How do oscillations in sensory receptors encode communication signals? During my PhD research with Bruce Carlson, I studied neural coding mechanisms in African mormyrid weakly electric fish. These fish generate very small amounts of electricity to communicate and to sense their environment. The sensory receptors responsible for detecting communication signals fire spikes in the majority of mormyrid species. How spiking receptors encode information and how this information is processed centrally is fairly well understood. However, some species have sensory receptors that produce spontaneously oscillating potentials. How these receptors encoded communication signals was entirely unknown. Using in vivo extracellular recordings, we showed that these receptors use transient synchrony across the population to encode signals sent by a nearby fish. Both receptor sensitivity and behavioral sensitivity suggest that, whereas spiking receptors are specialized for detecting communication signals from individual fish, oscillating receptors may be specialized for detecting signals arising from a large group of fish. We hypothesize that the physiology of oscillating receptors may facilitate detecting and finding a group of conspecifics in fish's native lakes and rivers.
How do central circuits establish single-neuron sensitivity to timing patterns in presynaptic inputs? The communication signals of a wide range of animals, including insects, fish, and frogs, consist of a series of sound or light pulses with species-specific timing patterns. Furthermore, the timing patterns of spikes also carry information in many central circuits. Therefore, how circuits establish single-neuron sensitivity to these patterns is a question of broad relevance. Mormyrid fish use distinct patterns of time intervals between successive electric pulses to communicate different behavioral states. The sensory pathway that detects communication signals faithfully preserves these time intervals until information reaches a midbrain nucleus, which makes mormryids ideal for studying temporal pattern sensitivity. Using in vivo whole-cell patch recordings, we showed that complex interactions between excitation and inhibition establish a population of midbrain neurons with a wide range of selectivity for particular timing patterns. We also demonstrated that using a combination of mechanisms to generate temporal selectivity results in a greater diversity of response properties than using one mechanism. We hypothesize that a population of neurons with widely varying selectivities enables enhanced detection and discrimination of behaviorally relevant timing patterns.
How does a population of interval-selective neurons encode behaviorally relevant temporal variation in communication signals? Although single neurons selective for particular time intervals have been described in many sensory circuits, how a population of interval-selective neurons encodes behaviorally relevant variation in timing patterns was unknown. Using behavioral playback assays and in vivo whole-cell electrophysiology, we found that fish's behavioral sensitivity to slight changes in the temporal pattern of a natural, individually stereotyped communication signal is due at least in part to the remarkable sensitivity of individual electrosensory midbrain neurons. The output of these neurons contains enough information to resolve inter-individual differences in natural communication signals, which raises the question of whether fish use this information to recognize the identity of a signaler.