A dynamic spike threshold with correlated noise predicts observed patterns of negative interval correlations in neuronal spike trains

Abstract

Negative correlations in the sequential evolution of interspike intervals (ISIs) are a signature of memory in neuronal spike-trains. They provide coding benefits including firing-rate stabilization, improved detectability of weak sensory signals, and enhanced transmission of information by improving signal-to-noise ratio. Primary electrosensory afferent spike-trains in weakly electric fish fall into two categories based on the pattern of ISI correlations: non-bursting units have negative correlations which remain negative but decay to zero with increasing lags (Type I ISI correlations), and bursting units have oscillatory (alternating sign) correlation which damp to zero with increasing lags (Type II ISI correlations). Here, we predict and match observed ISI correlations in these afferents using a stochastic dynamic threshold model. We determine the ISI correlation function as a function of an arbitrary discrete noise correlation function {{,mathrm{mathbf {R}},}}_k, where k is a multiple of the mean ISI. The function permits forward and inverse calculations of the correlation function. Both types of correlation functions can be generated by adding colored noise to the spike threshold with Type I correlations generated with slow noise and Type II correlations generated with fast noise. A first-order autoregressive (AR) process with a single parameter is sufficient to predict and accurately match both types of afferent ISI correlation functions, with the type being determined by the sign of the AR parameter. The predicted and experimentally observed correlations are in geometric progression. The theory predicts that the limiting sum of ISI correlations is -0.5 yielding a perfect DC-block in the power spectrum of the spike train. Observed ISI correlations from afferents have a limiting sum that is slightly larger at -0.475 pm 0.04 (text {mean} pm text {s.d.}). We conclude that the underlying process for generating ISIs may be a simple combination of low-order AR and moving average processes and discuss the results from the perspective of optimal coding.