Electric Imaging through Evolution, a Modeling Study of Commonalities and Differences

Abstract

Modeling the electric field and images in electric fish contributes to a better understanding of the pre-receptor conditioning of electric images. Although the boundary element method has been very successful for calculating images and fields, complex electric organ discharges pose a challenge for active electroreception modeling. We have previously developed a direct method for calculating electric images which takes into account the structure and physiology of the electric organ as well as the geometry and resistivity of fish tissues. The present article reports a general application of our simulator for studying electric images in electric fish with heterogeneous, extended electric organs. We studied three species of Gymnotiformes, including both wave-type (Apteronotus albifrons) and pulse-type (Gymnotus obscurus and Gymnotus coropinae) fish, with electric organs of different complexity. The results are compared with the African (Gnathonemus petersii) and American (Gymnotus omarorum) electric fish studied previously. We address the following issues: 1) how to calculate equivalent source distributions based on experimental measurements, 2) how the complexity of the electric organ discharge determines the features of the electric field and 3) how the basal field determines the characteristics of electric images. Our findings allow us to generalize the hypothesis (previously posed for G. omarorum) in which the perioral region and the rest of the body play different sensory roles. While the “electrosensory fovea” appears suitable for exploring objects in detail, the rest of the body is likened to a “peripheral retina” for detecting the presence and movement of surrounding objects. We discuss the commonalities and differences between species. Compared to African species, American electric fish show a weaker field. This feature, derived from the complexity of distributed electric organs, may endow Gymnotiformes with the ability to emit site-specific signals to be detected in the short range by a conspecific and the possibility to evolve predator avoidance strategies.

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

“…This response function results from a pre-receptor Laplacian filter, which was theoretically and experimentally described in previous papers (Budelli and Caputi, 2000;Caputi et al, 1998bCaputi et al, , 2002Gómez et al, 2004;Caputi et al, 2011;Sanguinetti-Scheck et al, 2011;Pedraja et al, 2014). In pulse markers, the latency reached a minimum at the center of the receptive field and increased in the periphery.…”

“…The site-specific waveform is due to the different weight of the different waveforms emitted by the different regions of the electric organ (Caputi et al, 1989(Caputi et al, , 1994(Caputi et al, , 1998aRodríguez-Cattáneo et al, 2008, 2013Castelló et al, 2009;Sanguinetti-Scheck et al, 2011;Pedraja et al, 2014;Waddell et al, 2016). Therefore, the presence of a large object on the side of the fish acts differently on the different EOD components generated by different regions of the fish's body.…”

“…These differences in responsiveness are important as the electric field generated by pulse gymnotiforms is the weighted sum of multiple electrocytes discharging sequentially along the length of the body, each having a different timing, waveform and amplitude (Caputi et al, 1989(Caputi et al, , 1994(Caputi et al, , 1998aRodríguez-Cattáneo et al, 2008, 2013. Spatiotemporal heterogeneity in electrocyte discharges results in regionally specific local fields 'illuminating' the objects in the surrounding water Aguilera et al, 2001;Castelló et al, 2009;Pedraja et al, 2014). As a consequence, at all points of the skin with the exception of the foveal region, i.e.…”

Cross-modal object recognition and dynamic weighting of sensory inputs in a fish

“…At longer object distances, the reliability of the electric sense decreases rapidly due to its small working range (22,46). Consequently, the dominance of the electric sense over vision decreases, and the conflict between vision and the electric sense is solved in favor of the visual information (Fig.…”

Sensory Flow as a Basis for a Novel Distance Cue in Freely Behaving Electric Fish

“…The former reveals specific features that cannot be sensed if an animal behaves differently, and the latter matches input properties to the sensitivity of the neuronal substrate. This motor aspect of sensing is crucial for the flexibility and adaptability of sensing (Schnitzler, 1973;Metzner et al, 2002;Towal and Hartmann, 2006;Diamond et al, 2008;Schroeder et al, 2010;Wachowiak, 2011;Braun et al, 2012;Arkley et al, 2014), and is often performed by highly specialized patterns of movement (i.e., "active sensing strategies") (Hofmann et al, 2013b;Anderson and Perona, 2014) that can be interpreted as an externalization of the brain's integrative functions. Here we investigate the spatiotemporal dynamics of behaviorally generated sensory input and how this sensorimotor interaction allows for the extraction of behaviorally relevant information in the weakly electric fish Gnathonemus petersii.…”