Rapid, activity-independent turnover of vesicular transmitter content at a mixed glycine/GABA synapse
Open accessAbstract
The release of neurotransmitter via the fusion of transmitter-filled, presynaptic vesicles is the primary means by which neurons relay information. However, little is known regarding the molecular mechanisms that supply neurotransmitter destined for vesicle filling, the endogenous transmitter concentrations inside presynaptic nerve terminals, or the dynamics of vesicle refilling after exocytosis. We addressed these issues by recording from synaptically coupled pairs of glycine/GABA coreleasing interneurons (cartwheel cells) of the mouse dorsal cochlear nucleus. We find that the plasma membrane transporter GlyT2 and the intracellular enzyme glutamate decarboxylase supply the majority of glycine and GABA, respectively. Pharmacological block of GlyT2 or glutamate decarboxylase led to rapid and complete rundown of transmission, whereas increasing GABA synthesis via intracellular glutamate uncaging dramatically potentiated GABA release within 1 min. These effects were surprisingly independent of exocytosis, indicating that prefilled vesicles re-equilibrated upon acute changes in cytosolic transmitter. Titration of cytosolic transmitter with postsynaptic responses indicated that endogenous, nonvesicular glycine/GABA levels in nerve terminals are 5-7 mm, and that vesicular transport mechanisms are not saturated under basal conditions. Thus, cytosolic transmitter levels dynamically set the strength of inhibitory synapses in a release-independent manner.
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Packaging GABA and/or glycine into vesicles largely depends on their intracellular intraaxonal concentrations, controlled by GAD1/2 synthesis or GlyT1/2 transporters.
“Therefore, packaging GABA and/or glycine into vesicles is largely dependent on their intracellular (intraaxonal) concentration, which are controlled by either intracellular synthesis (glutamate decarboxylase [GAD] 1/2) or plasma membrane transporters (GlyT1/2), respectively.51”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [51]
Synaptic potency depends not only on postsynaptic receptor number but also on presynaptic transmitter concentrations and vesicular loading.
“These results suggest that the potency of a synapse depends not only on the number of postsynaptic receptors but also on the concentrations of presynaptic transmitter and how much transmitter is loaded into the vesicle.”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [51]
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- Authors
- Apostolides, P. F., & Trussell, L. O.
- Affiliations
- Oregon Health & Science University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2013-03-13
- Volume
- 33
- Issue
- 11
- Pages
- 4768-4781
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3639006
- OpenAlex
- W2055623289
- Cited by
- 77
- References
- 66
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 2 · 2023: 10 · 2022: 4 · 2021: 5 · 2020: 4 · 2019: 4 · 2018: 5 · 2017: 9 · 2016: 10 · 2015: 4 · 2014: 12 · 2013: 5
- FWCI
- 5.07
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute on Deafness and Other Communication Disorders (F31DC012222, P30DC005983, R01DC004450)
- National Institute of Neurological Disorders and Stroke (R01NS028901)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
- Keywords
- glycine transporter 2, glutamic acid decarboxylase, cartwheel cells, dorsal cochlear nucleus, glutamate uncaging, inhibitory synapses, neurotransmitter transporters
- MeSH terms
- Channelrhodopsins, Animals, Benzamides, Biophysics, Electric Stimulation, Female, gamma-Aminobutyric Acid, Glutamate Decarboxylase, Glutamates, Glycine, Indoles, Interneurons, Male, Mice, Inbred CBA, Mice, Inbred C57BL, Mice, Transgenic, Models, Neurological, Neural Inhibition, Synaptic Transmission, Pregnancy, Pyridazines, Strychnine, Synapses, Synaptic Vesicles, Tetrodotoxin, Time Factors, Cochlear Nucleus, Patch-Clamp Techniques, Glycine Agents, Excitatory Amino Acid Antagonists, GABA Antagonists, Sodium Channel Blockers, Glycine Plasma Membrane Transport Proteins, Mice, Inhibitory Postsynaptic Potentials, In Vitro Techniques
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