Signal Diversification Is Associated with Corollary Discharge Evolution in Weakly Electric Fish

Abstract

Communication signal diversification is a driving force in the evolution of sensory and motor systems. However, little is known about the evolution of sensorimotor integration. Mormyrid fishes generate stereotyped electric pulses (electric organ discharge [EOD]) for communication and active sensing. The EOD has diversified extensively, especially in duration, which varies across species from 0.1 to >10 ms. In the electrosensory hindbrain, a corollary discharge that signals the timing of EOD production provides brief, precisely timed inhibition that effectively blocks responses to self-generated EODs. However, corollary discharge inhibition has only been studied in a few species, all with short-duration EODs. Here, we asked how corollary discharge inhibition has coevolved with the diversification of EOD duration. We addressed this question by comparing 7 mormyrid species (both sexes) having varied EOD duration. For each individual fish, we measured EOD duration and then measured corollary discharge inhibition by recording evoked potentials from midbrain electrosensory nuclei. We found that delays in corollary discharge inhibition onset were strongly correlated with EOD duration as well as delay to the first peak of the EOD. In addition, we showed that electrosensory receptors respond to self-generated EODs with spikes occurring in a narrow time window immediately following the first peak of the EOD. Direct comparison of time courses between the EOD and corollary discharge inhibition revealed that the inhibition overlaps the first peak of the EOD. Our results suggest that internal delays have shifted the timing of corollary discharge inhibition to optimally block responses to self-generated signals.

SIGNIFICANCE STATEMENT Corollary discharges are internal copies of motor commands that are essential for brain function. For example, corollary discharge allows an animal to distinguish self-generated from external stimuli. Despite widespread diversity in behavior and its motor control, we know little about the evolution of corollary discharges. Mormyrid fishes generate stereotyped electric pulses used for communication and active sensing. In the electrosensory pathway that processes communication signals, a corollary discharge inhibits sensory responses to self-generated signals. We found that fish with long-duration pulses have delayed corollary discharge inhibition, and that this time-shifted corollary discharge optimally blocks electrosensory responses to the fish's own signal. Our study provides the first evidence for evolutionary change in sensorimotor integration related to diversification of communication signals.