Chemical transmission between dopaminergic neuron pairs

*Université Pierre et Marie Curie, Paris 75005, France; and
^†Dynamique et Physiopathologie des Réseaux Neuronaux, Institut National de la Santé et de la Recherche Médicale U667, and
^‡Neurobiologie Pharmacologique, Institut National de la Santé et de la Recherche Médicale U114, Collège de France, 75005 Paris, France

Edited by Barry W. Connors, Brown University, Providence, RI, and accepted by the Editorial Board December 19, 2007 (received for review April 4, 2007)

Abstract

Midbrain dopaminergic (DAergic) neurons play a major regulatory role in in goal-directed behavior and reinforcement learning. DAergic neuron activity, and therefore spatiotemporal properties of dopamine release, precisely encodes reward signals. Neuronal activity is shaped both by external afferences and local interactions (chemical and electrical transmissions). Numerous hints suggest the existence of chemical interactions between DAergic neurons, but direct evidence and characterization are still lacking. Here, we show, using dual patch-clamp recordings in rat brain slices, a widespread bidirectional chemical transmission between DAergic neuron pairs. Hyperpolarizing postsynaptic potentials were partially mediated by D2-like receptors, and entirely resulted from the inhibition of the hyperpolarization-activated depolarizing current (Ih). These results constitute the first evidence in paired recordings of a chemical transmission relying on conductance decrease in mammals. In addition, we show that chemical transmission and electrical synapses frequently coexist within the same neuron pair and dynamically interact to shape DAergic neuron activity.

Footnotes

^§To whom correspondence should be addressed. E-mail: laurent.venance{at}college-de-france.fr
Author contributions: M.V. and L.V. designed research; M.V. performed research; M.V. analyzed data; and M.V., J.G., J.-M.D., and L.V. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. B.W.C. is a guest editor invited by the Editorial Board.
This article contains supporting information online at www.pnas.org/cgi/content/full/0703121105/DC1.