A frequency-resolved mutual information rate and its application to neural systems

The encoding and processing of time-dependent signals into sequences of action potentials of sensory neurons is still a challenging theoretical problem. Although, with some effort, it is possible to quantify the flow of information in the model-free framework of Shannon's information theory, this yields just a single number, the mutual information rate. This rate does not indicate which aspects of the stimulus are encoded. Several studies have identified mechanisms at the cellular and network level leading to low- or high-pass filtering of information, i.e., the selective coding of slow or fast stimulus components. However, these findings rely on an approximation, specifically, on the qualitative behavior of the coherence function, an approximate frequency-resolved measure of information flow, whose quality is generally unknown. Here, we develop an assumption-free method to measure a frequency-resolved information rate about a time-dependent Gaussian stimulus. We demonstrate its application for three paradigmatic descriptions of neural firing: an inhomogeneous Poisson process that carries a signal in its instantaneous firing rate; an integrator neuron (stochastic integrate-and-fire model) driven by a time-dependent stimulus; and the synchronous spikes fired by two commonly driven integrator neurons. In agreement with previous coherence-based estimates, we find that Poisson and integrate-and-fire neurons are broadband and low-pass filters of information, respectively. The band-pass information filtering observed in the coherence of synchronous spikes is confirmed by our frequency-resolved information measure in some but not all parameter configurations. Our results also explicitly show how the response-response coherence can fail as an upper bound on the information rate.