Single rodent mesohabenular axons release glutamate and GABA
Open accessAbstract
The lateral habenula (LHb) is involved in reward, aversion, addiction and depression through descending interactions with several brain structures, including the ventral tegmental area (VTA). The VTA provides reciprocal inputs to LHb, but their actions are unclear. Here we show that the majority of rat and mouse VTA neurons innervating LHb coexpress markers for both glutamate signaling (vesicular glutamate transporter 2; VGluT2) and GABA signaling (glutamic acid decarboxylase; GAD, and vesicular GABA transporter; VGaT). A single axon from these mesohabenular neurons coexpresses VGluT2 protein and VGaT protein and, surprisingly, establishes symmetric and asymmetric synapses on LHb neurons. In LHb slices, light activation of mesohabenular fibers expressing channelrhodopsin2 driven by VGluT2 (Slc17a6) or VGaT (Slc32a1) promoters elicits release of both glutamate and GABA onto single LHb neurons. In vivo light activation of mesohabenular terminals inhibits or excites LHb neurons. Our findings reveal an unanticipated type of VTA neuron that cotransmits glutamate and GABA and provides the majority of mesohabenular inputs.
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A VTA neuronal subtype coexpresses genes for the vesicular GABA transporter and vesicular glutamate transporter 2.
“One of the VTA neuronal subtypes is distinguished by coexpression of the genes encoding the vesicular transporters for GABA (Slc32a1) and glutamate (Slc17a6).32”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [32]
The postsynaptic LHb neuron may determine whether VTA input is primarily excitatory or inhibitory, likely through differential insertion of ionotropic GABA and glutamate receptors.
“suggesting that the postsynaptic LHb neuron, presumably by differential insertion of ionotropic GABA and glutamate receptors, may determine whether the input is primarily excitatory or inhibitory.”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [32]
These VTA neurons monosynaptically connect to lateral habenula neurons and cotransmit GABA and glutamate onto individual LHb neurons.
“They monosynaptically connect to neurons within the lateral habenula (mostly medial subregions) and cotransmit Cotransmission: process by which two (or more) neurotransmitters are synaptically released in response to an action potential and detected by receptors on the postsynaptic”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [32]
In vivo optogenetic excitation of VTA input to LHb causes excitation, inhibition, or both in extracellularly recorded LHb neurons.
“In vivo optogenetic excitation of VTA input to the LHb (using either Slc17a6-IRES-Cre or Slc32a1-IRES-Cre mice) results in either excitation, inhibition, or both of extracellularly recorded LHb neurons”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [32]
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- Authors
- Root, D. H., Mejias-Aponte, C. A., Zhang, S., Wang, H.-L., Hoffman, A. F., Lupica, C. R., & Morales, M.
- Affiliations
- National Institute on Drug Abuse (US)
- National Institutes of Health (US)
- Corresponding author
- Morales, Marisela
- Venue
- Nature Neuroscience
- Published
- 2014-09-21
- Volume
- 17
- Issue
- 11
- Pages
- 1543-1551
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC4843828
- OpenAlex
- W2033263745
- Cited by
- 349
- References
- 49
- Citations by year
- 2026: 17 · 2025: 25 · 2024: 34 · 2023: 27 · 2022: 27 · 2021: 27 · 2020: 28 · 2019: 31 · 2018: 30 · 2017: 37 · 2016: 25 · 2015: 37 · 2014: 3
- FWCI
- 15.53
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute on Drug Abuse (Z01DA000510)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
- Keywords
- ventral tegmental area, lateral habenula, glutamate co-release, co-transmission, vesicular glutamate transporter 2, vesicular GABA transporter, glutamic acid decarboxylase
- MeSH terms
- Animals, Axons, gamma-Aminobutyric Acid, Male, Neural Pathways, Reward, Synapses, Rats, Sprague-Dawley, Ventral Tegmental Area, Glutamic Acid, Habenula, Vesicular Glutamate Transport Protein 2
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