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The Journal of Neuroscience, January 28, 2004, 24(4):972-981; doi:10.1523/JNEUROSCI.4317-03.2004
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Cellular/Molecular
Dopamine Neurons Mediate a Fast Excitatory Signal via Their Glutamatergic Synapses
Nao Chuhma,1,6 Hui Zhang,2 Justine Masson,1,6 Xiaoxi Zhuang,7 David Sulzer,1,2,6 René Hen,3,5 andStephen Rayport1,4,5,6 Departments of 1Psychiatry, 2Neurology, 3Pharmacology, and 4Anatomy and Cell Biology, and 5Center for Neurobiology and Behavior, Columbia University, New York, New York 10032, 6Department of Neuroscience, New York State Psychiatric Institute, New York, New York 10032, and 7Department of Neurobiology, Pharmacology and Physiology, University of Chicago, Chicago, Illinois 60637
Dopamine neurons are thought to convey a fast, incentive salience signal, faster than can be mediated by dopamine. A resolution of this paradox may be that midbrain dopamine neurons exert fast excitatory actions. Using transgenic mice with fluorescent dopamine neurons, in which the axonal projections of the neurons are visible, we made horizontal brain slices encompassing the mesoaccumbens dopamine projection. Focal extracellular stimulation of dopamine neurons in the ventral tegmental area evoked dopamine release and early monosynaptic and late polysynaptic excitatory responses in postsynaptic nucleus accumbens neurons. Local superfusion of the ventral tegmental area with glutamate, which should activate dopamine neurons selectively, produced an increase in excitatory synaptic events. Local superfusion of the ventral tegmental area with the D2 agonist quinpirole, which should increase the threshold for dopamine neuron activation, inhibited the early response. So dopamine neurons make glutamatergic synaptic connections to accumbens neurons. We propose that dopamine neuron glutamatergic transmission may be the initial component of the incentive salience signal.
Key words: accumbens; addiction; dopamine; schizophrenia; slice; glutamate; ventral tegmental area; yellow fluorescent protein; incentive salience
Received Sep 22, 2003; revised November 30, 2003; accepted December 1, 2003.
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