An African wave-type electric fish, Gymnarchus, compares timing on the order of microseconds of sensory feedback from from its high-frequency (approximately 400 Hz) electric organ discharges (EODs) received at different parts of its body surfaces. This capability is essential for and demonstrated by the jamming avoidance response (JAR). The organization of the timing comparison mechanisms was identified in the electrosensory lateral line lobe (ELL) in the hindbrain by field potential, extra- and intracellular recordings, and intracellular labeling with biotinylated agents. Timing of phase of the EOD feedback is carried by action potentials of S-type primary afferent fibers that project to the inner cellular layer (ICL) of the medial zone of the ELL and to the giant neurons in the ELL. The giant neurons bilaterally project to the ICL, where neurons sensitive to phase differences between different parts of the body occur. Although sensitive to dynamic phase changes of several microseconds, these differential-phase-sensitive neurons showed adaptation to steady-state changes of phase difference over a wide range (greater than +/- 100 microseconds) and continued to respond to small modulations after the mean difference was shifted. Gymnarchus and an independently evolved South American electric fish, Eigenmannia, exhibit nearly identical JARs and share a rather complex but identical set of computational algorithms for JAR. This study showed that one of the computational steps, the timing comparison between body surfaces, occurs in the hindbrain in Gymnarchus, in contrast to the midbrain in Eigenmannia. Thus, similar systems with a similar overall function may have evolved differently in different genera by assigning a subfunction to different substructures within the brain.

Two distinct sensory cues in electrosensory signals, amplitude modulation and differential phase modulation, are essential for an African wave-type electric fish, Gymnarchus, to perform the jamming avoidance responses. Individual neurons in the first brain station for central processing, the electrosensory lateral line lobe (ELL), were investigated by the in vivo whole-cell recording and labeling technique for their physiological responses, location, morphology, and projection areas. Neurons in the dorsal zone of the ELL responded selectively to amplitude modulation. Neurons in the outer cell layer of the medial zone were categorized physiologically into two groups: amplitude-sensitive and differential phase-sensitive. All but one neuron in the inner cell layer of the medial zone responded exclusively to differential phase modulation. All neurons recorded and labeled in the ELL had pyramidal morphology with large and extensive apical dendrites and less extensive basal dendrites. They were found to project to two midbrain nuclei: the nucleus praeeminentialis and the torus semicircularis. Amplitude-sensitive neurons in the dorsal zone projected exclusively to the lateral posterior subdivision, the torus semicircularis. Neurons in the medial zone projected to the medial dorsal and lateral anterior subdivisions of the torus semicircularis. Although some neurons in the ELL responded to both amplitude and differential phase modulation, they did not differentiate between temporal patterns of the two cues that encode necessary information for the jamming avoidance response. Overlapping projection of amplitude and differential phase-sensitive neurons to the torus semicircularis suggests integration of the two sensory cues in this nucleus.

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) (Kawasaki and Guo, 1996). 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 phaselocked 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 ϳ6 sec. The PLNs represent zerocrossing times of each stimulus cycle with this accuracy even when stimulus phase was modulated at high frequencies (ϳ50 Hz). Distinct JAR occurred when time disparity was diminished below 1 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 (ϳ60 sec) was introduced to a stimulus that mimicked fish's own EOD and the time disparity for JAR was diminished to 1 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 (Rose and Heiligenberg, 1985b;Carr et al., 1986a). The present study revealed that the independently evolved Eigenmannia and Gymnarchus exhibit a comparative level of remarkable temporal accuracy.

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The sensory cues for a less known form of frequency shifting behavior, gradual frequency falls, of electric organ discharges (EODs) in a pulse-type gymnotiform electric fish, Rhamphichthys rostratus, were identified. We found that the gradual frequency fall occurs independently of more commonly observed momentary phase shifting behavior, and is due to perturbation of sensory feedback of the fish's own EODs by EODs of neighboring fish. The following components were identified as essential features in the signal mixture of the fish's own and the neighbor's EOD pulses: (1) the neighbor's pulses must be placed within a few millisecond of the fish's own pulses, (2) the neighbor's pulses, presented singly at low frequencies (0.2-4 Hz), were sufficient, (3) the frequency of individual pulse presentation must be below 4 Hz, (4) amplitude modulation of the sensory feedback of the fish's own pulses induced by such insertions of the neighbor's pulses must contain a high frequency component: sinusoidal amplitude modulation of the fish's own EOD feedback at these low frequencies does not induce gradual frequency falls. Differential stimulation across body surfaces, which is required for the jamming avoidance response (JAR) of wave-type gymnotiform electric fish, was not necessary for this behavior. We propose a cascade of high-pass and low-pass frequency filters within the amplitude processing pathway in the central nervous system as the mechanism of the gradual frequency fall response.