Sensory systems evolve in the ecological niches that each species is occupying. Accordingly, encoding of natural stimuli by sensory neurons is expected to be adapted to the statistics of these stimuli. For a direct quantification of sensory scenes, we tracked natural communication behavior of male and female weakly electric fish, , in their Neotropical rainforest habitat with high spatiotemporal resolution over several days. In the context of courtship, we observed large quantities of electrocommunication signals. Echo responses, acknowledgment signals, and their synchronizing role in spawning demonstrated the behavioral relevance of these signals. In both courtship and aggressive contexts, we observed robust behavioral responses in stimulus regimes that have so far been neglected in electrophysiological studies of this well characterized sensory system and that are well beyond the range of known best frequency and amplitude tuning of the electroreceptor afferents' firing rate modulation. Our results emphasize the importance of quantifying sensory scenes derived from freely behaving animals in their natural habitats for understanding the function and evolution of neural systems. The processing mechanisms of sensory systems have evolved in the context of the natural lives of organisms. To understand the functioning of sensory systems therefore requires probing them in the stimulus regimes in which they evolved. We took advantage of the continuously generated electric fields of weakly electric fish to explore electrosensory stimulus statistics in their natural Neotropical habitat. Unexpectedly, many of the electrocommunication signals recorded during courtship, spawning, and aggression had much smaller amplitudes or higher frequencies than stimuli used so far in neurophysiological characterizations of the electrosensory system. Our results demonstrate that quantifying sensory scenes derived from freely behaving animals in their natural habitats is essential to avoid biases in the choice of stimuli used to probe brain function.

Understanding how distributed neuronal circuits integrate sensory information and generate behavior is a central goal of neuroscience. Yet, studying neuronal networks at single-cell resolution across the entire adult brain has been difficult in vertebrates due to their size and opacity. We address this challenge by introducing the fish Danionella translucida as a model organism to neuroscience. This teleost remains small and transparent even in adulthood, when neural circuits and behavior have matured. Despite its small brain, Danionella displays a rich set of complex behaviors, including courtship, shoaling, schooling and acoustic communication. To enable optical activity measurements and perturbations with genetically encoded tools, we established CRISPR/Cas9 genome editing and Tol2 transgenesis techniques. These features make Danionella translucida a promising model organism for the study of adult vertebrate brain function at single-cell resolution.

Field studies on freely behaving animals commonly require tagging and often are focused on single species. Weakly electric fish generate a species-and individual-specific electric organ discharge (EOD) and therefore provide a unique opportunity for individual tracking without tagging. Here, we present and test tracking algorithms based on recordings with submerged electrode arrays. Harmonic structures extracted from power spectra provide fish identity. Localization of fish based on weighted averages of their EOD amplitudes is found to be more robust than fitting a dipole model. We apply these techniques to monitor a community of three species, Apteronotus rostratus, Eigenmannia humboldtii and Sternopygus dariensis, in their natural habitat in Darień, Panama. We found consistent upstream movements after sunset followed by downstream movements in the second half of the night. Extrapolations of these movements and estimates of fish density obtained from additional transect data suggest that some fish cover at least several hundreds of meters of the stream per night. Most fish, including E. humboldtii, were traversing the electrode array solitarily. From in situ measurements of the decay of the EOD amplitude with distance of individual animals, we estimated that fish can detect conspecifics at distances of up to 2 m. Our recordings also emphasize the complexity of natural electrosensory scenes resulting from the interactions of the EODs of different species. Electrode arrays thus provide an unprecedented window into the so-far hidden nocturnal activities of multispecies communities of weakly electric fish at an unmatched level of detail.

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