ArticleThe Journal of neuroscience : the official journal of the Society for Neuroscience2009
Presynaptic G-protein-coupled receptors dynamically modify vesicle fusion, synaptic cleft glutamate concentrations, and motor behavior.
Article in The Journal of neuroscience : the official journal of the Society for Neuroscience, 2009. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 20 papers.
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Who cites it
20 citing papers in PubMed, 31 citations in OpenAlex.
- Synaptic Integration of Subquantal Neurotransmission by Colocalized G Protein-Coupled Receptors in Presynaptic Terminals.The Journal of neuroscience : the official journal of the Society for Neuroscience · 2022Article
- Neurotransmitter content heterogeneity within an interneuron class shapes inhibitory transmission at a central synapse.Frontiers in cellular neuroscience · 2022Article
- Acetate, a Short-Chain Fatty Acid, Acutely Lowers Heart Rate and Cardiac Contractility Along with Blood Pressure.The Journal of pharmacology and experimental therapeutics · 2021Article
- The serotonin reuptake blocker citalopram destabilizes fictive locomotor activity in salamander axial circuits through 5-HTJournal of neurophysiology · 2020Article
- Serotonergic Modulation of Locomotor Activity From Basal Vertebrates to Mammals.Frontiers in neural circuits · 2020Review
- Gβγ SNARE Interactions and Their Behavioral Effects.Neurochemical research · 2019Review
- Disabling the Gβγ-SNARE interaction disrupts GPCR-mediated presynaptic inhibition, leading to physiological and behavioral phenotypes.Science signaling · 2019Article
- Dynamin 1 Restrains Vesicular Release to a Subquantal Mode In Mammalian Adrenal Chromaffin Cells.The Journal of neuroscience : the official journal of the Society for Neuroscience · 2019Article
- Axonal Ensheathment in the Nervous System of Lamprey: Implications for the Evolution of Myelinating Glia.The Journal of neuroscience : the official journal of the Society for Neuroscience · 2018Article
- Dopamine-mediated calcium channel regulation in synaptic suppression in L. stagnalis interneurons.Channels (Austin, Tex.) · 2018Article
- Environmental Enrichment Upregulates Striatal Synaptic Vesicle-Associated Proteins and Improves Motor Function.Frontiers in neurology · 2018Article
- Sensory Activation of Command Cells for Locomotion and Modulatory Mechanisms: Lessons from Lampreys.Frontiers in neural circuits · 2016Review
- Serotonin Attenuates Feedback Excitation onto O-LM Interneurons.Cerebral cortex (New York, N.Y. : 1991) · 2015Article
- Cdc42 controls the dilation of the exocytotic fusion pore by regulating membrane tension.Molecular biology of the cell · 2014Article
- A synaptic mechanism for network synchrony.Frontiers in cellular neuroscience · 2014Review
- Modulation of neurotransmission by GPCRs is dependent upon the microarchitecture of the primed vesicle complex.The Journal of neuroscience : the official journal of the Society for Neuroscience · 2014Article
- GPCR mediated regulation of synaptic transmission.Progress in neurobiology · 2012Review
- Label-free detection of G protein-SNARE interactions and screening for small molecule modulators.ACS chemical neuroscience · 2012Article
- Inhibition of Ca2+ channels and adrenal catecholamine release by G protein coupled receptors.Cellular and molecular neurobiology · 2010Review
- Article
Corrections and comments
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Authors and funding
6 authors at 3 institutions in 3 countries.
Funding
Abstract
Understanding how neuromodulators regulate behavior requires investigating their effects on functional neural systems, but also their underlying cellular mechanisms. Utilizing extensively characterized lamprey motor circuits, and the unique access to reticulospinal presynaptic terminals in the intact spinal cord that initiate these behaviors, we investigated effects of presynaptic G-protein-coupled receptors on locomotion from the systems level, to the molecular control of vesicle fusion. 5-HT inhibits neurotransmitter release via a Gbetagamma interaction with the soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) complex that promotes kiss-and-run vesicle fusion. In the lamprey spinal cord, we demonstrate that, although presynaptic 5-HT receptors inhibit evoked neurotransmitter release from reticulospinal command neurons, their activation does not abolish locomotion but rather modulates locomotor rhythms. Liberation of presynaptic Gbetagamma causes substantial inhibition of AMPA receptor-mediated synaptic responses but leaves NMDA receptor-mediated components of neurotransmission mostly intact. Because Gbetagamma binding to the SNARE complex is displaced by Ca(2+)-synaptotagmin binding, 5-HT-mediated inhibition displays Ca(2+) sensitivity. We show that, as Ca(2+) accumulates presynaptically during physiological bouts of activity, 5-HT/Gbetagamma-mediated presynaptic inhibition is relieved, leading to a frequency-dependent increase in synaptic concentrations of glutamate. This frequency-dependent phenomenon mirrors a shift in the vesicle fusion mode and a recovery of AMPA receptor-mediated EPSCs from inhibition without a modification of NMDA receptor EPSCs. We conclude that activation of presynaptic 5-HT G-protein-coupled receptors state-dependently alters vesicle fusion properties to shift the weight of NMDA versus AMPA receptor-mediated responses at excitatory synapses. We have therefore identified a novel mechanism in which modification of vesicle fusion modes may profoundly alter locomotor behavior.
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Registered trials
Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.