The slow pathway in the electrosensory lobe of Gymnotus omarorum: Field potentials and unitary activity
Introduction
This study focuses on the analysis of the sensory activity in the electrosensory lobe (ELL) of Gymnotus omarorum, a weakly electric fish. These animals use their electric organ discharge (EOD) to probe their nearby environment (Bastian, 1986a, Bell, 1979, Lissmann, 1958, Lissmann, 1951, Lissmann and Machin, 1958) and communicate with conspecifics (Black-Cleworth, 1970, Hopkins, 1981, Kramer, 1990, Moller, 1995).
The active electric sense relies on three parallel mechanisms for generating reafferent signals in sensory nerves: (a) the generation of the sensory carrier (the fish’s own EOD); (b) the active movements of the sensory surface to explore object features; and (c) prereceptor conditioning of reafferent images (Caputi, 2004). In some species the EOD is a brief pulse (“pulse fish”) whereas in other species it is a continuous wave (“wave fish”). Body shape and swimming movements have evolved together in these fish, with some species being carangiform1 and others balistiform2 swimmers (Blake, 1983). These electromotor and skeleton motor control characteristics are differently combined in the two largest groups of electric fish: African mormyriformes (comprising Mormyridae and Gymnarchidae) and America gymnotiformes (comprising Apteronotidae, Sternopygidae, Hypopomidae, Rhamphychthydae and Gymnotidae).
African Mormyridae are carangiform fish. They emit a brief pulsatile EOD (on the order of ms) separated by irregular intervals. This pulse is generated by an electrogenic organ (EO) concentrated at the caudal peduncle. Because of this localized EO, in the absence of objects, the electroreceptor stimuli have the same temporal course all over the fish surface (Caputi et al., 1998, Pedraja et al., 2014). Moreover, resistive objects change the amplitude pattern but do not change the temporal course of the local EOD. In addition, tail movements change the relative location of the EO with regard to the fish’s body. Thus electric images evoked by the EOD on the surface of the fish’s skin change in amplitude with swimming movements. These changes in object’s polarization are cancelled at the first central electrosensory relay, the electrosensory lobe (Sawtell, 2010).
Pulse gymnotiformes (Hypopomidae, Rhamphychthydae and Gymnotidae) also emit a pulsed EOD but separated by regular interval. In addition, these fish show a heterogeneous EO distributed over the caudal 90% of its fusiform body. Since the different body regions discharge different waveforms, the whole discharge consists of a complex but stereotyped spatio-temporal pattern (Caputi, 1999, Caputi et al., 2005, Caputi et al., 1998, Caputi et al., 1994, Caputi et al., 1989). These fish are propelled by a single anal ribbon fin that undulates driven by a traveling wave. Speed and traveling direction of this wave are controlled by a motorneuron network morphologically and functionally independent from the main motor system controlling lateral movements of the fish’s body (Trujillo-Cenóz et al., 1986).
African Gymnarchidae and American wave gymnotiformes (Apteronotidae, Sternopygidae) also have a fusiform body shape but emit a continuous sinewave-like carrier. Wave emitting fish show a distributed EO occupying the caudal 90% of the fish’s body in which regional EOD waveforms are shifted in phase (Pedraja et al., 2014).
These differences in electromotor and skeleton-motor behaviors are associated with differences in electrosensory systems. The first neural electrosensory relay is the electrosensory lateral line lobe (ELL) located dorso-laterally at the medulla. This is a cerebellum-like structure showing a so called “passive or ampullary” electrosensory pathway originated on ampullary receptors, mainly sensitive to slow variations of transcutaneous potentials but also in minor extent to their own EOD and to mechanical stimuli (Bell, 1979, Bell, 1981, Kalmijn, 1974) and two paths originated in tuberous receptors sensing transient changes in transcutaneous electric fields. These are (a) the fast electrosensory pathway encoding fast transients or zero crossings of self- and allo-generated emitted fields (Bell, 1989, Bell and Grant, 1989, Bell and Grant, 1992, Bell et al., 1992, Bell et al., 1993, Castelló et al., 1998, Hopkins and Bass, 1981, Matsushita et al., 2013, Nogueira and Caputi, 2011, Nogueira and Caputi, 2013, Nogueira et al., 2006, Sotelo et al., 1975, Szabo, 1967, Szabo et al., 1975) and (b) the slow electrosensory pathway encoding the changes in amplitude and waveform of the self- and allo-generated electric fields (Aguilera and Caputi, 2003, Bastian, 1986b, Bastian, 1986c, Bell, 1979, Bell and Grant, 1992, Bell et al., 1992, Caputi et al., 2008, Caputi et al., 2003, Pereira et al., 2005, Scheich and Bullock, 1974, von der Emde, 1990).
The slow electrosensory pathway has been extensively explored in mormyriformes and wave gymnotiformes (for wave gymnotiformes see: Bastian, 1995, Bastian, 1986a, Bastian, 1986b, Bastian, 1986c, Bastian et al., 1993, Bastian et al., 2004, Berman and Maler, 1998a, Berman and Maler, 1998b, Berman and Maler, 1998c, Carr and Maler, 1986, Chacron et al., 2005, Chacron et al., 2011, Clarke et al., 2013, Fernández et al., 2005, Khosravi-Hashemi and Chacron, 2014, Krahe and Maler, 2014, Maler, 1979, Maler et al., 1981, Maler et al., 1982, Marsat et al., 2012, Mehaffey et al., 2008, Turner et al., 1996; Turner and Maler, 1999; Turner et al., 2002 and for african pulse fish see: Bell and Grant, 1992, Bell et al., 1997a, Bell et al., 1997b, Bell et al., 1992, Engelmann et al., 2008, Han et al., 2000, Kennedy et al., 2014, Meek et al., 1999, Mohr et al., 2003a, Mohr et al., 2003b, Sawtell and Bell, 2008, Sawtell and Williams, 2008, Sawtell et al., 2007). However, only a few studies have examined the ELL of pulse Gymnotiforms (Caputi et al., 2008, Pereira et al., 2005, Réthelyi and Szabo, 1973a, Réthelyi and Szabo, 1973b, Schlegel, 1973, Stoddard, 1998) or wave mormyriforms (Kawasaki, 2005, Kawasaki, 1993, Matsushita and Kawasaki, 2004, Kawasaki and Guo, 1996). This motivates the present study that addresses the question of how the ELL network responds to the naturally generated EOD in G. omarorum.
We recorded field potentials and unitary activity evoked by the EOD in the ELL of decerebrated but spontaneously discharging fish. Three main sensory potentials at about 7, 13 and 23 ms after the EOD were identified. Unitary recordings show that individual neurons also fire following characteristic post-EOD patterns. In addition, some of these units show a clear reduction in firing probability immediately after the EOD, suggesting a fast feed forward inhibition in the ELL network that could precede the effects of slower afferent fibers.
Section snippets
Experimental procedures
Twelve G. omarorum of 20–30 cm in length were used following the guidelines of the CHEA (Comisión Honoraria de Experimentación Animal, ordinance 4332-99, Universidad de la República Oriental del Uruguay). Experiments were approved by the Animal Ethics Committee of the Instituto de Investigaciones Biológicas Clemente Estable (protocol number 001/03/2011). Fish were gathered at Laguna del Cisne (Maldonado, Uruguay) 1–4 months before the experiment, kept in individual aquaria under a natural light
The anatomical structure of the ELL
In order to provide the reader with a reference of the network under study we briefly summarize and illustrate the structure of the ELL of G. omarorum (to be described in detail elsewhere). Our data generally confirmed the findings of several authors in wave and pulse Gymnotiformes (Berman and Maler, 1999, Maler, 1979, Réthelyi and Szabo, 1973a, Sas and Maler, 1987, Sas and Maler, 1983, Schumway, 1989).
As in all gymnotiformes the ELL shows 3 laminated tuberous maps (Fig. 1A, centromedial, CM;
Discussion
Our anatomical results confirm the structure of the electrosensory lobe of G. omarorum previously described by Réthelyi and Szabo (1973a), and its similarity with the well-studied cerebellum-like homologous structure of wave Gymnotiformes (Berman and Maler, 1999, Carr and Maler, 1986, Chacron et al., 2011, Krahe and Maler, 2014, Maler, 2009a, Maler, 2009b, Maler, 1979, Maler et al., 1991, Marsat et al., 2012, Schumway, 1989). In particular, we confirmed recent findings (Maler, 2009a, Maler,
Conclusion
A clear excitation–inhibition–excitation post EOD activation sequence is observed in field potentials and unitary recordings. This is strikingly different from post EOD effects in wave fish. Thus, it appears that a similar neural structure might process differently the sensory information when it is driven at a different frequency regime. Our data indicate that some of these differences may be due to feed forward activation of an inhibitory path. More work is necessary to specify the
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