A computational theory of short-term synaptic plasticity: synapses learn to tell time

In computational neuroscience and deep learning models, synapses are viewed as simple computational elements with a single learnable parameter: synaptic strength. Here we propose that synapses are more sophisticated elements with multiple learnable parameters; allowing synapses to tune their short-term synaptic dynamics and optimize the processing of temporal information. We confirm a prediction of this hypothesis by showing that in mouse and human neocortex, synaptic dynamics is not preferentially shaped by the identity of the pre- or postsynaptic neuron. Using computational approaches, we demonstrate that learned synaptic dynamics allows for interval-selectivity and counting at the synaptic level, and significantly enhances the performance of feedforward networks on complex spatiotemporal tasks. Our results provide a framework to understand the mismatch between the computational simplicity of synapses in models and their biochemical complexity, as well as address a fundamental gap between how the brain and artificial neural networks process temporal information.