Waveform diversity of electric organ discharges: the role of electric organ auto-excitability inGymnotusspp.

Abstract

SUMMARYThis article shows that differences in the waveforms of the electric organ discharges (EODs) from two taxa are due to the different responsiveness of their electric organs (EOs) to their previous activity (auto-excitability). We compared Gymnotus omarorum endemic to Uruguay (35°South, near a big estuary), which has four components in the head to tail electric field (V 1 to V 4 ), with Gymnotus sp. endemic to the south of Brazil, Paraguay and Argentinean Mesopotamia (25°South, inland), which shows a fifth component in addition to the others (V 5 ). We found that: (a) the innervation pattern of the electrocytes, (b) the three earlier, neurally driven, EOD components (V 1 to V 3 ), and (c) their remnants after curarisation were almost identical in the two taxa. The equivalent electromotive forces of late components (V 4 and V 5 ) increased consistently as a function of the external current associated with the preceding component and were abolished by partial curarisation in both taxa. Taken together these data suggest that these components are originated in the responses of the electrocytes to longitudinal currents through the EO. By using a differential load procedure we showed that V 4 in G. omarorum responded to experimental changes in its excitation current with larger amplitude variations than V 4 in Gymnotus sp. We conclude that the differences in the EOD phenotype of the two studied taxa are due to the different EO auto-excitability. This, in turn, is caused either by the different expression of a genetic repertoire of conductance in the electrocyte membrane or in the wall of the tubes forming the EO.

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

“…(1) At the head and abdominal region of G. javari we found a complex EOD, suggesting the presence of an expansion of the EO behind the cleithrum-opercular aponeuroses, as previously described in G. coropinae (Castelló et al, 2009). (2) In G. obscurus, we noted what we will henceforth describe as a 'facultative monophasic EOD', with a dominant positive component followed by a much lower-amplitude negative component, the amplitude of which is strongly dependent on the external load (Bell et al, 1976;Caputi et al, 1998;Rodríguez-Cattáneo and Caputi, 2009). To accommodate these novel features, three specimens of G. javari were explored with smaller size gaps (1cm, starting from the snout) and one specimen using near-field recordings with the fish in water (see Near-field analysis, below).…”

“…The tail region of the biphasic G. obscurus specimen was further explored using a variation of the simple air gap method (Bell et al, 1976;Rodríguez-Cattáneo and Caputi, 2009). We split the load into two parallel 'one-way' paths of opposite direction using germanium diodes.…”

“…By changing the value of such resistance (R o ) we constructed a separate characteristic curve for the peak of each of the phases of alternating polarity in the EOD (its characteristic curve) (Caputi et al, 1989;Rodríguez-Cattáneo and Caputi, 2009). …”

“…Second, in traces where a negative peak preceded V 3 , we identified the presence of rostrally innervated electrocytes to define this peak as V 2 . Taking into account the curarization experiment [reported elsewhere (Caputi et al, 1989;Caputi and Aguilera, 1996;Rodríguez-Cattáneo and Caputi, 2009)] in which the activity following V 3 was shown to be the consequence of electrocyte responsiveness, we defined the first negativity after V 3 as V 4 , and the first positivity after V 3 as V 5 . In the case of V 1 , we found two slow waves: one originated at the head (V 1r ) and another (positive) originated at the limit between the central and caudal region of the body.…”

“…The influence of these six kinds of variation on EOD waveform has been well documented by a long series of studies involving cellular and integrative analysis of the EOD in the model species Gymnotus omarorum (Trujillo-Cenóz et al, 1984;Lorenzo et al, 1988;Lorenzo et al, 1990;Lorenzo et al, 1993; Trujillo-Cenóz and Echagüe, 1989; Macadar et al, 1989;Caputi and Trujillo-Cenóz, 1994;Caputi and Budelli, 1995;Sierra et al, 1995;Sierra et al, 2005;Caputi et al, 1989;Caputi et al, 1993;Caputi and Aguilera, 1996;Castelló et al, 2000;Aguilera et al, 2001;Rodríguez-Cattáneo and Caputi, 2009). Comparative studies of other species have allowed us to describe an additional type of EO organization that influences the EOD field and its waveform.…”