Coding Conspecific Identity and Motion in the Electric Sense

Abstract

Interactions among animals can result in complex sensory signals containing a variety of socially relevant information, including the number, identity, and relative motion of conspecifics. How the spatiotemporal properties of such evolving naturalistic signals are encoded is a key question in sensory neuroscience. Here, we present results from experiments and modeling that address this issue in the context of the electric sense, which combines the spatial aspects of vision and touch, with the temporal aspects of audition. Wave-type electric fish, such as the brown ghost knifefish, Apteronotus leptorhynchus, used in this study, are uniquely identified by the frequency of their electric organ discharge (EOD). Multiple beat frequencies arise from the superposition of the EODs of each fish. We record the natural electrical signals near the skin of a “receiving” fish that are produced by stationary and freely swimming conspecifics. Using spectral analysis, we find that the primary beats, and the secondary beats between them (“beats of beats”), can be greatly influenced by fish swimming; the resulting motion produces low-frequency envelopes that broaden all the beat peaks and reshape the “noise floor”. We assess the consequences of this motion on sensory coding using a model electroreceptor. We show that the primary and secondary beats are encoded in the afferent spike train, but that motion acts to degrade this encoding. We also simulate the response of a realistic population of receptors, and find that it can encode the motion envelope well, primarily due to the receptors with lower firing rates. We discuss the implications of our results for the identification of conspecifics through specific beat frequencies and its possible hindrance by active swimming.

Author Summary

Effectively processing information from a sensory scene is essential for animal survival. Motion in a sensory scene complicates this task by dynamically modifying signal properties. To address this general issue, we focus on weakly electric fish. Each fish produces a weak electrical carrier signal with a characteristic frequency. Electroreceptors on its skin encode the modulations of this carrier caused by nearby objects and other animals, enabling this fish to thrive in its nocturnal environment. Little is known about how swimming movements influence natural electrosensory scenes, specifically in the context of detection and identification of, and communication with conspecifics. Using recordings involving free-swimming fish, we characterize the amplitude modulations of the carrier signal arising from small groups of fish. The differences between individual frequencies (beats) are prominent features of these signals, with the number of beats reflecting the number of neighbours. We also find that the distance and motion of a free-swimming fish are represented in a slow modulation of the beat at the receiving fish. Modeling shows that these stimulus features can be effectively encoded in the activity of the electroreceptors, but that encoding quality of some features can be degraded by motion, suggesting that active swimming could hinder conspecific identification.