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The Journal of Neuroscience, January 12, 2005, 25(2):291-298; doi:10.1523/JNEUROSCI.4167-04.2005

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Cellular/Molecular
Electrical Synapses between Dopaminergic Neurons of the Substantia Nigra Pars Compacta

Marie Vandecasteele, Jacques Glowinski, and Laurent Venance

Laboratoire de Neurobiologie Pharmacologique, Institut National de la Santé et de la Recherche Médicale, Collège de France, 75005 Paris, France

Spatiotemporal properties of dopamine release play a major role both in striatal and nigral physiology because dopamine is released from nerve terminals and dendrites of nigrostriatal dopaminergic (DA) neurons. Pioneering work revealed gap junctional communication (assessed by dye-coupling experiments) between DA cells in the substantia nigra pars compacta (SNc). However, direct evidence of functional electrical synapses between DA neurons is still lacking. In this study, gap junctional communication between DA neurons was investigated in rat brain slices. Tracer coupling was observed in postnatal day 5 (P5) to P10 and P15-P25 rats. Dual whole-cell patch-clamp recordings revealed that 96% of DA neurons were coupled by electrical synapses in P7-P10 rats, and 20% were coupled in P17-P21 rats. These electrical synapses were mainly symmetrical and displayed strong low-pass filtering properties. When spontaneous firing activity was monitored, no significant synchronization was observed. Nevertheless, an efficient modulation of the spontaneous firing frequency of the postsynaptic cell occurred during injection of hyperpolarizing and depolarizing currents in the coupled presynaptic cell. Together, these observations demonstrate the existence of a fast communication between SNc DA neurons through electrical synapses.

Key words: dopaminergic neuron; substantia nigra pars compacta; electrical synapse; paired recordings; gap junctions; connexin

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Received June 3, 2004; revised November 16, 2004; accepted November 17, 2004.

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