A unified approach to the study of temporal, correlational and rate coding

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Abstract
We demonstrate that the information contained in the spike occurrence times of a population of neurons can be broken up into a series of terms, each of which reflect something about potential coding mechanisms. This is possible in the coding r{\'e}gime in which few spikes are emitted in the relevant time window. This approach allows us to study the additional information contributed by spike timing beyond that present in the spike counts; to examine the contributions to the whole information of different statistical properties of spike trains, such as firing rates and correlation functions; and forms the basis for a new quantitative procedure for the analysis of simultaneous multiple neuron recordings. It also provides theoretical constraints upon neural coding strategies. We find a transition between two coding r{\'e}gimes, depending upon the size of the relevant observation timescale. For time windows shorter than the timescale of the stimulus-induced response fluctuations, there exists a spike count coding phase, where the purely temporal information is of third order in time. For time windows much longer than the characteristic timescale, there can be additional timing information of first order, leading to a temporal coding phase in which timing information may affect the instantaneous information rate. We study the relative contributions of the dynamic firing rate and correlation variables to the full temporal information; the interaction of signal and noise correlations in temporal coding; synergy between spikes and between cells; and the effect of refractoriness. We illustrate the utility of the technique by analysis of a few cells from the rat barrel cortex.

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