Fish Geometry and Electric Organ Discharge Determine Functional Organization of the Electrosensory Epithelium

Abstract

Active electroreception in Gymnotus omarorum is a sensory modality that perceives the changes that nearby objects cause in a self generated electric field. The field is emitted as repetitive stereotyped pulses that stimulate skin electroreceptors. Differently from mormyriformes electric fish, gymnotiformes have an electric organ distributed along a large portion of the body, which fires sequentially. As a consequence shape and amplitude of both, the electric field generated and the image of objects, change during the electric pulse. To study how G. omarorum constructs a perceptual representation, we developed a computational model that allows the determination of the self-generated field and the electric image. We verify and use the model as a tool to explore image formation in diverse experimental circumstances. We show how the electric images of objects change in shape as a function of time and position, relative to the fish's body. We propose a theoretical framework about the organization of the different perceptive tasks made by electroreception: 1) At the head region, where the electrosensory mosaic presents an electric fovea, the field polarizing nearby objects is coherent and collimated. This favors the high resolution sampling of images of small objects and perception of electric color. Besides, the high sensitivity of the fovea allows the detection and tracking of large faraway objects in rostral regions. 2) In the trunk and tail region a multiplicity of sources illuminate different regions of the object, allowing the characterization of the shape and position of a large object. In this region, electroreceptors are of a unique type and capacitive detection should be based in the pattern of the afferents response. 3) Far from the fish, active electroreception is not possible but the collimated field is suitable to be used for electrocommunication and detection of large objects at the sides and caudally.

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.…”

Long-term Behavioral Tracking of Freely Swimming Weakly Electric Fish

“…For greater accuracy, the refractive effect introduced by the water and the oblique camera angle would have to be corrected by calibrating images in three dimensions. Our visual tracking method could be applied to study the electric image flow on fish's body surface 42,43 when fish swims nearby an object. As studied by Hofmann et al 26 , it would be interesting to investigate the object's electric image flow during free-swimming depending on the object distance, shape, size, and material.…”

Sensory flow shaped by active sensing: sensorimotor strategies in electric fish

“…This means that even the simple metrics suitable to determine the distance to a single object differ depending on the body region [e.g. head region versus trunk region (Hofmann et al, 2013;Migliaro et al, 2005;Sanguinetti-Scheck et al, 2011)]. Even worse, if two or more objects are close to one another, the EIs interfere and can lead to non-linear summations (Budelli et al, 2002;Caputi and Budelli, 2006;Migliaro et al, 2005).…”