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J Neurophysiol 87: 1046-1056, 2002;
0022-3077/02 $5.00
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The Journal of Neurophysiology Vol. 87 No. 2 February 2002, pp. 1046-1056
Copyright ©2002 by the American Physiological Society

D2 Receptors Inhibit the Secretory Process Downstream From Calcium Influx in Dopaminergic Neurons: Implication of K+ Channels

Patrice Congar, Annie Bergevin, and Louis-Eric Trudeau

Départements de Pharmacologie et de Psychiatrie, Centre de Recherche en Sciences Neurologiques, Centre de Recherche Fernand Seguin, Université de Montréal, Quebec H3C 3J7, Canada

Congar, Patrice, Annie Bergevin, and Louis-Eric Trudeau. D2 Receptors Inhibit the Secretory Process Downstream From Calcium Influx in Dopaminergic Neurons: Implication of K+ Channels. J. Neurophysiol. 87: 1046-1056, 2002. Dopaminergic (DAergic) neurons possess D2-like somatodendritic and terminal autoreceptors that modulate cellular excitability and dopamine (DA) release. The cellular and molecular processes underlying the rapid presynaptic inhibition of DA release by D2 receptors remain unclear. Using a culture system in which isolated DAergic neurons establish self-innervating synapses ("autapses") that release both DA and glutamate, we studied the mechanism by which presynaptic D2 receptors inhibit glutamate-mediated excitatory postsynaptic currents (EPSCs). Action-potential evoked EPSCs were reversibly inhibited by quinpirole, a selective D2 receptor agonist. This inhibition was slightly reduced by the inward rectifier K+ channel blocker barium, largely prevented by the voltage-dependent K+ channel blocker 4-aminopyridine, and completely blocked by their combined application. The lack of a residual inhibition of EPSCs under these conditions argues against the implication of a direct inhibition of presynaptic Ca2+ channels. To evaluate the possibility of a direct inhibition of the secretory process, spontaneous miniature EPSCs were evoked by the Ca2+ ionophore ionomycin. Ionomycin-evoked release was insensitive to cadmium and dramatically reduced by quinpirole, providing evidence for a direct inhibition of quantal release at a step downstream to Ca2+ influx through voltage-dependent Ca2+ channels. Surprisingly, this effect of quinpirole on ionomycin-evoked release was blocked by 4-aminopyridine. These results suggest that D2 receptor activation decreases neurotransmitter release from DAergic neurons through a presynaptic mechanism in which K+ channels directly inhibit the secretory process.




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