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Neuronal networks can produce stable oscillations and synchrony that are under tight control yet flexible enough to rapidly switch between dynamical states. The pacemaker nucleus in the weakly electric fish comprises a network of electrically coupled neurons that fire synchronously at high frequency. This activity sets the timing for an oscillating electric organ discharge with the lowest cycle-to-cycle variability of all known biological oscillators. Despite this high temporal precision, pacemaker activity is behaviorally modulated on millisecond time-scales for the generation of electrocommunication signals. The network mechanisms that allow for this combination of stability and flexibility are not well understood. In this study, we use an in vitro pacemaker preparation from Apteronotus leptorhynchus to characterize the neural responses elicited by the synaptic inputs underlying electrocommunication. These responses involve a variable increase in firing frequency and a prominent desynchronization of neurons that recovers within 5 oscillation cycles. Using a previously developed computational model of the pacemaker network, we show that the frequency changes and rapid resynchronization observed experimentally are most easily explained when model neurons are interconnected more densely and with higher coupling strengths than suggested by published data. We suggest that the pacemaker network achieves both stability and flexibility by balancing coupling strength with interconnectivity and that variation in these network features may provide a substrate for species-specific evolution of electrocommunication signals.

A crucial step in forming spatial representations of the environment involves the estimation of relative distance. Active sampling through specific movements is considered essential for optimizing the sensory flow that enables the extraction of distance cues. However, in electric sensing, direct evidence for the generation and exploitation of sensory flow is lacking. Weakly electric fish rely on a self-generated electric field to navigate and capture prey in the dark. This electric sense provides a blurred representation of the environment, making the exquisite sensory abilities of electric fish enigmatic. Stereotyped back-and-forth swimming patterns reminiscent of visual peering movements are suggestive of the active generation of sensory flow, but how motion contributes to the disambiguation of the electrosensory world remains unclear. Here, we show that a dipole-like electric field geometry coupled to motion provides the physical basis for a nonvisual parallax. We then show in a behavioral assay that this cue is used for electrosensory distance perception across phylogenetically distant taxa of weakly electric fish. Notably, these species electrically sample the environment in temporally distinct ways (using discrete pulses or quasisinusoidal waves), suggesting a ubiquitous role for parallax in electric sensing. Our results demonstrate that electrosensory information is extracted from sensory flow and used in a behaviorally relevant context. A better understanding of motion-based electric sensing will provide insight into the sensorimotor coordination required for active sensing in general and may lead to improved electric field-based imaging applications in a variety of contexts.

Tympanal organs are widespread in Nymphalidae butterflies, with a great deal of variability in the morphology of these ears. How this variation reflects differences in hearing physiology is not currently understood. This study provides the first examination of the hearing organs of the crepuscular owl butterfly, Caligo eurilochus. We hypothesize that (1) its hearing may function to detect the high-frequency calls of bats, or (2) like its diurnal relatives it may function to detect avian predators, or (3) it may have lost auditory sensitivity as a result of the lack of selective pressures. To test these hypotheses we examined the tuning and sensitivity of the C. eurilochus Vogel’s organ using laser Doppler vibrometry and extracellular neurophysiology. We show that the C. eurilochus ear responds to sound and is most sensitive to frequencies between 1-4 kHz, as confirmed by both the vibration of the tympanal membrane and the physiological response of the associated nerve branches. In comparison to the hearing of its diurnally active relative, Morpho peleides, C. eurilochus has a narrower frequency range with higher auditory thresholds. We conclude that hearing in this butterfly is partially-regressed, and may reflect a trade-off between hearing and vision for survival in low light conditions.

Butterflies use visual and chemical cues when interacting with their environment, but the role of hearing is poorly understood in these insects. Nymphalidae (brush-footed) butterflies occur worldwide in almost all habitats and continents, and comprise more than 6,000 species. In many species a unique forewing structure--Vogel's organ--is thought to function as an ear. At present, however, there is little experimental evidence to support this hypothesis. We studied the functional organization of Vogel's organ in the common blue morpho butterfly, Morpho peleides, which represents the majority of Nymphalidae in that it is diurnal and does not produce sounds. Our results confirm that Vogel's organ possesses the morphological and physiological characteristics of a typical insect tympanal ear. The tympanum has an oval-shaped outer membrane and a convex inner membrane. Associated with the inner surface of the tympanum are three chordotonal organs, each containing 10-20 scolopidia. Extracellular recordings from the auditory nerve show that Vogel's organ is most sensitive to sounds between 2-4 kHz at median thresholds of 58 dB SPL. Most butterfly species that possess Vogel's organ are diurnal, and mute, so bat detection and conspecific communication can be ruled out as roles for hearing. We hypothesize that Vogel's organs in butterflies such as M. peleides have evolved to detect flight sounds of predatory birds. The evolution and taxonomic distribution of butterfly hearing organs are discussed.