Plasticity of feedback inputs in the apteronotid electrosensory system

Abstract

Weakly electric fish generate an electric field surrounding their body by means of an electric organ typically located within the trunk and tail. Electroreceptors scattered over the surface of the body encode the amplitude and timing of the electric organ discharge (EOD), and central components of the electrosensory system analyze the information provided by the electroreceptor afferents. The electrosensory system is used for electrolocation, for the detection and analysis of objects near the fish which distort the EOD and for electrocommunication. Since the electric organ is typically located in the tail, any movement of this structure relative to the rest of the body alters the EOD field, resulting in large changes in receptor afferent activity. The amplitude of these reafferent stimuli can exceed the amplitudes of near-threshold electrolocation signals by several orders of magnitude. This review summarizes recent studies of the South American weakly electric fish Apteronotus leptorhynchus aimed at determining how the animals differentiate self-generated or reafferent electrosensory stimuli from those that are more behaviorally relevant. Cells within the earliest stages of central electrosensory processing utilize an adaptive filtering technique which allows the system preferentially to attenuate reafferent as well as other predictable patterns of sensory input without degrading responses to more novel stimuli. Synaptic plasticity within the system underlies the adaptive component of the filter and enables the system to learn to reject new stimulus patterns if these become predictable. A Ca2+-mediated form of postsynaptic depression contributes to this synaptic plasticity. The filter mechanism seen in A. leptorhynchus is surprisingly similar to adaptive filters described previously in mormyrid weakly electric fish and in elasmobranchs, suggesting that this mechanism may be a common feature of sensory processing systems.