Abstract

Short-term synaptic depression, caused by depletion of releasable neurotransmitter, modulates the strength of neuronal connections in a history-dependent manner. Quantifying the statistics of synaptic transmission requires stochastic models that link probabilistic neurotransmitter release with presynaptic spike-train statistics. Common approaches are to model the presynaptic spike train as either regular or a memory-less Poisson process: few analytical results are available that describe depressing synapses when the afferent spike train has more complex, temporally correlated statistics such as bursts. Here we present a series of analytical results—from vesicle release-site occupancy statistics, via neurotransmitter release, to the post-synaptic voltage mean and variance—for depressing synapses driven by correlated presynaptic spike trains. The class of presynaptic drive considered is that fully characterised by the inter-spike-interval distribution and encompasses a broad range of models used for neuronal circuit and network analyses, such as integrate-and-fire models with a complete post-spike reset and receiving sufficiently short-time correlated drive. We further demonstrate that the derived post-synaptic voltage mean and variance allow for a simple and accurate approximation of the firing rate of the post-synaptic neuron, using the exponential integrate-and-fire model as an example. These results extend the level of biological detail included in models of synaptic transmission and will allow for the incorporation of more complex and physiologically relevant firing patterns into future studies of neuronal networks.

Highlights

  • Variability in synaptic function arises from stochasticity in processes ranging in scale from the transitory opening and closing of ion channels to probabilistic neurotransmitter release and vesicle restock [1,2,3,4]

  • Non-Poissonian activity is regularly observed in vivo [13,14,15,16] and models suggest that, even in the absence of short-term synaptic dynamics, it can have a substantial effect on the propagation of activity [17,18,19,20,21]

  • While average rate effects under the influence of depression have been extensively studied [30,31,32], a compact set of analytical results for correlated spike trains and stochastic quantal vesicle release from multiple sites has remained elusive. It has been shown [33] that correlated firing patterns more regular than Poissonian can increase the rate of vesicle release, thereby enhancing the fidelity and efficiency of signal transmission, whilst more irregular spike trains can lead to a decrease in neurotransmitter release [25, 27]

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Summary

Introduction

Variability in synaptic function arises from stochasticity in processes ranging in scale from the transitory opening and closing of ion channels to probabilistic neurotransmitter release and vesicle restock [1,2,3,4]. While average rate effects under the influence of depression have been extensively studied [30,31,32], a compact set of analytical results for correlated spike trains and stochastic quantal vesicle release from multiple sites has remained elusive (for a full discussion of existing results, see the Discussion) It has been shown [33] that correlated firing patterns more regular than Poissonian can increase the rate of vesicle release, thereby enhancing the fidelity and efficiency of signal transmission, whilst more irregular spike trains can lead to a decrease in neurotransmitter release [25, 27]

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