Summary
Sensory systems evolve for processing complex natural scenes [1] in order to generate successful behavior. Consequently, natural-like stimuli have been crucial for recent advances in understanding the design and function of neural circuits in sensory systems (e.g., visual: [2, 3], auditory: [4, 5, 6]). Communication signals are by definition an important class of natural stimuli. Acoustic communication signals have been reported to evoke responses in peripheral auditory neurons that are highly informative about these stimuli [7, 8]. However, other stimulus ensembles that do not optimally drive sensory neurons can also be behaviorally relevant and equally important for understanding the functioning of neural systems. Unfortunately, they are often neglected [9]. By tracking electrocommunication behavior of weakly electric fish in their Neotropical habitat, we found frequent courtship and aggressive interactions that non-optimally drive sensory neurons just above their threshold. Nevertheless, these weak signals elicited reliable behavioral responses, such as echo-responses to communication signals (so called ″chirps″), synchronization of spawning by a tightly coordinated chirp interaction between male and female fish, and long-range attacks on intruding males. Surprisingly, abundant electrosensory signaling during courtship behaviors occur at the limits of the electroreceptors′ frequency tuning. Electrosensory stimuli during male-male interactions match receptor tuning much better, but many attacks are triggered at large inter-male distances when stimuli are exceedingly weak. Our findings demonstrate that the statistics of species-specific natural stimuli measured in the natural habitat might reveal unexpected behaviorally relevant scenes that are successfully processed by the neural system despite non-optimal activation of sensory neurons.