Abstract
The segregation of the readily releasable pool of synaptic vesicles (RRP) in sub-pools that are differentially poised for exocytosis shapes short-term plasticity. However, the frequency-dependent mobilization of these sub-pools is poorly understood. Using slice recordings and modeling of synaptic activity at cerebellar granule cell to Purkinje cell synapses of mice, we describe two sub-pools in the RRP that can be differentially recruited upon ultrafast changes in the stimulation frequency. We show that at low-frequency stimulations, a first sub-pool is gradually silenced, leading to full blockage of synaptic transmission. Conversely, a second pool of synaptic vesicles that cannot be released by a single stimulus is recruited within milliseconds by high-frequency stimulation and support an ultrafast recovery of neurotransmitter release after low-frequency depression. This frequency-dependent mobilization or silencing of sub-pools in the RRP in terminals of granule cells may play a role in the filtering of sensorimotor information in the cerebellum.
Highlights
In neuronal networks, transfer of information largely relies on the ability of presynaptic terminals to convert changes in the firing rate of action potential (AP) into corresponding changes of neurotransmitter release
We describe two subsets of synaptic vesicles (SVs) in the readily-releasable pool (RRP) with distinct properties: a fully-releasable pool that can be released by a single AP and a reluctant pool that is available for fusion within milliseconds at high stimulation frequencies
In order to better understand the mechanisms underlying the strong facilitation of glutamate release during repetitive stimulations of the granule cells (GCs)-Purkinje cell (PC) synapse, we first measured synaptic transmission over a broad range of frequencies using transverse cerebellar slices prepared from young mice (P18 to P25)
Summary
Transfer of information largely relies on the ability of presynaptic terminals to convert changes in the firing rate of action potential (AP) into corresponding changes of neurotransmitter release. At synapses between granule cells (GCs) and molecular layer interneurons (MLIs), two subsets of the RRP have been described that are mobilized by a two-step process, the transition is faster than at the Calyx of Held (Ishiyama et al, 2014; Miki et al, 2016).
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