Biophysical information representation in temporally correlated spike trains

Abstract

Spike trains commonly exhibit interspike interval (ISI) correlations caused by spike-activated adaptation currents. Here we investigate how the dynamics of adaptation currents can represent spike pattern information generated from stimulus inputs. By analyzing dynamical models of stimulus-driven single neurons, we show that the activation states of the correlation-inducing adaptation current are themselves statistically independent from spike to spike. This paradoxical finding suggests a biophysically plausible means of information representation. We show that adaptation independence is elicited by input levels that produce regular, non-Poisson spiking. This adaptation-independent regime is advantageous for sensory processing because it does not require sensory inferences on the basis of multivariate conditional probabilities, reducing the computational cost of decoding. Furthermore, if the kinetics of postsynaptic activation are similar to the adaptation, the activation state information can be communicated postsynaptically with no information loss, leading to an experimental prediction that simple synaptic kinetics can decorrelate the correlated ISI sequence. The adaptation-independence regime may underly efficient weak signal detection by sensory afferents that are known to exhibit intrinsic correlated spiking, thus efficiently encoding stimulus information at the limit of physical resolution.