Interspike interval correlations in neuron models with adaptation and correlated noise

The generation of neural action potentials (spikes) is random but nevertheless may result in a rich statistical structure of the spike sequence. In particular, contrary to the popular renewal assumption of theoreticians, the intervals between adjacent spikes are often correlated. Experimentally, different patterns of interspike-interval correlations have been observed and computational studies have identified spike-frequency adaptation and correlated noise as the two main mechanisms that can lead to such correlations. Analytical studies have focused on the single cases of either correlated (colored) noise or adaptation currents in combination with uncorrelated (white) noise. For low-pass filtered noise or adaptation, the serial correlation coefficient can be approximated as a single geometric sequence of the lag between the intervals, providing an explanation for some of the experimentally observed patterns. Here we address the problem of interval correlations for a widely used class of models, multidimensional integrate-and-fire neurons subject to a combination of colored and white noise sources and a spike-triggered adaptation current. Assuming weak noise, we derive a simple formula for the serial correlation coefficient, a sum of two geometric sequences, which accounts for a large class of correlation patterns. The theory is confirmed by means of numerical simulations in a number of special cases including the leaky, quadratic, and generalized integrate-and-fire models with colored noise and spike-frequency adaptation. Furthermore we study the case in which the adaptation current and the colored noise share the same time scale, corresponding to a slow stochastic population of adaptation channels; we demonstrate that our theory can account for a nonmonotonic dependence of the correlation coefficient on the channel’s time scale. Another application of the theory is a neuron driven by network-noise-like fluctuations (green noise). We also discuss the range of validity of our weak-noise theory and show that by changing the relative strength of white and colored noise sources, we can change the sign of the correlation coefficient. Finally, we apply our theory to a conductance-based model which demonstrates its broad applicability.Author summary: The elementary processing units in the central nervous system are neurons that transmit information by short electrical pulses, so called action potentials or spikes. The generation of the action potential is a random process that can be shaped by correlated fluctuations (colored noise) and by adaptation. A consequence of these two ubiquitous features is that the successive time intervals between spikes, the interspike intervals, are not independent but correlated. As these correlations can significantly improve information transmission and weak-signal detection, it is an important task to develop analytical approaches to these statistics for well-established computational models. Here we present a theory of interval correlations for a widely used class of integrate-and-fire models endowed with an adaptation mechanism and subject to correlated fluctuations. We demonstrate which patterns of interval correlations can be expected from the interplay of colored noise, adaptation and intrinsic nonlinear dynamics.