Statistics of subthreshold neuronal voltage fluctuations due to conductance-based synaptic shot noise

Abstract

Neurons in the central nervous system, and in the cortex in particular, are subject to a barrage of pulses from their presynaptic populations. These synaptic pulses are mediated by conductance changes and therefore lead to increases or decreases of the neuronal membrane potential with amplitudes that are dependent on the voltage: synaptic noise is multiplicative. The statistics of the membrane potential are of experimental interest because the measurement of a single subthreshold voltage can be used to probe the activity occurring across the presynaptic population. Though the interpulse interval is not always significantly smaller than the characteristic decay time of the pulses, and so the fluctuations have the nature of shot noise, the majority of results available in the literature have been calculated in the diffusion limit, which is valid for high-rate pulses. Here the effects that multiplicative conductance noise and shot noise have on the voltage fluctuations are examined. It is shown that both these aspects of synaptic drive sculpt high-order features of the subthreshold voltage distribution, such as the skew. It is further shown that the diffusion approximation can only capture the effects arising from the multiplicative conductance noise, predicting a negative voltage skew for excitatory drive. Exact results for the full dynamics are derived from a master-equation approach, predicting positively skewed distributions with long tails in voltage ranges typical for action potential generation. It is argued that, although the skew is a high-order feature of subthreshold voltage distributions, the increased probability of reaching firing threshold suggests a potential role for shot noise in shaping the neuronal transfer function.