Spike-frequency Adaptation Separates Transient Communication Signals from Background Oscillations

Spike-frequency adaptation is a prominent feature of many neurons. However, little is known about its computational role in processing behaviorally relevant natural stimuli beyond filtering out slow changes in stimulus intensity. Here, we present a more complex example in which we demonstrate how spike-frequency adaptation plays a key role in separating transient signals from slower oscillatory signals. We recorded in vivo from very rapidly adapting electroreceptor afferents of the weakly electric fish Apteronotus leptorhynchus. The firing-frequency response of electroreceptors to fast communication stimuli ("small chirps") is strongly enhanced compared with the response to slower oscillations ("beats") arising from interactions of same-sex conspecifics. We are able to accurately predict the electroreceptor afferent response to chirps and beats, using a recently proposed general model for spike-frequency adaptation. The parameters of the model are determined for each neuron individually from the responses to step stimuli. We conclude that the dynamics of the rapid spike-frequency adaptation is sufficient to explain the data. Analysis of additional data from step responses demonstrates that spike-frequency adaptation acts subtractively rather than divisively as expected from depressing synapses. Therefore, the adaptation dynamics is linear and creates a high-pass filter with a cutoff frequency of 23 Hz that separates fast signals from slower changes in input. A similar critical frequency is seen in behavioral data on the probability of a fish emitting chirps as a function of beat frequency. These results demonstrate how spike-frequency adaptation in general can facilitate extraction of signals of different time scales, specifically high-frequency signals embedded in slower oscillations.