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Synapses exhibit an extraordinary degree of shortterm malleability, with release probabilities and effective synaptic strengths changing markedly over multiple timescales. From the perspective of a fixed computational operation in a network, this seems like a most unacceptable degree of added noise. We suggest an alternative theory according to which short term synaptic plasticity plays a normativelyjustifiable role. This theory starts from the commonplace observation that the spiking of a neuron is an incomplete, digital, report of the analog quantity that contains all the critical information, namely its membrane potential. We suggest that one key task for a synapse is to solve the inverse problem of estimating the presynaptic membrane potential from the spikes it receives and prior expectations, as in a recursive filter. We show that shortterm synaptic depression has canonical dynamics which closely resemble those required for optimal estimation, and that it indeed supports high quality estimation. Under this account, the local postsynaptic potential and the level of synaptic resources track the (scaled) mean and variance of the estimated presynaptic membrane potential. We make experimentally testable predictions for how the statistics of subthreshold membrane potential fluctuations and the form of spiking nonlinearity should be related to the properties of shortterm plasticity in any particular cell type.
Author Information
JeanPascal Pfister (Cambridge University)
Peter Dayan (Gatsby Unit, UCL)
I am Director of the Gatsby Computational Neuroscience Unit at University College London. I studied mathematics at the University of Cambridge and then did a PhD at the University of Edinburgh, specialising in associative memory and reinforcement learning. I did postdocs with Terry Sejnowski at the Salk Institute and Geoff Hinton at the University of Toronto, then became an Assistant Professor in Brain and Cognitive Science at the Massachusetts Institute of Technology before moving to UCL.
Mate Lengyel (University of Cambridge)
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