Encoding phase spectrum for evaluating “electric qualia”

Abstract

The most broadly expressed and studied aspect of sensory transduction is receptor tuning to the power spectral density of the incoming signals. Temporal cues expressed in the phase spectrum are relevant in African and American pulse-emitting electric fish showing electroreceptors sensing the signals carried by the selfand conspecific-generated electric organ discharges. This article concerns the role of electroreceptor phase sensitivity in American pulse Gymnotiformes. These fish show electroreceptors sharply tuned to narrow frequency bands. This led to the common thought that most electrosensory information is contained in the amplitude spectra of the signals. However, behavioral and modeling studies suggest that in their pulses, Gymnotiformes electroreceptors also encode cues embodied in the phase spectrum of natural stimuli. Here, we show that the two main types of tuberous primary afferents of Gymnotus omarorum differentially respond to cues embodied in the amplitude and phase spectra of self-generated electrosensory signals. One afferent type, pulse markers, is mainly driven by the amplitude spectrum, while the other, burst coders, is predominantly sensitive to the phase spectrum. This dual encoding strategy allows the fish to create a sensory manifold where patterns of 'electric color' generated by object impedance and other potential sources of 'colored' images (such as large nearby objects and other electric fish) can be represented.

Waveform discrimination in a pair of pulse‐generating electric fishes

“…These results are congruent with behavioural experiments showing that individuals can discriminate between phase-shifted conspecific waveforms in Hypopomidae (Heiligenberg & Altes, 1978), and electrophysiological observations of electroreceptor sensitivity to phase components of the EOD in G. omarorum (Caputi & Aguilera, 2019). While the advantage of the phase-locked approach is that we avoid interference and jamming avoidance responses, an alternative explanation for these results is that the fish cannot differentiate the echo stimulus from a permanent change in their own EOD, and therefore perceive changes in the echo as a result of a change in the environment, and may elicit true "novelty responses" [as classically shown when an object modifies their own EOD, see Aguilera and Caputi (2003)].…”

“…Because the power spectra of G. omarorum and B. gauderio overlap (Figure a,b), this suggests that phase components are likely more important than spectral components in waveform discrimination. These results are congruent with behavioural experiments showing that individuals can discriminate between phase‐shifted conspecific waveforms in Hypopomidae (Heiligenberg & Altes, ), and electrophysiological observations of electroreceptor sensitivity to phase components of the EOD in G. omarorum (Caputi & Aguilera, ).…”

“…Other experiments suggest the capability to discriminate among sexually dimorphic EODws relies on the presence of electroreceptor types differentiated by their sensitivity to spectral and temporal cues (Hopkins & Westby, 1986;Shumway & Zelick, 1988;Zakon, 1986). The role of temporal (e.g., phase) cues in discrimination was shown by the differential sensitivity of individuals (Heiligenberg & Altes, 1978), electroreceptors (Caputi & Aguilera, 2019) and central nervous system structures (Shumway & Zelick, 1988) to artificially generated EODs possessing the same power spectral density. Wave-type gymnotiforms (e.g., those that produce a constant sinewave-like discharge, contrasting with discrete pulses) have also been shown to discriminate among EODws on the basis of time (Kramer, 1999;Kramer & Otto, 1991) and frequency cues (power spectral properties, see, e.g., Hopkins, 1976;Kramer, 1987;Fugère & Krahe, 2010).…”

Electrocommunication in pulse Gymnotiformes: the role of EOD time course in species identification.

“…Pulse-emitting Gymnotiformes, the focus of this study, possess two main types of electroreceptors, referred to as pulse markers and burst coders (Bastian, 1976(Bastian, , 1977Caputi and Aguilera, 2019;McKibben et al, 1993;Rodríguez-Cattáneo et al, 2017;Watson and Bastian, 1979;Yager and Hopkins, 1993). Both types are innervated by a single primary afferent and respond to active electrolocation and communication signals.…”

“…Pulse markers fire a single latency-modulated spike (Rodríguez-Cattáneo et al, 2017), and exhibit V-shaped tuning with a diversity of best frequencies located at the center of the power spectrum (Watson and Bastian, 1979). When stimulus signals are manipulated, they show better tuning to the amplitude than to the phase spectrum of the stimulus (Caputi and Aguilera, 2019). Burst coders, in contrast, respond to the EOD with a burst of spikes.…”