Representation of accurate temporal information in the electrosensory system of the African electric fish, Gymnarchus niloticus.

Differential-phase-sensitive neurons in the electrosensory lateral line lobe (ELL) of the African electric fish, Gymnarchus niloticus, are sensitive to time disparities on the order of microseconds between afferent action potentials. These action potentials fire in a phase-locked manner in response to the animal's own wave-type electric organ discharges (EODs) (). The time disparity is one of the essential cues for an electrical behavior, the jamming avoidance response (JAR). To gain an insight into the accurate temporal processing in the ELL, firing time accuracy and dynamic response properties of action potentials of the phase-locked neurons (PLNs) in the ELL were examined. The temporal accuracy of the entire neuronal circuit for the JAR was also measured using behavioral responses. Standard deviation of firing times of PLNs' action potentials was approximately 6 micro;sec. The PLNs represent zerocrossing times of each stimulus cycle with this accuracy even when stimulus phase was modulated at high frequencies ( approximately 50 Hz). Distinct JAR occurred when time disparity was diminished below 1 micro;sec, and a marginal JAR could still be detected with a time disparity of 100 nsec. Standard deviation of the firing times of EODs was approximately several hundred nanoseconds. This stability of the EOD, however, was demonstrated to be unnecessary for the JAR. JARs occurred even when a large artificial jitter ( approximately 60 micro;sec) was introduced to a stimulus that mimicked fish's own EOD and the time disparity for JAR was diminished to 1 micro;sec. This immunity of JAR to the EOD jitter is explained by the insensitivity of the differential-phase-sensitive neurons in the ELL to a common phase modulation. The JAR of the South American electric fish, Eigenmannia, also occurs in response to stimuli that generate comparably small phase differences (; ). The present study revealed that the independently evolved Eigenmannia and Gymnarchus exhibit a comparative level of remarkable temporal accuracy.