Optimal time scale for spike-time reliability: theory, simulations, and experiments

Use of spike timing to encode information requires that neurons respond with high temporal precision and with high reliability. Fast fluctuating stimuli are known to result in highly reproducible spike times across trials, whereas constant stimuli result in variable spike times. Here, we first studied mathematically how spike-time reliability depends on the rapidness of aperiodic stimuli. Then, we tested our theoretical predictions in computer simulations of neuron models (Hodgkin-Huxley and modified quadratic integrate-and-fire), as well as in patch-clamp experiments with real neurons (mitral cells in the olfactory bulb and pyramidal cells in the neocortex). As predicted by our theory, we found that for firing frequencies in the beta/gamma range, spike-time reliability is maximal when the time scale of the input fluctuations (autocorrelation time) is in the range of a few milliseconds (2-5 ms), coinciding with the time scale of fast synapses, and decreases substantially for faster and slower inputs. Finally, we comment how these findings relate to mechanisms causing neuronal synchronization.