Neuronal circuitry for comparison of timing in the electrosensory lateral line lobe of the African wave-type electric fish Gymnarchus niloticus

Abstract

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.

Temporal Coding of Concurrent Acoustic Signals in Auditory Midbrain

“…2 A, B, NC). The locations of central recording sites were verified after iontophoretic injection of neurobiotin (Vector Laboratories, Inc., Burlingame, CA; 5% in 3 M KC l, ϩ3 A, 10 min) and survival times of ϳ15 min -15 hr (after Bass et al, 1996;Kawasaki and Guo, 1996); the procedures used for fixation and visualization of a dense reaction product (Fig. 2C) have been described elsewhere .…”

Representation of Accurate Temporal Information in the Electrosensory System of the African Electric Fish,Gymnarchus niloticus

“…This layer was localized by recording field potentials in the ELL that show systematic change of waveform along the depth (see Fig. 2 in Kawasaki and Guo, 1996) with a glass-capillary electrode (5-10 m tip diameter, 3 M NaCl). No anatomical confirmation was made to distinguish recordings from the terminals of the S-type afferent fibers and giant neurons.…”

“…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).…”

“…Although such behavioral experiments clearly demonstrate the ability of the CNS to deal with temporal codes of microseconds or even submicroseconds, the physiological mechanisms underlying this capability are not fully understood. Kawasaki and Guo (1996) recently discovered that neurons in an early stage of central processing of electrosensory information in an African electric fish, Gymnarchus niloticus, exhibit a sensitivity to time disparities between electrosensory inputs on the order of microseconds.…”

“…Because the S-type afferent fibers and giant cells, collectively referred to as phaselocked neurons (PLNs) in this study, fire one action potential for each zerocrossing of the electrosensory signal with a certain latency, times of zerocrossing of signals at different electroreceptors are represented at the ICL as the times of the action potentials of PLNs. Kawasaki and Guo (1996) describe physiological and morphological characteristics of these PLNs that give input to differential-phase-sensitive neurons that are sensitive to time disparities on the order of single-digit microseconds (Fig. 1).…”