An essential role of acetylcholine-glutamate synergy at habenular synapses in nicotine dependence
Open accessAbstract
A great deal of interest has been focused recently on the habenula and its critical role in aversion, negative-reward and drug dependence. Using a conditional mouse model of the ACh-synthesizing enzyme choline acetyltransferase (Chat), we report that local elimination of acetylcholine (ACh) in medial habenula (MHb) neurons alters glutamate corelease and presynaptic facilitation. Electron microscopy and immuno-isolation analyses revealed colocalization of ACh and glutamate vesicular transporters in synaptic vesicles (SVs) in the central IPN. Glutamate reuptake in SVs prepared from the IPN was increased by ACh, indicating vesicular synergy. Mice lacking CHAT in habenular neurons were insensitive to nicotine-conditioned reward and withdrawal. These data demonstrate that ACh controls the quantal size and release frequency of glutamate at habenular synapses, and suggest that the synergistic functions of ACh and glutamate may be generally important for modulation of cholinergic circuit function and behavior.
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Complementary dependencies may explain observed synergies between vGluT and VAChT or vGluT and ZnT3 on the same synaptic vesicle.
“These complementary dependencies may explain the observed synergies between vGluT and VAChT or vGluT and the vesicular zinc transporter (ZnT3) when these are localized to the same synaptic vesicle.5,21,22”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [21]
Several groups found that vGluT and VAChT function synergistically, and depletion of one transporter or neurotransmitter also depletes loading and release of the other.
“Interestingly, several groups have found that vGluT and VAChT function synergistically and that depletion of one transporter or neurotransmitter also depletes loading and release of the other.21,22,63,69”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [21]
Immunogold EM and immunoprecipitation suggest that vGluT and VAChT co-package glutamate and ACh into the same synaptic vesicle in mHb-IPN and striatal cholinergic-to-SPN synapses.
“Immunogold EM and immunoprecipitation experiments suggest that vGluT and VAChT co-package glutamate and ACh into the same synaptic vesicle in both mHb to IPN synapses and striatal cholinergic to medium spiny neuron synapses 21,22,56 (Figure 1A).”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [21]
Ach and glutamate are copackaged into the same synaptic vesicles at the mHb-to-IPN synapse.
“Several groups have found evidence for Ach and glutamate being copackaged into the same synaptic vesicles at this synapse 21,22,56,124”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [21]
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Translational Research in Nicotine DependencePreprint
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Basal forebrain cholinergic signalling: development, connectivity and roles in cognition
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Synaptic and circuit functions of multitransmitter neurons in the mammalian brain
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Paradoxical network excitation by glutamate release from VGluT3+ GABAergic interneurons
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Chronic Nicotine Exposure Alters the Neurophysiology of Habenulo-Interpeduncular Circuitry
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- Authors
- Frahm, S., Antolin-Fontes, B., Görlich, A., Zander, J.-F., Ahnert-Hilger, G., & Ibañez-Tallon, I.
- Affiliations
- Max Delbrück Center (DE)
- Molecular Neurobiology Group, Max Delbrück Center for Molecular Medicine, Berlin, Germany
- Rockefeller University (US)
- Charité – Universitätsmedizin Berlin (DE)
- Institute for Integrative Neuroanatomy, Charité - Universitätsmedizin Berlin, Berlin, Germany
- ORCID
- Frahm, Silke
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2015-12-01
- Volume
- 4
- Pages
- e11396-e11396
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC4718731
- OpenAlex
- W2186909533
- Cited by
- 98
- References
- 104
- Citations by year
- 2026: 1 · 2025: 13 · 2024: 9 · 2023: 10 · 2022: 8 · 2021: 16 · 2020: 8 · 2019: 12 · 2018: 4 · 2017: 12 · 2016: 5
- FWCI
- 3.27
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (acceptedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institute on Drug Abuse (P30DA035756)
- Deutsche Forschungsgemeinschaft (GO 2334/1-1, AH67/7-1)
- Helmholtz-Gemeinschaft
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- acetylcholine, glutamate, habenula, nicotine dependence, choline acetyltransferase, medial habenula, interpeduncular nucleus, synaptic vesicles, presynaptic facilitation, nicotine reward, nicotine withdrawal, cholinergic circuits, vesicular glutamate transporter, quantal release
- MeSH terms
- Acetylcholine, Animals, Conditioning, Classical, Synapses, Tobacco Use Disorder, Glutamic Acid, Habenula, Mice, Cholinergic Neurons
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
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