Know Thy Neighbour: A Normative Theory of Synaptic Depression

Synapses exhibit an extraordinary degree of short-term 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 normatively-justifiable 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 pre-synaptic membrane potential from the spikes it receives and prior expectations, as in a recursive filter. We show that short-term 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 non-linearity should be related to the properties of short-term plasticity in any particular cell type.