The slow pathway in the electrosensory lobe of Gymnotus omarorum: Field potentials and unitary activity

https://doi.org/10.1016/j.jphysparis.2014.07.005Get rights and content

Highlights

  • Self-activation pattern of the electrosensory lobe of G. omarorum is described.

  • Current source density analysis shows a typical sequence of sinks and sources.

  • Six main types of neurons were identified according to their activation pattern.

  • Sinks and spikes indicate three main volleys of activity across the lobe.

  • This suggests different electrosensory processing in pulse and wave fish.

Abstract

This is a first communication on the self-activation pattern of the electrosensory lobe in the pulse weakly electric fish Gymnotus omarorum. Field potentials in response to the fish’s own electric organ discharge (EOD) were recorded along vertical tracks (50 μm step) and on a transversal lattice array across the electrosensory lobe (resolution 50 μm × 100 μm). The unitary activity of 82 neurons was recorded in the same experiments. Field potential analysis indicates that the slow electrosensory path shows a characteristic post-EOD pattern of activity marked by three main events: (i) a small and early component at about 7 ms, (ii) an intermediate peak about 13 ms and (iii) a late broad component peaking after 20 ms. Unit firing rate showed a wide range of latencies between 3 and 30 ms and a variable number of spikes (median 0.28 units/EOD). Conditional probability analysis showed monomodal and multimodal post-EOD histograms, with the peaks of unit activity histograms often matching the timing of the main components of the field potentials. Monomodal responses were sub-classified as phase locked monomodal (variance smaller than 1 ms), early monomodal (intermediate variance, often firing in doublets, peaking range 10–17 ms) and late monomodal (large variance, often firing two spikes separated about 10 ms, peaking beyond 17 ms). The responses of multimodal units showed that their firing probability was either enhanced, or depressed just after the EOD. In this last (depressed) subtype of unit the probability stepped down just after the EOD. Early inhibition and the presence of early phase locked units suggest that the observed pattern may be influenced by a fast feed forward inhibition. We conclude that the ELL in pulse gymnotiformes is activated in a complex sequence of events that reflects the ELL network connectivity.

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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