Spike-frequency adaptation separates transient communication signals from background oscillations

Jan Benda, André Longtin & Len Maler

Journal of Neuroscience 25(9), 2312-2321 (2005)

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Abstract

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 where 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 to 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 model's parameters 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.
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