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Fast vesicle reloading and a large pool sustain high bandwidth transmission at a central synapse
Abstract
What limits the rate at which sensory information can be transmitted across synaptic connections in the brain? High-frequency signalling is restricted to brief bursts at many central excitatory synapses, whereas graded ribbon-type synapses can sustain release and transmit information at high rates. Here we investigate transmission at the cerebellar mossy fibre terminal, which can fire at over 200 Hz for sustained periods in vivo, yet makes few synaptic contacts onto individual granule cells. We show that connections between mossy fibres and granule cells can sustain high-frequency signalling at physiological temperature. We use fluctuation analysis and pharmacological block of desensitization to identify the quantal determinants of short-term plasticity and combine these with a short-term plasticity model and cumulative excitatory postsynaptic current analysis to quantify the determinants of sustained high-frequency transmission. We show that release is maintained at each release site by rapid reloading of release-ready vesicles from an unusually large releasable pool of vesicles (approximately 300 per site). Our results establish that sustained vesicular release at high rates is not restricted to graded ribbon-type synapses and that mossy fibres are well suited for transmitting broad-bandwidth rate-coded information to the input layer of the cerebellar cortex.
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“MF–GC synapses show a combination of synaptic facilitation and depression upon paired‐pulse stimulation, with depression prevailing at shorter intervals (Saviane & Silver, 2006).”
From MicroRNA‐138‐5p suppresses excitatory synaptic strength at the cerebellar input layer (2025) · cites this paper as Saviane & Silver, 2006
In the citing paper
“MF–GC synapses are capable of operating with a high bandwidth of presynaptic AP frequencies (Delvendahl & Hallermann, 2016) and typically exhibit prominent short‐term depression upon sustained stimulation (Saviane & Silver, 2006).”
From MicroRNA‐138‐5p suppresses excitatory synaptic strength at the cerebellar input layer (2025) · cites this paper as Saviane & Silver, 2006
Citations
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Cited by
Sorted by citations
Short-Term Presynaptic Plasticity
Regehr, W. G. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005702 · Cited by 482
Silver, R. A. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2864 · Cited by 481
Self-citationSynaptic Vesicle Pools and Dynamics
Alabi, A. A., & Tsien, R. W. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a013680 · Cited by 284
Structural determinants of transmission at large hippocampal mossy fiber synapses
Rollenhagen, A., Sätzler, K., Rodríguez, E. P., Jonas, P., Frotscher, M., & Lübke, J. H. R. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1946-07.2007 · Cited by 246
Synaptic weight set by Munc13-1 supramolecular assemblies
Sakamoto, H., Ariyoshi, T., Kimpara, N., Sugao, K., Taiko, I., Takikawa, K., Asanuma, D., Namiki, S., & Hirose, K. (2018) · Nature Neuroscience · doi:10.1038/s41593-017-0041-9 · Cited by 235
Metadata
- Authors
- Saviane, C., & Silver, R. A.
- Venue
- Nature
- Published
- 2006-02
- Volume
- 439
- Issue
- 7079
- Pages
- 983-987
- ISSN
- 0028-0836
- 1476-4687
- Cited by
- 241
- References
- 3
- Language
- en
- Licence
- www.springer.com/tdm (tdm)
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