Impact of correlated synaptic input on output firing rate and variability in simple neuronal models

Cortical neurons are typically driven by thousands of synaptic inputs. The arrival of a spike from one input may or may not be correlated with the arrival of other spikes from different inputs. How does this interdependence alter the probability that the postsynaptic neuron will fire? We constructed a simple random walk model in which the membrane potential of a target neuron fluctuates stochastically, driven by excitatory and inhibitory spikes arriving at random times. An analytic expression was derived for the mean output firing rate as a function of the firing rates and pairwise correlations of the inputs. This stochastic model made three quantitative predictions. (1) Correlations between pairs of excitatory or inhibitory inputs increase the fluctuations in synaptic drive, whereas correlations between excitatory-inhibitory pairs decrease them. (2) When excitation and inhibition are fully balanced (the mean net synaptic drive is zero), firing is caused by the fluctuations only. (3) In the balanced case, firing is irregular. These theoretical predictions were in excellent agreement with simulations of an integrate-and-fire neuron that included multiple conductances and received hundreds of synaptic inputs. The results show that, in the balanced regime, weak correlations caused by signals shared among inputs may have a multiplicative effect on the input-output rate curve of a postsynaptic neuron, i.e. they may regulate its gain; in the unbalanced regime, correlations may increase firing probability mainly around threshold, when output rate is low; and in all cases correlations are expected to increase the variability of the output spike train.