Microsecond and millisecond time processing in weakly electric fishes

Abstract

Weakly electric fishes possess two distinctive electrosensory systems that are specialized to detect amplitude and time (phase) information. The amplitude sensitive system detects electric feedback signals from the fish’s own electric organ discharges that are altered by the resistive component of nearby objects. The time (phase) sensitive system, on the other hand, detects signal times that are altered by the capacitive component of the objects. These subcomponents of the electrosensory system are fundamental to the fish’s ability to obtain the electric image of its immediate surroundings. The jamming avoidance response is a behavior in which the fish alter the frequency of their electric organ discharges to avoid mutual jamming of the electrolocation behavior. The information necessary to perform correct jamming avoidance responses is encoded in the time pattern of amplitude and time signals that occurs in the millisecond time scale. The time signal is encoded in the difference in phases between signals at different locations on the body surface. This differential phase sensitive system operates on the microsecond time scale. Our behavioral experiments demonstrated that even submicrosecond phase differences could be detected by the electrosensory system and manifested in the jamming avoidance responses. Neurons of the central nervous system that are specialized to process amplitude and differential phase information were found in the electrosensory lateral line lobe. In the midbrain, neurons are sensitive to specific time patterns of activities of the amplitude and differential phase sensitive neurons projecting from the lower station. These midbrain neurons examine time pattern of synaptic potentials and exhibit responses necessary for the jamming avoidance response. The electrosensory system of electric fishes is one of the best-understood systems for temporal coding of sensory information.