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. 2014 Jul 10;10(7):e1003722.
doi: 10.1371/journal.pcbi.1003722. eCollection 2014 Jul.

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

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Free PMC article

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

Federico Pedraja et al. PLoS Comput Biol. .
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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.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Voltages, dipoles and poles for G. omarorum.
(A) Recorded potential differences through the air gaps. (B) Rostral poles of the dipoles calculated from the recorded potentials, fish resistivity and fish morphology. The diagram between A and B represents the fish in the multiple air gap. Red dots represent the position of the poles in the model. (C) Poles calculated from the dipoles as a function of time. The red and green dotted vertical lines represent the positive peak of the htEOD and the negative peak respectively.
Figure 2
Figure 2. Head to tail EOD waveforms and electric potential in a horizontal plane.
(A) The experimental htEOD recording across the species (B). The htEOD recording calculated using the BEM model. Dotted line indicates zero voltage. (C) G. obscurus: three instants before the positive peak, the positive peak, an instant between the positive peak and the negative peak, the negative peak and one instant later. A. albifrons at the peak of the negative wave of the htEOD, two instants close to the zero crossing between the negative and positive peaks, at the peak of the positive wave, two instants close to the zero crossing between the positive and negative peaks and again at the peak of the negative wave. Black lines indicate the points where the potential is zero. The insets show the htEOD waveform at the selected instants (red dots).
Figure 3
Figure 3. Electric potentials and fields perpendicular to the fish skin on a horizontal plane.
(A) G. petersii (B) G. obscurus (C) G. coropinae (D) G. omarorum (E) A. albifrons. The top row shows the htEOD waveforms recorded in air as a reference. The second row shows the potential along a horizontal line on the skin as a colormap: x axis represents time along the EOD and y axis represents the position on the skin. Reversal points in black. The third row shows the transcutaneous currents using a similar representation. (F) schematic representation of the localization of the skin section in a lateral view (left) and seen from above (right). We have used the body profiles of G. omarorum but these are similar in the other fish.
Figure 4
Figure 4. Comparison of maximum fields along the EOD.
The color maps represent the maximum absolute value of the field at each point of space computed for the whole time course of the EOD. Purple lines show the experimentally obtained thresholds for active electrolocation for G. omarorum (continuous line); G. petersii (dotted line); and A. albifrons (dashed line). For the sake of comparison, in every fish we plot (continuous lines) the threshold values of active (in sky-blue) and passive (in black) electroreception, corresponding to those experimentally determined for G. omarorum (values taken from [46], [47], [48], [49], [51]).
Figure 5
Figure 5. Time course of the image when the object is placed before the fovea and at the side of the body.
(A) Diagram of the scene. The red dots marked as b and c correspond to the places where the traces shown in B and C were calculated. (B) Time courses at the fovea. Left column: Time courses of transcutaneous currents in the absence (red), and in the presence (blue) of an object facing the fovea. Right column: The image calculated as the difference between the traces on the left (black). (C) Time courses for transcutaneous currents with and without an object situated laterally. (D) Diagram of the scene. The red dots marked as e and f correspond to the places where the traces shown in E and F were calculated. (E) Time courses at the fovea. Left column: Time courses of transcutaneous currents in the absence (red), and in the presence (blue) of an object facing the side. Right column: The image calculated as the difference between the traces on the left (black). (F) Time courses on the side, color-coded as above.
Figure 6
Figure 6. Image profiles for spheres of different size facing the fovea.
Amplitude image profiles for G. obscurus, G. coropinae and A. albifrons when (A) a small (0.25 cm radius) and (B) a large sphere (1 cm radius) face the fovea at when the distance between the skin and the surface of the sphere is 1 cm) and (C) when the small sphere faces the fovea at a shorter distance (0.5 cm). The plot shows the profile for the entire EOD normalized by the absolute maximum of each peak. The yellow area indicates the projection of the object on the skin. Note the different shapes for G. coropinae. (D) Schematic representation of the localization of the skin section in a lateral view (left) and seen from above (right), for G. obscurus. See Figure S3 for the complete image.
Figure 7
Figure 7. Images of a sphere facing the middle portion of the fish body.
(A) The diagram shows the relative position of the sphere when the distance to the longitudinal axis is 2 cm. (B) Each row shows the image profiles of a sphere situated at 2 cm from the sagittal plane for the studied species. (C) Image profile with the sphere at 6 cm. The plots show the profiles at the peaks of the htEOD waves: positive peak (green) and negative peak (blue). Also shown are the rostral positive peak (red) for G. coropinae and the first negative peak (red) for G. omarorum,. Insets show the superposition of normalized profiles (divided by the maximum absolute value along the EOD). The triangles and squares indicate the fovea and the tail tip respectively; the yellow area indicates the object projection on the skin.

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Grant support

This work was partially supported by grants from the 7th Frame Program of the European Union (to RB and AAC) as a part of ANGELS project (http://www.theangelsproject.eu), CSIC (Universidad de la Republica Oriental del Uruguay, to Ruben Budelli) and PEDECIBA (to Federico Pedraja, as a part of his master studies). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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