Ventral tegmental area glutamate neurons co-release GABA and promote positive reinforcement

Ji Hoon Yoo, Vivien Zell, Navarre Gutierrez-Reed, Johnathan Wu, Reed Ressler, Mohammad Ali Shenasa, Alexander B. Johnson, Kathryn H. Fife, Lauren Faget and Thomas S. Hnasko ()
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Ji Hoon Yoo: University of California, San Diego
Vivien Zell: University of California, San Diego
Navarre Gutierrez-Reed: Biomedical Sciences Graduate Program, University of California, San Diego
Johnathan Wu: University of California, San Diego
Reed Ressler: University of California, San Diego
Mohammad Ali Shenasa: University of California, San Diego
Alexander B. Johnson: University of California, San Diego
Kathryn H. Fife: Neuroscience Graduate Program, University of California, San Diego
Lauren Faget: University of California, San Diego
Thomas S. Hnasko: University of California, San Diego

Nature Communications, 2016, vol. 7, issue 1, 1-13

Abstract: Abstract In addition to dopamine neurons, the ventral tegmental area (VTA) contains GABA-, glutamate- and co-releasing neurons, and recent reports suggest a complex role for the glutamate neurons in behavioural reinforcement. We report that optogenetic stimulation of VTA glutamate neurons or terminals serves as a positive reinforcer on operant behavioural assays. Mice display marked preference for brief over sustained VTA glutamate neuron stimulation resulting in behavioural responses that are notably distinct from dopamine neuron stimulation and resistant to dopamine receptor antagonists. Whole-cell recordings reveal EPSCs following stimulation of VTA glutamate terminals in the nucleus accumbens or local VTA collaterals; but reveal both excitatory and monosynaptic inhibitory currents in the ventral pallidum and lateral habenula, though the net effects on postsynaptic firing in each region are consistent with the observed rewarding behavioural effects. These data indicate that VTA glutamate neurons co-release GABA in a projection-target-dependent manner and that their transient activation drives positive reinforcement.

Date: 2016
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DOI: 10.1038/ncomms13697

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