mosaic: compartmental distribution of calcium binding protein and parvalbumin in the basal ganglia of the rat and monkey. Proc. Natl. Acad. Sci. USA 82: 8780-8784, 1985.
25. GERFEN, C. R., BAIMBRIDGE, K. G., AND THIBAULT, J. The neostriatal mosaic. III. Biochemical and developmental dissociation of patch-matrix mesostriatal systems. J. Neurosci. 7: 3935-3944, 1987a.
26. GERFEN, C. R., HERKENHAM, M., AND THIBAULT, J. The neostriatal mosaic. II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems. J. Neurosci. 7: 3915-3934, 1987b.
27. GERMAN, D. C., DUBACH, M., ASKARI, S., SPECIALE, S. G., AND BOWDEN, D. M. MPTP-induced Parkinsonian syndrome in Macaca fascularis : which midbrain dopaminergic neurons are lost? Neuroscience 24: 161- 174, 1988.
28. GERMAN, D. C. AND MANAYE, K. F. Midbrain DA neurons (A8, 9, 10): 3D reconstruction in the rat. J. Comp. Neurol. 331: 297-309, 1993.
29. GIBB, W. R. G. AND LEES, A. J. Anatomy, pigmentation, ventral and dorsal subpopulations of the substantia nigra, and differential cell death in Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 54: 388-396, 1991.
30. GIROS, B., JABER, M., JONES, S. R., WIGHTMAN, R. M., AND CARON, M. G. Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature Lond. 379: 606-612, 1996.
31. GREENFIELD, S. A. The significance of dendritic release of transmitter and protein in the substantia nigra. Neurochem. Int. 7: 887-901, 1985.
32. GROVES, P. M. AND LINDER, J. C. Dendro-dendritic synapses in substantia nigra: descriptions based on analysis of serial sections. Exp. Brain Res. 49: 209-217, 1983.
33. GROVES, P. M., WILSON, C. J., YOUNG, S. J., AND REBEC, G. V. Self-inhibition by dopaminergic neurons. Science Wash. DC 190: 522-529, 1975.
34. HAJÓS, M. AND GREENFIELD, S. A. Topographic heterogeneity of substantia nigra neurons: diversity in intrinsic membrane properties and synaptic inputs. Neuroscience 55: 919-934, 1993.
35. HEERINGA, M. J. AND ABERCROMBIE, E. D. Biochemistry of somatodendritic DA release in the substantia nigra: an in vivo comparison with striatal dopamine release. J. Neurochem. 65: 192-200, 1995.
36. HEIKKILA, R. E. AND MANZINO, L. Behavioural properties of GBR 12909, GBR 13069 and GBR 13099: specific inhibitors of DA uptake. Eur. J. Pharmacol. 103: 241-248, 1984.
37. 2 receptor mRNAs are differentially expressed in limbic- and motor-related subpopulations of human mesencephalic neurons. Neuroscience 63: 357-362, 1994.
38. JAVITCH, J. A., D'AMATO, R. J., STRITTMATTER, S. M., AND SNYDER, S. H. Parkinsonism-inducing neurotoxin, MPTP: uptake of the metabolite N-methyl-4-phenylpyridine by dopamine neurons explains selective neurotoxicity. Proc. Natl. Acad. Sci. USA 82: 2173-2177, 1985.
39. JIMENEZ-CASTELLANOS, J. AND GRAYBIEL, A. M. Subdivisions of the dopamine containing A8-A9-A10 complex identified by their differential mesostriatal innervation of striosomes and extrastriosomal matrix. Neuroscience 23: 223-242, 1987.
40. 2+ ions during measurements of catecholamine release in slices of rat amygdala with fast-scan cyclic voltammetry. J. Neurosci. Methods 52: 1-10, 1994.
41. JURASKA, J. M., WILSON, C. J., AND GROVES, P. M. The substantia nigra of the rat: a Golgi study. J. Comp. Neurol. 172: 585-600, 1977.
42. KALIVAS, P. W. AND DUFFY, P. A comparison of axonal and somatodendritic DA release using in vivo dialysis. J. Neurochem. 56: 961-967, 1991.
43. 3H ]-dopamine is taken up and released from non-dopaminergic nerve terminals in the rat substantia nigra in vitro. J. Neurochem. 45: 137-144, 1985.
44. KREUGER, B. Kinetics and block of dopamine uptake in synaptosome from rat caudate nucleus. J. Neurochem. 55: 260-267, 1990.
45. LACEY, M. G., MERCURI, N. B., AND NORTH, R. A. Actions of cocaine on rat dopaminergic neurones in vitro. Br. J. Pharmacol. 99: 731-735, 1990.
46. LEVY, G. AND RAITERI, M. Carrier-mediated release of neurotransmitters. Trends Neurosci. 16: 415-419, 1993.
47. 2+-independent dopamine release from striatal slices: a possible role of reverse dopamine transport. J. Pharmacol. Exp. Ther. 256: 1132-1138, 1991.
48. MERCER, L., DEL FIACCO, M., AND CUELLO, A. C. The smooth endoplasmic reticulum as a possible storage site for dendritic dopamine in substantia nigra neurones. Experientia 35: 101-103, 1978.
49. MERCURI, N. B., CALABRESI, P., AND BERNARDI, G. The mechanism of amphetamine-induced inhibition of rat substantia nigra compacta neurones investigated with intracellular recording in vitro. Br. J. Pharmacol. 98: 127-134, 1989.
50. MERCURI, N. B., CALABRESI, P., AND BERNARDI, G. Dopamine uptake inhibition potentiates the effects of L-DOPA on rat substantia nigra zona compacta neurons. Neurosci. Lett. 126: 79-82, 1991.
51. MILLAR, J. Extracellular single and multiple unit recording with microelectrodes. In: Monitoring Neuronal Activity, edited by J. A. Stamford. London: Oxford Univ. Press, 1992, p. 1-27.
52. NEDERGAARD, S. AND GREENFIELD, S. A. Sub-populations of pars compacta neurons in the substantia nigra: the significance of qualitatively and quantitatively distinct conductances. Neuroscience 48: 423-437, 1992.
53. NICHOLSON, C. Interaction between diffusion and Michaelis-Menten uptake of dopamine following iontophoresis in striatum. Biophys. J. 68: 1699-1715, 1995.
54. NICHOLSON, C. AND HOUNSGAARD, J. Diffusion in the slice microenvronment and implications for physiological studies. Federation Proc. 42: 2865-2868, 1983.
55. NICHOLSON, C. AND RICE, M. E. Diffusion of ions and transmitters in the brain cell microenvironment. In: Volume Transmission in the Brain, edited by K. Fuxe and L. F. Agnati. New York: Raven, 1991, p. 279-294.
56. NIEOULLON, A., CHERAMY, A., AND GLOWINSKI, J. Release of DA in vivo from cat SN. Nature Land. 266: 375-377, 1977.
57. NlRENBERG, M. J., LlU, Y., PETER, D., EDWARDS, R. H., AND PlCKEL, V. M. The vesicular monoamine transporter-2 is present in small synaptic vesicles and preferentially localises to large dense core vesicles in rat solitary tract nuclei. Proc. Natl. Acad. Sci. USA 92: 8773-8777, 1995.
58. NlRENBERG, M. J., VAUGHAN, R. A., UHL, G. R., KUHAR, M. J., AND PlCKEL, V. M. The dopamine transporter is localized to dendritic and axonal plasma membranes of nigrostriatal dopaminergic neurons. J. Neurosci. 16: 436-447, 1996.
59. NISSBRANDT, H., ENGBERG, G., AND PILEBLAD, E. The effects of GBR 12909, a dopamine uptake inhibitor, on monoaminergic neurotransmission in rat striatum, limbic forebrain, cortical hemispheres and substantia nigra. Naunyn-Schmeidebergs Arch. Pharmacol. 344: 16-28, 1991.
60. PIFL, C., GIROS, B., AND CARON, M. G. Dopamine transporter expression confers cytotoxicity to low does of the parkinsonism-inducing neurotoxin MPTP. J. Neurosci. 13: 4246-4253, 1993.
61. POZZI, L., INVERNIZZI, R., CERVO, L., VALLEBUONA, F., AND SAMANIN, R. Evidence that extracellular concentrations of dopamine are regulated by noradrenergic neurons in the frontal cortex of rats. J. Neurochem. 63: 195-200, 1994.
62. QUATACKER, J. R., ANNAERT, W. G., MISEREZ, B. J., AND DE POTTER, W. P. Immunocytochemical demonstration of dopamine-β-hydroxylase and cytochrome B561 on the axonal reticulum in bovine sympathetic neurons. J. Histochem. Cytochem. 40: 1599-1604, 1992.
63. RICE, M. E., CRAGG, S. J., AND GREENFIELD, S. A. Characteristics of electrically evoked somatodendritic dopamine release in substantia nigra and ventral tegmental area in vitro. J. Neurophysiol. 77: 853-862, 1997.
64. RICE, M. E. AND NICHOLSON, C. Measurement of nanomolar dopamine diffusion using low noise perfluorinated ionomer coated carbon fiber microelectrodes and high speed cyclic voltammetry. Anal. Chem. 61: 1805-1810, 1989.
65. RICE, M. E. AND NICHOLSON, C. Diffusion and ion shifts in the brain extracellular microenvironment and their relevance for voltammetric measurements. In: Neuromethods: Voltammetric Methods in Brain Systems, edited by A. Boulton, G. Baker, and R. N. Adams. Clifton, NJ: Humana, 1995, vol. 27, p. 27-79.
66. RICE, M. E., RICHARDS, C. D., NEDERGAARD, S., HOUNSGAARD, J., NICHOL SON, C., AND GREENFIELD, S. A. Direct monitoring of dopamine and 5-HT release in substantia nigra and ventral tegmental area in vitro. Exp. Brain Res. 100: 395-406, 1994.
67. RICHFIELD, E.K. Quantitative autoradiography of the dopamine uptake complex in rat brain using [3h]GBR 12909. Brain Res. 540: 1-13, 1991.
68. SANGHERA, M. K., MANAYE, K. F., LIANG, C.-L., IACOPINO, A. M., BANNON, M.K., MANAYE, K. F., LIANG, C.-L., IACOPINO, A. M., BANNON, M. J., AND GERMAN, D. C. Low dopamine transporter mRNA levels in mid-brain regions containing calbindin. Neuroreport 5: 1641-1644, 1944.
69. SHIMADA, S., KITAYAMA, S., WALTHER, D., AND UHL, G. Dopamine transporter mRNA: dense expression in ventral midbrain neurons. Mol. Brain Res. 13: 359-362, 1992.
70. SIMON, J. R. AND GHETTI, B. Is there significant somatodendritic uptake of DA in the SN? Evidence from the Weaver mutant mouse. Neurochem. Int. 22: 471-477, 1933.
71. SITGES, M., REYES, A., AND CHIU, L. M. Dopamine transporter-mediated release of dopamine: role of cloride. J. Neurosci. Res. 39: 11-22, 1994.
72. SMEETS, W. J. AND STEINBUSCH, H. W. Distribution of noradrenaline immunoreactivity in the forebrain and midbrain of the lizard Gekko gecko. J. Comp. Neurol. 285: 453-466, 1989.
73. SMITS, R. P. J., STEINBUSCH, H. W. M., AND MULDER, A. H. Distribution of DA-immunoreactive cell bodies in the guinea pig brain. J. Chem. Neuroanat. 3: 101-123, 1990.
74. STUDER, A. AND SCHULTZ, W The catecholamine uptake inhibitor nomifensine depresses impulse activity of dopamine neurons in mouse substantia nigra. Neurosci. Lett. 80: 207-212, 1987.
75. SULZER, D. AND MAIDMENT, N. T. Amphetamine and other weak bases act to promote reverse transport of dopamine in ventral midbrain neurons. J. Neurochem. 60: 527-535, 1993.
76. SUNDSTRÖM, E., GOLDSTEIN, M., AND JONSSON, G. Uptake inhibition pro tects nigro-striatal dopamine neurons from the neurotoxicity of 1-methyl 4-phenylpyridine (MPP+) in mice. Eur. J. Pharmacol. 131: 289-292, 1986.
77. TULLOCH, I. F. AND JOHNSON, A. M. The pharmacological profile of paro xetine, a new selective serotonin re-uptake inhibitor. J. Clin. Psychiatry 53: 7-12, 1992.
78. WASSEF, M., BEROD, A., AND SOTELO, C. Dopaminergic dendrites in the pars reticulata of the rat substantia nigra and their striatal input. Combined immunocytochemical localisation of tyrosine hydroxylase and anterograde degeneration. Neuroscience 6: 2125-2139, 1982.
79. WASZCZAK, B. L. AND WALTERS, J. R. Endogenous dopamine can modulate inhibition of substantia nigra pars reticulata neurons elicited by GABA iontophoresis or striatal stimulation. J. Neurosci. 6: 120-126, 1986.
80. WHEELER, D. D., EDWARDS, A. M., CHAPMAN, B. M., AND ONDO, J. G. A model of the sodium dependence of dopamine uptake in rat striatal synaptosomes. Neurochem. Res. 18: 927-936, 1993.
81. WILSON, C. J., GROVES, P. M., AND FIFKÓVA, E. Monoaminergic synapses, including dendro-dendritic synapses in the rat substantia nigra. Exp. Brain Res. 30: 161-174, 1977.
82. YAMADA, T., MCGEER, P. L., BAIMBRIDGE, K. G., AND MCGEER, E. G. Relative sparing in Parkinson's disease of substantia nigra dopamine neurons containing calbindin-D28K. Brain Res. 526: 303-307, 1990.
83. YUNG, K. K., BOLAM, J. P., SMITH, A. D., HERSCH, S. M., CILIAX, B. J., AND LEVEY, A. I. Immunocytochemical localisation of D1 and D2 receptors in the basal ganglia of the rat: light and electron microscopy. Neuroscience 65: 709-730, 1995.