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- W2535101800 abstract "High-frequency neuronal action potential firing (>100 Hz frequency) occurs ubiquitously throughout the mammalian CNS. However, the detection and analysis of high-frequency neuronal signaling can be precluded by several technical reasons. Recent studies using high-resolution methods revealed remarkable speed of synaptic transmission at central synapses, reaching the kilohertz frequency range. At the cerebellar mossy fiber to granule cell synapse, the highest firing frequencies so far have been observed and high-resolution in vitro and in vivo studies are feasible. This synapse could thus serve as a prototype for high-frequency transmission. Despite surprisingly limited knowledge about and inconsistent definitions of fundamental synaptic parameters, a framework seems to emerge that establishes how synapses are tuned for high-frequency transmission. The speed of neuronal information processing depends on neuronal firing frequency. Here, we describe the evolutionary advantages and ubiquitous occurrence of high-frequency firing within the mammalian nervous system in general. The highest firing frequencies so far have been observed at the cerebellar mossy fiber to granule cell synapse. The mechanisms enabling high-frequency transmission at this synapse are reviewed and compared with other synapses. Finally, information coding of high-frequency signals at the mossy fiber synapse is discussed. The exceptionally high firing frequencies and amenability to high-resolution technical approaches both in vitro and in vivo establish the cerebellar mossy fiber synapse as an attractive model to investigate high-frequency signaling from the molecular up to the network level. The speed of neuronal information processing depends on neuronal firing frequency. Here, we describe the evolutionary advantages and ubiquitous occurrence of high-frequency firing within the mammalian nervous system in general. The highest firing frequencies so far have been observed at the cerebellar mossy fiber to granule cell synapse. The mechanisms enabling high-frequency transmission at this synapse are reviewed and compared with other synapses. Finally, information coding of high-frequency signals at the mossy fiber synapse is discussed. The exceptionally high firing frequencies and amenability to high-resolution technical approaches both in vitro and in vivo establish the cerebellar mossy fiber synapse as an attractive model to investigate high-frequency signaling from the molecular up to the network level. refers to the specialized area of presynaptic plasma membrane and the associated protein network where vesicle release occurs. Thus, active zones include presynaptic Ca2+ channels and several evolutionary conserved proteins that are involved in docking and priming of synaptic vesicles, recruitment of Ca2+ channels, and tethering of vesicles. Note that active zones seem not required for fusion competence of vesicles per se [104Wang S.S. et al.Fusion competent synaptic vesicles persist upon active zone disruption and loss of vesicle docking.Neuron. 2016; 91: 777-791Abstract Full Text Full Text PDF PubMed Scopus (10) Google Scholar], but rather appear to increase release probability and organize vesicle recruitment. contains a single mossy fiber bouton or terminal that contacts several GC dendrites and Golgi cell dendrites. In addition, a cerebellar glomerulus typically also includes axons of inhibitory Golgi cells. The glomerular structure is ensheathed by glia. can be used to estimate the time course of presynaptic vesicle release by measuring the postsynaptic current. The current is deconvolved using the measured waveform of miniature postsynaptic currents originating from spontaneous single vesicle fusion and a calculated ‘residual’ current due to glutamate accumulation in the synaptic cleft. For this type of deconvolution analysis, paired recordings between presynaptic terminal and postsynaptic neuron are required. proteins with Ca2+-binding domains that alter the spatiotemporal characteristics of intracellular Ca2+ concentration. Endogenous Ca2+ buffers can be classified as fixed (immobile) or mobile. Typical proteins that constitute endogenous mobile buffers include calretinin, parvalbumin, and calbindin. refers to a localized presynaptic Ca2+ signal that governs release of synaptic vesicles. Nanodomain coupling usually refers to a distance between the Ca2+ sensor of vesicles and the Ca2+ channels of <100 nm, with larger distances being termed ‘microdomain’ [59Eggermann E. et al.Nanodomain coupling between Ca2+ channels and sensors of exocytosis at fast mammalian synapses.Nat. Rev. Neurosci. 2012; 13: 7-21Crossref Scopus (164) Google Scholar, 60Stanley E.F. The nanophysiology of fast transmitter release.Trends Neurosci. 2016; 39: 183-197Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar]. This distance may change during development [62Wang L.Y. et al.Synaptic vesicles in mature calyx of Held synapses sense higher nanodomain calcium concentrations during action potential-evoked glutamate release.J. Neurosci. 2008; 28: 14450-14458Crossref PubMed Scopus (63) Google Scholar, 63Nakamura Y. et al.Nanoscale distribution of presynaptic Ca2+ channels and its impact on vesicular release during development.Neuron. 2015; 85: 145-158Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar]. can be used by neurons to represent information. For rate-coded signaling, the frequency of APs within a certain time frame, and not the temporal occurrence of APs, conveys the required information. Rate coding is typical in many sensory systems and motoneurons. the pool of readily releasable vesicles is heterogeneous [105Neher E. Merits and limitations of vesicle pool models in view of heterogeneous populations of synaptic vesicles.Neuron. 2015; 87: 1131-1142Abstract Full Text Full Text PDF PubMed Scopus (41) Google Scholar, 106Thanawala M.S. Regehr W.G. Presynaptic calcium influx controls neurotransmitter release in part by regulating the effective size of the readily releasable pool.J. Neurosci. 2013; 33: 4625-4633Crossref PubMed Scopus (50) Google Scholar] and might even be a ‘fussy concept’ [107Pan B. Zucker R.S. A general model of synaptic transmission and short-term plasticity.Neuron. 2009; 62: 539-554Abstract Full Text Full Text PDF PubMed Scopus (83) Google Scholar]. Here, we differentiate between the RRP that can be evoked by APs (RRPAP) and by depolarizations (RRPDepol). is measured with, for example, fluctuation analysis and back-extrapolations [105Neher E. Merits and limitations of vesicle pool models in view of heterogeneous populations of synaptic vesicles.Neuron. 2015; 87: 1131-1142Abstract Full Text Full Text PDF PubMed Scopus (41) Google Scholar, 106Thanawala M.S. Regehr W.G. Presynaptic calcium influx controls neurotransmitter release in part by regulating the effective size of the readily releasable pool.J. Neurosci. 2013; 33: 4625-4633Crossref PubMed Scopus (50) Google Scholar], but postsynaptic receptor saturation can cause an underestimation of this RRP. with depolarizations, an additional pool of slowly releasing vesicles (SRP [71Neher E. Sakaba T. Multiple roles of calcium ions in the regulation of neurotransmitter release.Neuron. 2008; 59: 861-872Abstract Full Text Full Text PDF PubMed Scopus (427) Google Scholar]) can be released, which is probably not being released by APs [72Sakaba T. Roles of the fast-releasing and the slowly releasing vesicles in synaptic transmission at the calyx of Held.J. Neurosci. 2006; 26: 5863-5871Crossref PubMed Scopus (73) Google Scholar]. However, dissecting the SRP and vesicle recruitment is difficult. In general, the higher the rate of vesicle recruitment is assumed, the smaller the RRP will be. For example, neglecting vesicle recruitment during depolarizations (with a duration of often >30 ms) or sucrose application (often >1 s) can lead to an overestimation of the RRP. describes an additional increase in release probability of synaptic vesicles after having been docked and primed at the presynaptic plasma membrane. refers to a type of information representation that relies on the temporal correlation of APs in different neurons. Temporal coding can be used for coincidence detection and has an important role in oscillating neuronal networks." @default.
- W2535101800 created "2016-10-28" @default.
- W2535101800 creator A5007022136 @default.
- W2535101800 creator A5068812519 @default.
- W2535101800 date "2016-11-01" @default.
- W2535101800 modified "2023-10-16" @default.
- W2535101800 title "The Cerebellar Mossy Fiber Synapse as a Model for High-Frequency Transmission in the Mammalian CNS" @default.
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