ArticleThe Journal of neuroscience : the official journal of the Society for Neuroscience2011
A new kinetic framework for synaptic vesicle trafficking tested in synapsin knock-outs.
Article in The Journal of neuroscience : the official journal of the Society for Neuroscience, 2011. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 21 papers.
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Who cites it
21 citing papers in PubMed.
- Power-law adaptation in the presynaptic vesicle cycle.Communications biology · 2025Article
- Parallel processing of quickly and slowly mobilized reserve vesicles in hippocampal synapses.eLife · 2024Article
- A sequential two-step priming scheme reproduces diversity in synaptic strength and short-term plasticity.Proceedings of the National Academy of Sciences of the United States of America · 2022Article
- Article
- A Slow Short-Term Depression at Purkinje to Deep Cerebellar Nuclear Neuron Synapses Supports Gain-Control and Linear Encoding over Second-Long Time Windows.The Journal of neuroscience : the official journal of the Society for Neuroscience · 2020Article
- Glycinergic Transmission in the Presence and Absence of Functional GlyT2: Lessons From the Auditory Brainstem.Frontiers in synaptic neuroscience · 2020Article
- Sparse force-bearing bridges between neighboring synaptic vesicles.Brain structure & function · 2019Article
- Considerations for Measuring Activity-Dependence of Recruitment of Synaptic Vesicles to the Readily Releasable Pool.Frontiers in synaptic neuroscience · 2019Review
- Dynamic balance of excitation and inhibition rapidly modulates spike probability and precision in feed-forward hippocampal circuits.Journal of neurophysiology · 2016Article
- A Well-Defined Readily Releasable Pool with Fixed Capacity for Storing Vesicles at Calyx of Held.PLoS computational biology · 2016Article
- Functions of synapsins in corticothalamic facilitation: important roles of synapsin I.The Journal of physiology · 2015Article
- The structure and function of 'active zone material' at synapses.Philosophical transactions of the Royal Society of London. Series B, Biological sciences · 2015Review
- Quantitative analysis of vesicle recycling at the calyx of Held synapse.Proceedings of the National Academy of Sciences of the United States of America · 2015Article
- A three-pool model dissecting readily releasable pool replenishment at the calyx of held.Scientific reports · 2015Article
- ATP binding to synaspsin IIa regulates usage and clustering of vesicles in terminals of hippocampal neurons.The Journal of neuroscience : the official journal of the Society for Neuroscience · 2015Article
- Recovery of vesicular storage and release parameters after high frequency stimulation in rat hippocampus.Cognitive neurodynamics · 2013Article
- Sustaining rapid vesicular release at active zones: potential roles for vesicle tethering.Trends in neurosciences · 2013Review
- Overexpression of synapsin Ia in the rat calyx of Held accelerates short-term plasticity and decreases synaptic vesicle volume and active zone area.Frontiers in cellular neuroscience · 2013Article
- Synaptic vesicle pools and dynamics.Cold Spring Harbor perspectives in biology · 2012Review
- Synapsin selectively controls the mobility of resting pool vesicles at hippocampal terminals.The Journal of neuroscience : the official journal of the Society for Neuroscience · 2012Article
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8 authors.
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Abstract
At least two rate-limiting mechanisms in vesicle trafficking operate at mouse Schaffer collateral synapses, but their molecular/physical identities are unknown. The first mechanism determines the baseline rate at which reserve vesicles are supplied to a readily releasable pool. The second causes the supply rate to depress threefold when synaptic transmission is driven hard for extended periods. Previous models invoked depletion of a reserve vesicle pool to explain the reductions in the supply rate, but the mass-action assumption at their core is not compatible with kinetic measurements of neurotransmission under maximal-use conditions. Here we develop a new theoretical model of rate-limiting steps in vesicle trafficking that is compatible with previous and new measurements. A physical interpretation is proposed where local reserve pools consisting of four vesicles are tethered to individual release sites and are replenished stochastically in an all-or-none fashion. We then show that the supply rate depresses more rapidly in synapsin knock-outs and that the phenotype can be fully explained by changing the value of the single parameter in the model that would specify the size of the local reserve pools. Vesicle-trafficking rates between pools were not affected. Finally, optical imaging experiments argue against alternative interpretations of the theoretical model where vesicle trafficking is inhibited without reserve pool depletion. This new conceptual framework will be useful for distinguishing which of the multiple molecular and cell biological mechanisms involved in vesicle trafficking are rate limiting at different levels of synaptic throughput and are thus candidates for physiological and pharmacological modulation.
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