Prospective and retrospective coding in cortical neurons

Brains can process sensory information from different modalities at astonishing speed; this is surprising as the integration of inputs through the membrane of each individual neuron already causes a delayed response. Neuronal recordings em in vitro reveal a possible explanation for this fast processing, in terms of individual neurons advancing their output firing rates with respect to the input, a concept which we refer to as prospective coding. The underlying mechanisms of prospective coding, however, are not completely understood. We propose a mechanistic explanation for individual neurons advancing their output on the level of single action potentials and instantaneous firing rates. We show that the spike generation mechanism can be the source for prospective (advanced) or retrospective (delayed) responses. A simplified Hodgkin-Huxley model identifies sodium inactivation as a source for prospective firing, controlling the timing of the neuron's output as a function of the voltage and its temporal derivative. We further show that slow adaptation processes, such as spike-frequency adaptation or deactivating dendritic currents, represent mechanisms generating prospective firing for inputs that undergo slow temporal modulations. In general, we show that adaptation processes at different time scales can cause advanced neuronal responses to time-varying inputs that are modulated on the corresponding time scales.