Distinct neuron phenotypes may serve object feature sensing in the electrosensory lobe of Gymnotus omarorum.

Early sensory relay circuits in the vertebrate medulla often adopt a cerebellum-like organization specialized for comparing primary afferent inputs with central expectations. These circuits usually have a dual output, carried by center ON and center OFF neurons responding in opposite ways to the same stimulus at the center of their receptive fields. Here, we show in the electrosensory lateral line lobe of Gymnotiform weakly electric fish that basilar pyramidal neurons, representing 'ON' cells, and non-basilar pyramidal neurons, representing 'OFF' cells, have different intrinsic electrophysiological properties. We used classical anatomical techniques and electrophysiological in vitro recordings to compare these neurons. Basilar neurons are silent at rest, have a high threshold to intracellular stimulation, delayed responses to steady-state depolarization and low pass responsiveness to membrane voltage variations. They respond to low-intensity depolarizing stimuli with large, isolated spikes. As stimulus intensity increases, the spikes are followed by a depolarizing after-potential from which phase-locked spikes often arise. Non-basilar neurons show a pacemaker-like spiking activity, smoothly modulated in frequency by slow variations of stimulus intensity. Spike-frequency adaptation provides a memory of their recent firing, facilitating non-basilar response to stimulus transients. Considering anatomical and functional dimensions, we conclude that basilar and non-basilar pyramidal neurons are clear-cut, different anatomo-functional phenotypes. We propose that, in addition to their role in contrast processing, basilar pyramidal neurons encode sustained global stimuli such as those elicited by large or distant objects while non-basilar pyramidal neurons respond to transient stimuli due to movement of objects with a textured surface.

Cell Proliferation, Migration, and Neurogenesis in the Adult Brain of the Pulse Type Weakly Electric Fish, Gymnotus omarorum.

Adult neurogenesis, an essential mechanism of brain plasticity, enables brain development along postnatal life, constant addition of new neurons, neuronal turnover, and/or regeneration. It is amply distributed but negatively modulated during development and along evolution. Widespread cell proliferation, high neurogenic, and regenerative capacities are considered characteristics of teleost brains during adulthood. These anamniotes are promising models to depict factors that modulate cell proliferation, migration, and neurogenesis, and might be intervened to promote brain plasticity in mammals. Nevertheless, the migration path of derived cells to their final destination was not studied in various teleosts, including most weakly electric fish. In this group adult brain morphology is attributed to sensory specialization, involving the concerted evolution of peripheral electroreceptors and electric organs, encompassed by the evolution of neural networks involved in electrosensory information processing. In wave type gymnotids adult brain morphology is proposed to result from lifelong region specific cell proliferation and neurogenesis. Consistently, pulse type weakly electric gymnotids and mormyrids show widespread distribution of proliferation zones that persists in adulthood, but their neurogenic potential is still unknown. Here we studied the migration process and differentiation of newborn cells into the neuronal phenotype in the pulse type gymnotid Gymnotus omarorum. Pulse labeling of S-phase cells with 5-Chloro-2'-deoxyuridine thymidine followed by 1 to 180 day survivals evidenced long distance migration of newborn cells from the rostralmost telencephalic ventricle to the olfactory bulb, and between layers of all cerebellar divisions. Shorter migration appeared in the tectum opticum and torus semicircularis. In many brain regions, derived cells expressed early neuronal markers doublecortin (chase: 1-30 days) and HuC/HuD (chase: 7-180 days). Some newborn cells expressed the mature neuronal marker tyrosine hydroxylase in the subpallium (chase: 90 days) and olfactory bulb (chase: 180 days), indicating the acquisition of a mature neuronal phenotype. Long term CldU labeled newborn cells of the granular layer of the corpus cerebelli were also retrogradely labeled "in vivo," suggesting their insertion into the neural networks. These findings evidence the neurogenic capacity of telencephalic, mesencephalic, and rhombencephalic brain proliferation zones in G. omarorum, supporting the phylogenetic conserved feature of adult neurogenesis and its functional significance.

Spatial distribution and cellular composition of adult brain proliferative zones in the teleost, Gymnotus omarorum.

Proliferation of stem/progenitor cells during development provides for the generation of mature cell types in the CNS. While adult brain proliferation is highly restricted in the mammals, it is widespread in teleosts. The extent of adult neural proliferation in the weakly electric fish, Gymnotus omarorum has not yet been described. To address this, we used double thymidine analog pulse-chase labeling of proliferating cells to identify brain proliferation zones, characterize their cellular composition, and analyze the fate of newborn cells in adult G. omarorum. Short thymidine analog chase periods revealed the ubiquitous distribution of adult brain proliferation, similar to other teleosts, particularly Apteronotus leptorhynchus. Proliferating cells were abundant at the ventricular-subventricular lining of the ventricular-cisternal system, adjacent to the telencephalic subpallium, the diencephalic preoptic region and hypothalamus, and the mesencephalic tectum opticum and torus semicircularis. Extraventricular proliferation zones, located distant from the ventricular-cisternal system surface, were found in all divisions of the rombencephalic cerebellum. We also report a new adult proliferation zone at the caudal-lateral border of the electrosensory lateral line lobe. All proliferation zones showed a heterogeneous cellular composition. The use of short (24 h) and long (30 day) chase periods revealed abundant fast cycling cells (potentially intermediate amplifiers), sparse slow cycling (potentially stem) cells, cells that appear to have entered a quiescent state, and cells that might correspond to migrating newborn neural cells. Their abundance and migration distance differed among proliferation zones: greater numbers and longer range and/or pace of migrating cells were associated with subpallial and cerebellar proliferation zones.

Waveform generation in the weakly electric fish Gymnotus coropinae (Hoedeman): the electric organ and the electric organ discharge.

This article deals with the electric organ and its discharge in Gymnotus coropinae, a representative species of one of the three main clades of the genus. Three regions with bilateral symmetry are described: (1) subopercular (medial and lateral columns of complex shaped electrocytes); (2) abdominal (medial and lateral columns of cuboidal and fusiform electrocytes); and (3) main [four columns, one dorso-lateral (containing fusiform electrocytes) and three medial (containing cuboidal electrocytes)]. Subopercular electrocytes are all caudally innervated whereas two of the medial subopercular ones are also rostrally innervated. Fusiform electrocytes are medially innervated at the abdominal portion, and at their rostral and caudal poles at the main portion. Cuboidal electrocytes are always caudally innervated. The subopercular portion generates a slow head-negative wave (V(1r)) followed by a head-positive spike (V(3r)). The abdominal and main portions generate a fast tetra-phasic complex (V(2345ct)). Since subopercular components prevail in the near field and the rest in the far field, time coincidence of V(3r) with V(2) leads to different waveforms depending on the position of the receiver. This confirms the splitting hypothesis of communication and exploration channels based on the different timing, frequency band and reach of the regional waveforms. The following hypothesis is compatible with the observed anatomo-functional organization: V(1r) corresponds to the rostral activation of medial subopercular electrocytes and V(3r) to the caudal activation of all subopercular electrocytes; V(2), and part of V(3ct), corresponds to the successive activation of the rostral and caudal poles of dorso-lateral fusiform electrocytes; and V(345ct) is initiated in the caudal face of cuboidal electrocytes by synaptic activation (V(3ct)) and it is completed (V(45ct)) by the successive activation of rostral and caudal faces by the action currents evoked in the opposite face.

Active electroreception in Gymnotus omari: imaging, object discrimination, and early processing of actively generated signals.

Weakly electric fishes "electrically illuminate" the environment in two forms: pulse fishes emit a succession of discrete electric discharges while wave fishes emit a continuous wave. These strategies are present in both taxonomic groups of weakly electric fishes, mormyrids and gymnotids. As a consequence one can distinguish four major types of active electrosensory strategies evolving in parallel. Pulse gymnotids have an electrolocating strategy common with pulse mormyrids, but brains of pulse and wave gymnotids are alike. The beating strategy associated to other differences in the electrogenic system and electrosensory responses suggests that similar hardware might work in a different mode for processing actively generated electrosensory images. In this review we summarize our findings in pulse gymnotids' active electroreception and outline a primary agenda for the next research.

Post-natal development of the electromotor system in a pulse gymnotid electric fish.

Some fish emit electric fields generated by the coordinated activation of electric organs. Such discharges are used for exploring the environment and for communication. This article deals with the development of the electric organ and its discharge in Gymnotus, a pulse genus in which brief discharges are separated by regular silent intervals. It is focused on the anatomo-functional study of fish sized between 10 and 300 mm from the species of Gymnotus, in which electrogenic mechanisms are best known. It was shown that: (1) electroreception and electromotor control is present from early larval stages; (2) there is a single electric organ from larval to adult stages; (3) pacemaker rhythmicity becomes similar to that of the adult when the body length becomes greater than 45 mm and (4) there is a consistent developmental profile of the electric organ discharge in which waveform components are added according to a programmed sequence. The analysis of these data allowed us to identify three main periods in post-natal development of electrogenesis: (1) before fish reach 55 mm in length, when maturation of neural structures is the main factor determining a characteristic sequence of changes observed in the discharge timing and waveform; (2) between 55 and 100 mm in length, when peripheral maturation of the effector cells and changes in post-effector mechanisms due to the fish's growth determine minor changes in waveform and the increase in amplitude of the discharge and (3) beyond 100 mm in length, when homothetic growth of the fish body explains the continuous increase in electric power of the discharge.

The role of single spiking spherical neurons in a fast sensory pathway.

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.

Electrolocation and electrocommunication in pulse gymnotids: signal carriers, pre-receptor mechanisms and the electrosensory mosaic.

Constraints introduced by signal carriers, pre-receptor mechanisms and receptor transduction are fundamental for shaping the signals used by the brain to build up perceptual images. This review analyses some of these constraints in the electrosensory system of pulse Gymnotids. First, it describes the characteristics and differences of electrolocation and electrocommunication carriers. Second, it analyses the role of electrogenic and non-electrogenic tissues of the fish body in the generation and conditioning of these carriers. Two pre-receptor mechanisms are discussed: (a) the funneling of currents to the perioral region and (b) a Mexican-hat profile involved in edge detection. Finally, some characteristics of the electroreceptor structure and the sensory mosaic are examined. We conclude that there is an electrosensory fovea at the perioral region where a large density and variety of receptors is stimulated by self- and conspecific-generated currents funneled there by non electrogenic tissues. Differences in carrier waveform may be used to distinguish between reafferent and communication signals.