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The Journal of Neuroscience, October 1, 2001, 21(19):7841-7847

Novel Ca²⁺ Dependence and Time Course of Somatodendritic Dopamine Release: Substantia Nigra versus Striatum

Billy T. Chen and Margaret E. Rice

Departments of Physiology and Neuroscience and Neurosurgery, New York University School of Medicine, New York, New York 10016

Somatodendritic release of dopamine (DA) in midbrain represents a novel form of intercellular signaling that inherently differs from classic axon-terminal release. Here we report marked differences in the Ca²⁺ dependence and time course of stimulated increases in extracellular DA concentration ([DA]_o) between the substantia nigra pars compacta (SNc) and striatum. Evoked [DA]_o was monitored with carbon-fiber microelectrodes and fast-scan cyclic voltammetry in brain slices. In striatum, pulse-train stimulation (10 Hz, 30 pulses) failed to evoke detectable [DA]_o in 0 or 0.5 mM Ca²⁺ but elicited robust release in 1.5 mM Ca²⁺. Release increased progressively in 2.0 and 2.4 mM Ca²⁺. In sharp contrast, evoked [DA]_o in SNc was nearly half-maximal in 0 mM Ca²⁺ and increased significantly in 0.5 mM Ca²⁺. Surprisingly, somatodendritic release was maximal in 1.5 mM Ca²⁺, with no change in 2.0 or 2.4 mM Ca²⁺. Additionally, after single-pulse stimulation, evoked [DA]_o in striatum reached a maximum (t_max) in <200 msec, whereas in SNc, [DA]_o continued to rise for 2-3 sec. Similarly, the time for [DA]_o to decay to 50% of maximum (t₅₀) was 12-fold longer in SNc than striatum. A delayed t_max in SNc compared with striatum persisted when DA uptake was inhibited by GBR-12909 and D₂ autoreceptors were blocked by sulpiride, although these agents eliminated the difference in t₅₀. Together, these data implicate different release mechanisms in striatum and SNc, with minimal Ca²⁺ required to trigger prolonged DA release in SNc. Coupled with limited uptake, prolonged somatodendritic release would facilitate DA-mediated volume transmission in midbrain.

Key words: calcium; dopamine; dopamine transporter; substantia nigra pars compacta; voltammetry; volume transmission; synaptic transmission

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Copyright © 2001 Society for Neuroscience  0270-6474/01/21197841-07$05.00/0

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