Cellular Mechanisms for the Stimulus-Evoked Quenching of Neuronal Variability

A wealth of experimental studies show that the trial-to-trial variability of neuronal activity is quenched during stimulus evoked responses. Several network models have been proposed to explain this phenomenon through a variety of circuit mechanisms. However, in all cases, from the vantage of a neuron embedded within the network,  quenching of its response variability is inherited from its synaptic input. We analyze in vivo whole cell recordings from principal cells in layer 2/3 of mouse visual cortex. While the variability of the membrane potential is quenched upon stimulation, the variability of excitatory and inhibitory currents afferent to the neuron are amplified.  This discord complicates the simple inheritance assumption that underpins network models of neuronal variability. We propose and validate an alternative (yet not mutually exclusive) mechanism for the quenching of neuronal variability.  We show how an increase in synaptic conductance in the evoked state shunts the transfer of current to the membrane potential, formally decoupling changes in their trial-to-trial variability.  The ubiquity of conductance based neuronal transfer combined with the simplicity of our model, provides an appealing framework. In particular, it shows how the dependence of cellular properties upon neuronal state is a critical, yet often ignored, factor.