Electric organ discharge diversity in the genusGymnotus: functional groups and electrogenic mechanisms

Abstract

SUMMARYPrevious studies describe six factors accounting for interspecific diversity of electric organ discharge (EOD) waveforms in Gymnotus. At the cellular level, three factors determine the locally generated waveforms: (1) electrocyte geometry and channel repertoire; (2) the localization of synaptic contacts on electrocyte surfaces; and (3) electric activity of electromotor axons preceding the discharge of electrocytes. At the organismic level, three factors determine the integration of the EOD as a behavioral unit: (4) the distribution of different types of electrocytes and specialized passive tissue forming the electric organ (EO); (5) the neural mechanisms of electrocyte discharge coordination; and (6) post-effector mechanisms. Here, we reconfirm the importance of the first five of these factors based on comparative studies of a wider diversity of Gymnotus than previously investigated. Additionally, we report a hitherto unseen aspect of EOD diversity in Gymnotus. The central region of the EO (which has the largest weight on the conspecific-received field) usually exhibits a negative-positive-negative pattern where the delay between the early negative and positive peaks (determined by neural coordination mechanisms) matches the delay between the positive and late negative peaks (determined by electrocyte responsiveness). Because delays between peaks typically determine the peak power frequency, this matching implies a co-evolution of neural and myogenic coordination mechanisms in determining the spectral specificity of the intraspecific communication channel. Finally, we define four functional species groups based on EO/EOD structure. The first three exhibit a heterogeneous EO in which doubly innervated electrocytes are responsible for a main triphasic complex. Group I species exhibit a characteristic cephalic extension of the EO. Group II species exhibit an early positive component of putative neural origin, and strong EO auto-excitability. Group III species exhibit an early, slow, negative wave of abdominal origin, and variation in EO auto-excitability. Representatives of Group IV generate a unique waveform comprising a main positive peak followed by a small, load-dependent negative component.

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

“…First, in pulse gymnotiforms, the self-generated electric field polarizing the nearby objects in the near environment has a different waveform depending upon object location relative to the body Caputi et al, 1989Caputi et al, , 1994Caputi et al, , 1998aCastelló et al, 2009;Rodríguez-Cattáneo et al, 2008, 2013Stoddard et al, 1999;Waddell et al, 2016). 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).…”

“…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.…”

“…The differences between low pass and wide band were not so clear in subsequent reports (McKibben et al, 1993;Yager and Hopkins, 1993). 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).…”

Waveform Sensors: The Next Challenge in Biomimetic Electroreception

“…Males and females have seasonally modulated electric organ discharges in such a way that the sharp frequency tuning of electroreceptors parallels the changes induced by sexual hormones, 45 Four, pulse gymnotiformes emit pulses resulting from the summated activity of different sources located at different places along the fish's body. [46][47][48] Linearity suggests that whole object polarization is the sum of object polarization by such self-generated components having each a characteristic waveform. This site-dependent polarization linear effect is enhanced by the secondary polarization induced by the polarization fields coming from rest of the scene.…”

Proximate and ultimate causes of signal diversity in the electric fishGymnotus

“…Adapted to live in such a geometrically complex environment, Gymnotus utilize pulsed EODs and an array of cutaneous electroreceptors both to sense the presence of nearby objects Caputi et al, 2003) and to communicate (Black-Cleworth, 1970;Westby, 1974). Gymnotus exhibit considerable diversity of electric organ (EO) structure across their distributional range, and this diversity is translated into the spatiotemporal pattern of the EOD-associated electric field Rodríguez-Cattáneo et al, 2013;Rodríguez-Cattáneo et al, 2008). There is increasing evidence that the conspecific-detected EOD waveform serves as a communication signal, and contains information that may mediate interspecific, and even individual, recognition in Gymnotus (Aguilera et al, 2001;Crampton and Albert, 2006;Crampton et al, 2008;Crampton et al, 2011;McGregor and Westby, 1993).…”