Waveform sensitivity of electroreceptors in the pulse weakly electric fish Gymnotus omarorum

Abstract

As in most sensory systems, electrosensory images in weakly electric fish are encoded in two parallel pathways, fast and slow. From work on wave-type electric fish, these fast and slow pathways are thought to encode the time and amplitude of electrosensory signals, respectively. The present study focuses on the primary afferents giving origin to the slow path of the pulse-type weakly electric fish Gymnotus omarorum. We found that burst duration coders respond with a high-frequency train of spikes to each electric organ discharge. They also show high sensitivity to phase-frequency distortions of the self-generated local electric field. We explored this sensitivity by manipulating the longitudinal impedance of a probe cylinder to modulate the stimulus waveform, while extracellularly recording isolated primary afferents. Resistive loads only affect the amplitude of the re-afferent signals without distorting the waveform. Capacitive loads cause large waveform distortions aside from amplitude changes. Stepping from a resistive to a capacitive load in such a way that the stimulus waveform was distorted, without changing its total energy, caused strong changes in latency, inter-spike interval and number of spikes of primary afferent responses. These burst parameters are well correlated suggesting that they may contribute synergistically in driving downstream neurons. This correlation also suggests that each receptor encodes a single parameter in the stimulus waveform. The finding of waveform distortion sensitivity is relevant because it may contribute to: (a) enhance electroreceptive range in the peripheral 'electrosensory field', (b) a better identification of living prey at the 'foveal electrosensory field' and (c) detect the presence and orientation of conspecifics. Our results also suggest a revision of the classical view of amplitude and time encoding by fast and slow pathways in pulse-type electric fish.

Waveform Sensors: The Next Challenge in Biomimetic Electroreception

“…The output of receptor cells are then rectified by a synaptic-like module similar to an electronic diode and transformed in a burst of discrete events using a leaky integratefire-and-reset circuit. 66 This model is able to reproduce experimental performance of electroreceptors observed experimentally 34,40,41,59 and can be easily implemented electronically.…”

“…In the case of active electroreception, several experimental and theoretical studies in electric fish indicate that the change in waveform caused by the polarization of capacitive objects 14,[32][33][34] and differential changes in the rotational 8,22 of fields differing in time waveforms and originated in different regions of the body may provide clues for discriminating object impedance, shape and location. The change in signal waveform by the presence of capacitive objects results from a transient charge of the objects, while the presence of multiple sources generating different waveforms at different distances from the object as occurs in pulse gymnotiformes might yield position dependent changes in signal waveform.…”

“…38 Tuberous electroreceptors show specific responses tuned to the best frequency in the power spectral density of the self-generated stimulus, 40,41 and also to different time courses even when the power spectral density of the stimulus remains constant. 34,42 Tuning is important for several reasons. First, because it allows increasing the ratio between self and non-self-generated carrier electric fields and among these last fields between conspecifics and other sources.…”

“…Second, changes in the amplitude or phase spectra may inform about the presence of complex impedance introduced by capacitive elements of the object. 34,43 The presence of more than one type of electroreceptor with different tuning opens the possibility to perceive more than one dimension in the electric image as it occurs, for example, in color vision or tone audition (electric color, 14,32,44 ). Third, in nature, receptor tuning to species-specific electric organ discharges allows the fish to detect potential mates.…”

Strategies of object polarization and their role in electrosensory information gathering

“…We used object probes consisting of a nonconductive cylinder with conductive bases [1,3,33,83,[97][98].…”