Jamming avoidance behavior in Gymnotoid electric fish with pulse-type discharges: Sensory encoding for a temporal pattern discrimination

Summary

The jamming avoidance response (JAR) is an increase or decrease in an electric fish's frequency of electric organ discharges (EODs), in order to avoid “jamming” of its electrolocation sense by another fish at a slightly lower or higher frequency. This study is concerned with the pulse speciesHypopomus occidentalis andGymnotus carapo, which fire their electric organs in brief pulses separated by intervals of silence.

The JAR can be obtained in curarized preparations in which a train of EOD-mimic (S ₁) pulses is scanned by a train of jamming pulses (S ₂) mimicking a “foreign” fish at a slightly lower frequency (“left-right scan”) or a higher frequency (“right-left scan”); see Fig. 1. Thus the behavior is a function of a single temporal waveform, providing an experimentally convenient preparation in which to study a temporal pattern discrimination problem.

Neurophysiological studies of the sensory encoding of JAR-eliciting stimuli show that burst duration coders (BDCs, Fig. 2), but not pulse markers (Fig. 3) or ampullary cells (Fig. 5), provide information related to normal scanning stimuli. BDCs fire a burst of spikes, phase-locked to the largeS ₁ pulse; the burst is modulated by theS ₂ scanning stimuli. These cells respond differentially to the EOD-mimic signal and the other fish's signals on the basis of amplitude.

BDC responses to left-right and right-left scans are approximate mirror images (Fig. 2). This and other observations indicate that BDC activity reflects primarily the most recentS ₁+S ₂ waveform.

The behavioral discrimination of left-right vs. right-left scans is invariant with respect to an inversion of the “foreign” fish's signal, yet this procedure reverses the responses of BDCs (Fig. 7). Consequently the sequence of excitation and inhibition from any one receptor is ambiguous.

BDCs can be classified into four categories, based on the range ofS ₁/S ₂ latencies at which they respond and by their current direction sensitivity (Fig. 8):α-cells have lowest thresholds to negative (inward) current,β-cells to positive (outward) current, and theγ andδ types to both (Fig. 10). The categories are not sharp (i.e., intermediate types exist). The types are scattered along the length of the fish (Fig. 11).

One proposal is that the central nervous system compares the relative timing of responses from the different classes of BDCs, in order to discriminate left-right vs. right-left scans. An alternative idea is that the JAR is controlled by the sequence of “gentle” vs. “strong” perturbations of overall electroreceptive feedback.