Voltage dependence of synaptic plasticity is essential for rate based learning with short stimuli

In computational neuroscience, synaptic plasticity rules are often formulated in terms of firing rates. The predominant description of in vivo neuronal activity, however, is the instantaneous rate (or spiking probability). In this article we resolve this discrepancy by showing that fluctuations of the membrane potential carry enough information to permit a precise estimate of the instantaneous rate in balanced networks. As a consequence, we find that rate based plasticity rules are not restricted to neuronal activity that is stable for hundreds of milliseconds to seconds, but can be carried over to situations in which it changes every few milliseconds. We illustrate this, by showing that a voltage-dependent realization of the classical BCM rule achieves input selectivity, even if stimulus duration is reduced to a few milliseconds each.