Pulse-discharging, weakly electric fish actively electrolocate by emitting electric organ discharges and sensing changes provided by objects on transepidermal self-generated electric fields. In this way they create a series of discrete electric images on a cutaneous electroreceptive mosaic (Lissmann, 1958; cf. Bullock, 1986 cf. Bullock, , 1999Bastian, 1986). In this study we examine how fish discriminate between electrosensory images of different contrast. This kind of analysis requires unambiguous definition and measurement of the stimulus (input) and of the related performance of a sensory system (output; Marr, 1982). Our recent knowledge of electric image generation mechanisms allowed us to control and measure the electrosensory image (Caputi and Budelli, 1995;Rasnow, 1996;Caputi et al., 1998;Stoddard et al., 1999;Nelson and MacIver, 1999;Budelli and Caputi, 2000;Sicardi et al., 2000;Caputi et al., 2003). Whereas the input is a clearly defined physical entity, the output of a sensory system can be considered as a broad spectrum of 'intangible facts'. Although sensation and perception may exist independently of any behavioural response, only behaviour can be measured objectively (Spector, 2000). So, we restricted our research to the analysis of an orienting behavior ('a specific behavioural act directed towards the extraction of information from the environment'; Sokolov, 1990) elicited by changes in stimulus contrast, aiming to infer electrosensory processing mechanisms.Pulse gymnotids show a typical orienting behavior, the novelty response (Lissmann, 1958;Szabo and Fessard, 1965;Larimer and McDonald, 1968;Bullock, 1969; cf. Hopkins, 1983;Kramer, 1990;Moller, 1995). This behavior consists of a transient shortening of the inter-electric organ discharge (EOD) interval triggered by changes in nearby impedance. It has been frequently used to test a fish's electrolocation ability and to assess the effects of reafferent and exafferent input on pacemaker frequency (Bullock, 1969;Heiligenberg, 1980;Grau and Bastian, 1986;Hall et al., 1995;Zellick and von der Emde, 1995;Post and von der Emde, 1999).After studying novelty responses evoked by a short-circuit in the presence of different amounts of noise, Heiligenberg (1980)

The fast electrosensory pathway (FEP) of gymnotiform fish is mediated by tuberous electroreceptor organs innervated by ganglion cells that synapse with spherical cells of the electrosensory lateral line lobe (ELL). Spherical cells project to the magnocellular mesencephalic nucleus. The electrosensory environment was represented somatotopically within ELL. The mandibular (MN) and the supraorbital (SON) nerves projected to rostral ELL (occupying 19-28% and 4-10%, respectively), and the posterior branch of the anterior lateral line nerve (pALLN) projected to caudal ELL (occupying 56-64%). Labeling with horseradish peroxidase or biotinylated dextran-amine demonstrated three kinds of synaptic endings coupling primary afferents to spherical cells: multiple synaptic knobs, medium-sized calyxes, and very large calyxes. Multiple synaptic knobs arose from MN and SON primary afferents and were found in a narrow rostral area covering the centrolateral (CLS) and lateral (LS) segments of ELL. Medium and large calyxes, proceeding from the same nerves, predominated in the remaining parts of the three segments of ELL containing spherical cells. Calyx-type endings were also found in the LS-occupying regions in which the pALLNs projected. Calyx-type endings formed gap junctions but also contained vesicles and showed submembrane specializations typical of chemical synapses. The postsynaptic spherical cells were linked by dendrosomatic gap junctions and were also contacted by unlabeled en passant synaptic boutons, whose fine structure suggested chemical transmission. Electrophysiological studies indicated that spherical cell responsiveness diminished after electrosensory stimulation. This apparently inhibitory phenomenon may be subserved by the unlabeled synaptic boutons, which possibly originate from interneurons that have yet to be identified.

No abstract

SUMMARYSupplementary material available online at

No abstract

No abstract

This paper describes the peripheral mechanisms involved in signal processing of self- and conspecific-generated electric fields by the electric fish Gymnotus carapo. The distribution of the different types of tuberous electroreceptor and the occurrence of particular electric field patterns close to the body of the fish were studied. The density of tuberous electroreceptors was found to be maximal on the jaw (foveal region) and very high on the dorsal region of the snout (parafoveal region), decaying caudally. Tuberous type II electroreceptors were much more abundant than type I electroreceptors. Type I electroreceptors occurred exclusively on the head and rostral trunk regions, while type II electroreceptors were found along as much as 90 % of the fish. Electrophysiological data indicated that conspecific- and self-generated electric currents are ‘funnelled’ by the high conductivity and geometry of the body of the fish. These currents are concentrated at the peri-oral zone, where most electroreceptors are located. Moreover, within this region, field vector directions were collimated, constituting the most efficient stimulus for electroreceptors. It can be concluded that the passive properties of the fish tissue represent a pre-receptor device that enhances exafferent and reafferent electrical signals at the fovea-parafoveal region.

SUMMARY One difficulty in understanding the brain is that of linking the structure of the neurons with their computational roles in neural circuits. In this paper we address this subject in a relative simple system, the fast electrosensory pathway of an electric fish, where sensory images are coded by the relative latency of a volley of single spikes. The main input to this path is a stream of discrete electric images resulting from the modulation of a self-generated carrier by the environment. At the second order cell level, a window of low responsiveness, reducing potential interference from other stimuli, follows activation of the path. In the present study, we further characterize the input–output relationship at the second order neurons by recording field potentials, and ascertain its cellular basis using in vitro whole cell patch recordings. The field potentials from freely behaving, socially interacting fish were obtained from chronically implanted fish restrained in a mesh pen. In addition, at the end of some experiments the fish was curarized and the fast electrosensory path responses to artificial stimuli were further explored. These in vivo approaches showed that larger stimuli cause larger and longer windows of low responsiveness. The simple spherical geometry of the second order cells allowed us to unveil the membrane mechanisms underlying this phenomenon in vitro. These spherical cells respond with a single spike at the onset of current steps of any amplitude and duration, showing inward and outward rectification, and a long refractory period. We postulate that a low-threshold K+ conductance generates the outward rectification. The most parsimonious interpretation of our data indicates that slow deactivation of this conductance causes the long refractory period. These non-linear properties of the membrane explain the single spiking profile of spherical cells and the low-responsiveness window observed in vivo. Since the electric organ discharges are emitted at intervals slightly longer than the duration of the low-responsiveness window,we propose that the described cellular mechanisms allow fish streaming self-generated images.