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

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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)

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.

Suggested Citation

  • Ji Hoon Yoo & Vivien Zell & Navarre Gutierrez-Reed & Johnathan Wu & Reed Ressler & Mohammad Ali Shenasa & Alexander B. Johnson & Kathryn H. Fife & Lauren Faget & Thomas S. Hnasko, 2016. "Ventral tegmental area glutamate neurons co-release GABA and promote positive reinforcement," Nature Communications, Nature, vol. 7(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms13697
    DOI: 10.1038/ncomms13697
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    Cited by:

    1. Lauren Faget & Lucie Oriol & Wen-Chun Lee & Vivien Zell & Cody Sargent & Andrew Flores & Nick G. Hollon & Dhakshin Ramanathan & Thomas S. Hnasko, 2024. "Ventral pallidum GABA and glutamate neurons drive approach and avoidance through distinct modulation of VTA cell types," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Huanyuan Zhou & KongFatt Wong-Lin & Da-Hui Wang, 2018. "Parallel Excitatory and Inhibitory Neural Circuit Pathways Underlie Reward-Based Phasic Neural Responses," Complexity, Hindawi, vol. 2018, pages 1-20, April.

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