From stimulus estimation to combination sensitivity: encoding and processing of amplitude and timing information in parallel, convergent sensory pathways

Information theoretical approaches to sensory processing in electric fish have focused on the encoding of amplitude modulations in a single sensory pathway in the South American gymnotiforms. To assess the generality of these studies, we investigated the encoding of amplitude and phase modulations in the distantly related African fish Gymnarchus. In both the amplitude- and time-coding pathways, primary afferents accurately estimated the time course of random modulations whereas hindbrain neurons extracted information about specific stimulus features. Despite exhibiting a clear preference for encoding amplitude or phase, afferents and hindbrain neurons could encode significant amounts of modulation of their nonpreferred attribute. Although no increase in feature extraction performance occurred where the two pathways converge in the midbrain, neurons there were increasingly sensitive to simultaneous modulation of both attributes. A shift from accurate stimulus estimation in the periphery to increasingly sparse representations of specific features appears to be a general strategy in electrosensory processing.