Neuronal coupling benefits the encoding of weak periodic signals in symbolic spike patterns

Abstract

The biophysical mechanisms by which an input signal elicits a neuronal response are well known (sufficiently large inputs change the membrane potential of the neuron and generate electrical pulses, known as action potentials or spikes), yet, a good understanding of how neurons use these spikes to encode the signal information remains elusive. Recent theoretical studies have focused on how neurons encode a weak periodic signal (that by itself is unable to generate spikes) in a noisy environment, where stochastic electrical fluctuations that do not encode any information occur. Analyzing spike sequences generated by individual neurons and by two coupled neurons (that were simulated with the stochastic FitzHugh–Nagumo model), it has been found that the relative timing of the spikes can encode the signal information. Using a symbolic method to analyze the spike sequence, preferred and infrequent spike patterns were detected, whose probabilities vary with both, the amplitude and the frequency of the signal. To investigate if this encoding mechanism is plausible also for neuronal ensembles, here we analyze the activity of a group of neurons, when they all perceive a weak periodic signal. We find that, as in the case of one or two coupled neurons, the probabilities of the spike patterns, now computed from the spike sequences of all the neurons, depend on the signal’s amplitude and period, and thus, the patterns’ probabilities encode the information of the signal. We also find that the resonances with the period of the signal or with the noise level are more pronounced when a group of neurons perceive the signal, in comparison with when only one or two coupled neurons perceive it. Neuronal coupling is beneficial for signal encoding as a group of neurons is able to encode a small-amplitude signal, which could not be encoded when it is perceived by just one or two coupled neurons. Interestingly, we find that for a group of neurons, just a few connections with one another can significantly improve the encoding of small-amplitude signals. Our findings indicate that information encoding in preferred and infrequent spike patterns is a plausible mechanism that can be employed by neuronal populations to encode weak periodic inputs, exploiting the presence of neural noise.