Comparative anatomy of the electrosensory lateral line lobe of mormyrids: the mystery of the missing map in the genus Stomatorhinus (family: Mormyridae)

Fish in the family Mormyridae produce weak electric organ discharges that are used in orientation and communication. The peripheral and central anatomy of the electrosensory system has been well studied in the species Gnathonemus petersii, but comparative studies in other species are scarce. Here we report on one genus of mormyrid that displays a remarkable change in the electrosensory lateral line lobe (ELL), the hypertrophied rhombencephalic structure that receives primary electroreceptor input. Although all other mormyrids studied have three distinct zones on each side of the ELL, fish of the genus Stomatorhinus exhibit only two. Therefore, the two-zone ELL is a unique derived characteristic shared by Stomatorhinus. We examined the cutaneous electroreceptors that project to the ELL in Stomatorhinus. All three types of electroreceptors previously described for G. petersii were present, but there was a significant change in one type, the mormyromast. Both mormyromast sensory cell types (A- and B-cells) are present, but the B-cell is not innervated in Stomatorhinus. We conclude that, although all cutaneous sensory cells are present, the missing B-cell afferents account for the loss of the dorsolateral zone of the ELL, and therefore the loss of an entire sensory map. Because mormyromasts are involved in electrolocation behavior, this anatomical difference is probably related to differences in electrolocation abilities. Stomatorhinus could prove to be an excellent system for linking evolutionary changes in behavior with modifications in their neural substrates.     

Calretinin-like immunoreactivity in mormyrid and gymnarchid electrosensory and electromotor systems

Calretinin-like immunoreactivity was examined in the electrosensory and electromotor systems of the two families of mormyriform electric fish. Mormyrid fish showed the strongest immunoreactivity in the knollenorgan electroreceptor pathway; in the nucleus of the electrosensory lateral line lobe (ELL) and the big cells of the nucleus exterolateralis pars anterior. Mormyromast and ampullary zones of the ELL showed calretinin-like immunoreactivity in the ganglion, granule, and intermediate cell and fiber layers. Mormyromast zones additionally showed labeling of apical dendrites and commissural cells, but the ampullary zone did not. In the electromotor system, two nuclei in the corollary discharge pathway showed labeling: in the paratrigeminal command-associated nucleus and the juxtalobar nucleus. Gymnarchus niloticus (Gymnarchidae) showed strongest calretinin-like immunoreactivity in part of the phase-coding pathway; in S-type electroreceptor afferents. Zones of the ELL not receiving phase-coder input had weak labeling. The electromotor system showed labeling in the lateral relay nucleus and less strongly in the medullary relay nucleus, but none in the pacemaker. The concentration of calcium-binding proteins in mormyrid and gymnarchid time-coding electrosensory pathways is consistent with the hypothesis that they play a role in preserving temporal information across synapses. Cell types that encode temporal characteristics of stimuli in precise spike times have high levels of calcium-binding proteins, but cells that re-code temporal information into presence or magnitude of activity have low levels. Some cell types in the electromotor pathways and early in the time-coding electrosensory pathways do not follow this hypothesis, and therefore preserve temporal information using a mechanism independent of calcium-binding proteins. In particular, electromotor systems may use extensive electrotonic coupling within nuclei to ensure precise timing. J. Comp. Neurol. 387:341–357, 1997. © 1997 Wiley-Liss, Inc.     

Descending control of electroreception. I. Properties of nucleus praeeminentialis neurons projecting indirectly to the electrosensory lateral line lobe

The first-order CNS processing region within the electrosensory system, the electrosensory lateral line lobe, receives massive descending inputs from the nucleus praeeminentialis as well as the primary afferent projection. The n. praeeminentialis receives its input from the electrosensory lateral line lobe as well as from higher centers; hence this nucleus occupies an important position in a feedback loop within the electrosensory system. This report describes the physiological properties of a category of n. praeeminentialis neurons characterized by very high spontaneous firing frequency, but relatively poor sensitivity to electrolocation targets as compared to neurons in the electrosensory lateral line lobe. These neurons are specialized to encode long-term changes in electric organ discharge amplitude with high resolution. Intracellular recording and Lucifer yellow staining of these neurons show that they are the previously described multipolar neurons of the n. praeeminentialis, and they project bilaterally to the posterior eminentia granularis. Posterior eminentia granularis efferents project to the electrosensory lateral line lobe forming its dorsal molecular layer. Hence, these multipolar cells influence the electrosensory lateral line lobe circuitry indirectly. The information that the multipolar cells encode regarding the electric organ discharge amplitude may be needed for a gain control mechanism operative within the electrosensory lateral line lobe. Previous studies have shown that the indirect projection from the n. praeeminentialis to the electrosensory lateral line lobe must be intact for this gain control mechanism to operate.     

Descending control of electroreception. II. Properties of nucleus praeeminentialis neurons projecting directly to the electrosensory lateral line lobe

The nucleus praeeminentialis projects to the electrosensory lateral line lobe via 2 distinct pathways. Neurons that project to the posterior eminentia granularis and therefore influence the electrosensory lateral line lobe indirectly are described in the preceding report. This report describes the physiological properties and anatomical characteristics, revealed with Lucifer yellow staining, of n. praeeminentialis neurons that project directly to the ventral molecular layer of the electrosensory lateral line lobe. The neurons studied were the stellate cells described by Sas and Maler (1983), and we found 2 physiological subtypes of these. These neurons typically had no spontaneous activity, but responded vigorously to either increased electric organ discharge amplitude on the contralateral side of the body (ST-E cells) or to decreased amplitude (ST-I cells). These neurons also responded to low-frequency sinusoidal electric organ discharge amplitude modulations (AM) but were inhibited by AMs having frequencies greater than about 16 Hz. These stellate neurons were unable to encode information about long-term changes in electric organ discharge amplitude, but they responded very well to moving electrolocation targets. The relatively long response latency of these neurons suggests that they receive inputs from higher centers in addition to those from the electrosensory lateral line lobe. It is suggested that these cells alter the sensitivity of restricted populations of output cells in the electrosensory lateral line lobe and process temporally and spatially restricted stimuli. They may act to increase the intensity of the neural representation of important stimuli.     

Postembryonic changes in the peripheral electrosensory system of a weakly electric fish: addition of receptor organs with age

The organization of the peripheral electrosensory system of the cheek was studied in an age-graded series of Sternopygus dariensis in Nissl-stained sections and silver-stained whole mounts of skin. As in other gymnotoids, both ampullary and tuberous electroreceptors are present. Small fish have only one ampullary organ or tuberous organ per axon, and the number of receptor organs per axon increases with age in both ampullary and tuberous systems. Large fish may have up to ten tuberous organs per axon, although the distribution of tuberous organs per axon is bimodal with one peak occurring at a single receptor organ per axon and the other peak shifting upward in relation to the age of the fish. The ampullary system adds receptor organs at a faster rate and a large fish may have 20 ampullary organs per axon. With increasing size, the number of sensory receptor cells in each organ remains constant for both types of electroreceptors. Evidence is presented for addition of new electroreceptor units by de novo production in small fish and increases in the number of organs in existing electroreceptor units by division of previously formed organs in medium-sized and large fish. As the surface area of the skin increases with growth, the density of electroreceptor units decreases and, although new receptor organs are still being added to existing receptor units, no generation of new receptor units occurs in medium-sized to large fish.     

Larval electroreceptors in the epidermis of mormyrid fish: II. The promormyromast

Promormyromasts were found in the epidermis of the head of the larvae of five species of mormyrids bred in captivity. The promormyromast is a larval electroreceptor belonging to the specific lateral line system. In 12-day-old larvae this electroreceptor is characterized by a single sensory cell and two types of accessory cells. One type of accessory cell has dark cytoplasm, few microtubules, and contacts the sensory cell directly, whereas a second type has pale cytoplasm, many microtubules, and forms an outer layer not directly in contact with the sensory cell. This second type is referred to as a long pyriform accessory cell. This assembly of cells is situated below an intraepidermal cavity filled with acid polysaccharides. The bordering epidermal cells extend microvilli into the intraepidermal cavity. The apexes of the sensory cell, and of the two types of accessory cells, also open into the intraepidermal cavity but bear no microvilli. The promormyromast is innervated by an unmyelinated sensory nerve fiber passing through the basal membrane, which then splits into several branches between the accessory cells. These branches contact the periphery of the sensory cell with terminal boutons. At the site of each contact a ribbon-like structure surrounded by vesicles is present in the cytoplasm of the sensory cell. In older larvae of Campylomormyrus cassaicus, membrane foldings develop at the periphery of the pyriform accessory cells and accessory cell staining properties change just before transformation to become a mormyromast. The functional role of the promormyromast of the larval mormyrids is discussed.     

The effects of postembryonic receptor cell addition on the response properties of electroreceptive afferents

The weakly electric fish Sternopygus detects electric fields with a receptor organ called a tuberous electroreceptor. Previous studies have shown that an electroreceptive afferent fiber innervates a single organ in small fish and that as fish grow some of these organs divide, giving rise to daughter organs; these divide in turn to produce a cluster of organs. All of the organs in a cluster are innervated by the original afferent, which sprouts new terminals to accommodate them. Other organs, however, seldom divide. Thus, the distribution of the number of tuberous organs per afferent becomes increasingly bimodal with fish body length (Zakon, 1984a). In order to investigate the effect of organ addition on neural coding within the afferent fiber, activity was recorded from single units within the anterior branch of the anterior lateral line nerve in fish of a range of sizes. It was found that, as fish increase in body length, the best frequency, sharpness of tuning, and sensitivity increase in a subset of afferents, while others remain essentially unchanged. This results in an increasingly bimodal distribution of these physiological measures with increasing fish body length. These results suggest that the afferents that innervate multiple receptor organs are more sensitive and possess higher best frequencies than those that innervate 1 or 2 organs. This was confirmed by dye injections of electroreceptive fibers with Lucifer yellow.(ABSTRACT TRUNCATED AT 250 WORDS)     

Termination of electroreceptor and mechanical lateral line afferents in the mormyrid acousticolateral area

The projection regions of electroreceptor and mechanical lateral line afferents in electric fish of the mormyridae family are described. Electroreceptor afferents from the posterior dorsal skin run in the dorsal branch of the posterior lateral line nerve. Electroreceptor afferents from ventral skin and mechanical lateral line afferents and efferents run in the ventral branch of the nerve. Horseradish peroxidase (HRP) injections into each branch resulted in filling of its central terminals with the marker enzyme. The method yields a Golgi-like staining of afferent terminals, allowing some aspects of their morphology to be described. Comparison of results from dorsal and ventral branch injections shows the separate medullary regions to which electroreceptor and mechanical afferents project, and also demonstrates four separate somatotopic maps within the electroreceptor region. Mechanical afferents end predominantly ipsilaterally in nucleus anterior and eminentia granularis as has been suggested by others. Ipsilateral endings in nucleus octavius are also seen. Electroreceptor afferents end exclusively in the cortex and nucleus of posterior lateral line lobe (PLLL). Within the cortex there are three distinct maps of the skin surface which are separated from each other by discontinuities in the cellular layers. Somatotopic mapping is also present in the nucleus of PLLL though it is less precise than in the cortical zones. Large club endings of the cells of this nucleus are filled with HRP. Labeled cells are seen within a small midline nucleus located at the level of the eighth nerve just above the medial longitudinal fasciculus. These are probably the cell bodies of lateral line efferents.     

Tuberous electroreceptor organs form in denervated regenerating skin of a weakly electric fish

Weakly electric fish use tuberous electroreceptor organs to detect their own electric fields. We investigated the role of innervation upon regeneration and differentiation of tuberous electroreceptor organs. The left, infraorbital, anterior lateral line nerve of brown ghosts (Apteronotus leptorhynchus) was sectioned, and the proximal stump was dipped in ricin to prevent regrowth. Immediately after denervation, a piece of cheek skin (∼0.5 cm²) was removed bilaterally to induce skin regeneration. After survival periods of 3, 4, or 5 weeks, regenerated skin from the left (denervated) and the right (reinnervated) sides was removed and processed for immunocytochemistry or electron microscopy. Tuberous electroreceptor organs were present in regenerated reinnervated, as well as regenerated denervated skin patches at all survival times. With increased time after skin removal, the number of fully differentiated organs increased in the reinnervated regenerated skin while the number of organs with degenerating receptor cells or entirely devoid of receptor cells increased in the denervated regenerated skin. These results suggest that innervation is not essential for tuberous electroreceptor organ development, but that it is necessary for complete sensory cell differentiation and long-term survival. © 1996 Wiley-Liss, Inc.     

Development of the electrosensory nervous system in Eigenmannia (Gymnotiformes): I. The peripheral nervous system

The nerves of the anterior lateral line system in embryonic and larval stages of the weakly electric gymnotiform fish Eigenmannia were visualized by injection of the fluorescent marker DiI into the primordium of the anterior (ALLN) and posterior (PLLN) lateral line nerves. Examination of developmental series reveals that the nerve fibers that innervate the electrosensory and mechanosensory components of the anterior lateral line system are present before the first mechanoreceptors and electroreceptors have differentiated. This suggests that nerve fibers might induce the formation of lateral line receptors. Whereas the innervation of the mechanoreceptive system is already established at an early stage, the afferent innervation of electroreceptors continues to arborize in the periphery, presumably by following pioneer axon pathways. The earliest recognizable stage of the anterior lateral line nerve ganglion (ALLNG) is evident 2 days after spawning. The ganglion shows two germinal cell masses that develop into the supraorbital-infraorbital and the hyomandibular placodes. The supraorbital-infraorbital placode forms the dorsal part of the ALLNG; the hyomandibular placode forms the ventral part of the ALLNG. Counts of ALLNG cells in embryonic, larval, and adult stages of Eigenmannia show that, at each stage examined, the number of ganglion cells is always significantly larger than the number of mechanoreceptors and electroreceptor units in the periphery. During development, the distribution of ALLNG cell diameters shifts from a unimodal distribution in juveniles to a bimodal distribution in adults, peaking at 8 microns and 18 microns. These results suggest that tuberous electroreceptive organs, which are innervated by the large ALLNG cells, may not be functional prior to day 18. Our results further suggest that the number of ALLNG cells correlates with the rate of induction of lateral line receptors in the periphery.     

Peripheral organization and central projections of the electrosensory nerves in gymnotiform fish

The electrosensory system of weakly electric gymnotiform fish is described from the receptor distribution on the body surface to the termination of the primary afferentsin the posterior lateral line lobe (PLLL). There are two types of electroreceptor(ampullary and tuberous) and a single type of lateral line mechanoreceptor (neuromast). Receptor counts in Apteronotus albifronsshow that (1) neuromasts are distributed as in other teleosts; (2) ampullary receptors number 151 on one side of the head and 208 on one side of the body; (3) tuberous receptors were estimated to number 3,000-3,500 on one side of the head and 3,500-5,000 on one side of the body. The distribution of each receptor type is described. Each receptor is innervated by a single primary afferent. Electro-sensory afferents have myelinated cell bodies in the ganglion of the anterior lateral line nerve (ALLN). The distribution of these ganglion cell diameters is strongly bimodal in Apteronotus and Eigenmannia: The smaller-diameter cells may be those which innervate ampullary electroreceptors, the larger-diameter tuberous electroreceptors. Transganglionic HRP transport techniques were used to determine the first-order connections of the anterior lateral line nerve in six species of gymnotiform fish. Small branches of the ALLN were labeled so as to determine the somatotopic organization in the PLLL. The PLLL is divided into four segments from medial to lateral, termed medial, centromedial, centrolateral, and lateral segments (Heiligenberg and Dye, '81). Representations of the head are found rostrally in each zone, and the trunk is mapped caudally in each zone. Thus there are four body maps in the PLLL. The medial segment receives ampullary input (Heiligenberg and Dye, '82) and maps the dorsoventral body axis mediolaterally, as does the tuberous centrolateral segment. The tuberous centromedial and lateral segments map the dorsoventral axis lateromedially. Thus the medial and centromedial segments meet belly to belly, the centromedial and centrolateral segments meet back to back, and the centrolateral and lateral segments meet belly to belly. Adjacent electrosensory maps within the PLLL are therefore always mirror images.     

Mormyrid electrosensory lobe in vitro: Morphology of cells and circuits

The electrosensory lobe (ELL) of mormyrid electric fish is a cerebellum-like brainstem structure that receives the primary afferent fibers from electroreceptors in the skin. The ELL and similar sensory structures in other fish receive extensive input from other central sources in addition to the peripheral input. The responses to some of these central inputs are adaptive and serve to minimize the effects of predictable sensory inputs. Understanding the interaction between peripheral and central inputs to the mormyrid ELL requires knowledge of its functional circuitry, and this paper examines this circuitry in the in vitro slice preparation and describes the axonal and dendritic morphology of major ELL cell types based on intracellular labeling with biocytin. The cells described include medium ganglion cells, large ganglion cells, large fusiform cells, thick-smooth dendrite cells, small fusiform cells, granule cells, and primary afferent fibers. The medium ganglion cells are Purkinje-like interneurons that terminate on the two types of efferent cells, i.e., large ganglion and large fusiform cells, as well as on each other. These medium ganglion cells fall into two morphologically distinct types based on the distributions of basal dendrites and axons. These distributions suggest hypotheses about the basic circuit of the ELL that have important functional consequences, such as enhancement of contrast between “on” elements that are excited by increased afferent activity and “off” elements that are inhibited. J. Comp. Neurol. 404:359–374, 1999. © 1999 Wiley-Liss, Inc.     

Variation in the mode of receptor cell addition in the electrosensory system of gymnotiform fish

Age-related changes in ampullary and tuberous receptor organ morphology were studied in six species of gymnotiform weakly electric fish. Cheek skin was silver-stained, whole-mounted, and viewed under Nomarski differential interference contrast optics. The ampullary receptor units of all species show an increasing number of receptor organs per afferent fiber with fish size, presumably the result of addition of newly formed receptor organs. Ampullary units composing over a dozen organs were observed in large specimens of a few species. Receptor cells were also added in the tuberous receptor system of all species, but in different ways. As previously reported for Sternopygus, small specimens of Eigenmannia had only a single tuberous receptor organ per afferent. Fish of increasing size retained a population of afferents that innervated only a single receptor organ and, in addition, had a population of afferents that innervated a cluster of receptor organs. The mean number of receptor organs per cluster increased in fish of increasing size. In addition, the mean number of sensory receptor cells per organ increased. New organs presumably derive from older ones, which divide under the stimulus of continued addition of new receptor cells. Apteronotus, Adontosternarchus, and Hypopomus all added more receptor cells to their tuberous organs. In these species, every afferent innervated only a single tuberous organ and there was no indication of division of receptor organs. Gymnorhamphichthys and Gymnotus were intermediate in that they added new receptor cells to each receptor organ, and, in larger fish, these were segregated into discrete patches within a single receptor organ. It is likely that the addition of new receptor cells aids in increasing sensitivity of both ampullary and tuberous receptors as fish grow.     

Mucin-like glycopolymer gels in electrosensory tissues generate cues which direct electrolocation in amphibians and neuronal activation in mammals

Mucin-like glycoproteins have established roles in epithelial boundary protection and lubricative roles in some tissues.This mini-review illustrates alternative functional roles which rely on keratan sulphate and sialic acid modifications to mucin glycopolymers which convey charge properties suggestive of novel electroconductive properties not previously ascribed to these polymers.Many tumour cells express mucin-like glycopolymers modified with highly sulphated keratan sulphate and sialic which can be detected using diagnostic biosensors.The mucin-like keratan sulphate glycopolymer present in the ampullae of lorenzini is a remarkable sensory polymer which elasmobranch fish(sharks,rays,skate) use to detect weak electrical fields emitted through muscular activity of prey fish.Information on the proton gradients is conveyed to neuromast cells located at the base of the ampullae and mechanotransduced to neural networks.This ampullae keratan sulphate sensory gel is the most sensitive proton gradient detection polymer known in nature.This process is known as electrolocation,and allows the visualization of prey fish under conditions of low visibility.The bony fish have similar electroreceptors located along their lateral lines which consist of neuromast cells containing sensory hairs located within a cupula which contains a sensory gel polymer which detects distortions in fluid flow in channels within the lateral lines and signals are sent back to neural networks providing information on the environment around these fish.One species of dolphin,the Guiana dolphin,has electrosensory pits in its bill with similar roles to the ampullae but which have evolved from its vibrissal system.Only two terrestrial animals can undertake electrolocation,these are the Duck-billed platypus and long and short nosed Echidna.In this case the electrosensor is a highly evolved innervated mucous gland.The platypus has 40,000 electroreceptors around its bill through which it electrolocates food species.The platypus has poor eyesight,is a nocturnal feeder and closes its eyes,nostrils and ears when it hunts,so electrolocation is an essential sensory skill.Mammals also have sensory cells containing stereocilia which are important in audition in the organ of corti of the cochlea and in olfaction in the olfactory epithelium.The rods and cones of the retina also have an internal connecting cilium with roles in the transport of phototransduced chemical signals and activation of neurotransmitter release to the optic nerve.Mucin-like glycopolymer gels surround the stereocilia of these sensory hair cells but these are relatively poorly characterized however they deserve detailed characterization since they may have important functional attributes.     

Somatotopy within the medullary electrosensory nucleus of the little skate, Raja erinacea

The dorsal octavolateral nucleus is the primary electrosensory nucleus in the elasmobranch medulla. We have studied the topographic organization of electrosensory afferent projections within the dorsal nucleus of the little skate, Raja erinacea, by anatomical (HRP) and physiological experiments. The electrosensory organs (ampullae of Lorenzini) in skates are located in four groups on each side of the body, and each group is innervated by a separate ramus of the anterior lateral line nerve (ALLN). Transganglionic transport of HRP in individual rami demonstrated that electroreceptor afferents in each ramus project to a separate, nonoverlapping division of the central zone of the ipsilateral dorsal nucleus. These divisions, which are distinct areas separated by compact cell plates, are somatopically arranged. The volume of each division of the dorsal nucleus that is related to a single ramus is proportional to the number of ampullae innervated by the ramus, but not to the body surface area on which the receptors are distributed. Nearly one-half of the nucleus is devoted to electrosensory inputs from the buccal and superficial ophthalmic ampullae concentrated in a small area on the ventral surface of the head rostral to the mouth. Multiple and single unit recordings demonstrated that adjacent cells in the nucleus have similar receptive fields on the body surface and revealed a detailed point-to-point somatotopy within the nucleus. With threshold stimuli most single units have ipsilateral receptive fields made up by excitatory inputs from 2-5 ampullary organs. The somatotopy within the mechanosensory medial nucleus, also revealed by the HRP fills of individual ALLN rami, appears less rigid than that in the dorsal nucleus, as extensive overlap is present in the terminal fields of separate ALLN rami.     

Functional foveae in an electrosensory system

Several species of Mormyrid weakly electric fish have a mobile chin protuberance that serves as a mobile antenna during prey detection, tracking behaviors, and foraging for food. It has been proposed that it constitutes a fovea of the electrosensory system. The distribution of the three types of receptor organs involved in active imaging of the local surroundings, prey detection, and passive electroreception, and their central projection to the electrosensory lobe (ELL), have been studied in Gnathonemus petersii. Density distributions were compared for different body regions. Primary afferent projections were labeled with biocytin or biotinylated dextrans. This showed that there is considerable central "over-representation" of the mandibular and nasal regions of the sensory surface involved in electrolocation, at the expense of the other body regions investigated. This over-representation is not a mere effect of the very high density of receptor organs in these areas, but is found to be due to central magnification. This magnification differs between the subclasses of electroreceptors, suggesting a functional segregation in the brain. We conclude that the chin protuberance and the nasal region are the regions of greatest sensitivity for the resistive, capacitive, and low-frequency characteristics of the environment, and are probably most important in prey detection, whereas other regions of the skin with a lesser resolution and sensitivity to phase distortion of the EOD, in particular the trunk, are probably designed for imaging larger, inanimate features of the environment. Our data support the hypothesis that the chin appendage and nasal region are functionally distinct electrosensory foveae.     

Immunocytochemical identification of cell types in the mormyrid electrosensory lobe

The electrosensory lobes (ELLs) of mormyrid and gymnotid fish are useful sites for studying plasticity and descending control of sensory processing. This study used immunocytochemistry to examine the functional circuitry of the mormyrid ELL. We used antibodies against the following proteins and amino acids: the neurotransmitters glutamate and gamma-aminobutyric acid (GABA); the GABA-synthesizing enzyme glutamic acid decarboxylase (GAD); GABA transporter 1; the anchoring protein for GABA and glycine receptors, gephyrin; the calcium binding proteins calbindin and calretinin; the NR1 subunit of the N-methyl-D-aspartate glutamate receptor; the metabotropic glutamate receptors mGluR1alpha, mGluR2/3, and mGluR5; and the intracellular signaling molecules calcineurin, calcium calmodulin kinase IIalpha (CAMKIIalpha) and the receptor for inositol triphosphate (IP3R1alpha). Selective staining allowed for identification of new cell types including a deep granular layer cell that relays sensory information from primary afferent fibers to higher order cells of ELLS. Selective staining also allowed for estimates of relative numbers of different cell types. Dendritic staining of Purkinje-like medium ganglion cells with antibodies against metabotropic glutamate receptors and calcineurin suggests hypotheses concerning mechanisms of the previously demonstrated synaptic plasticity in these cells. Finally, several cell types including the above-mentioned granular cells, thick-smooth dendrite cells, and large multipolar cells of the intermediate layer were present in the two zones of ELL that receive input from mormyromast electroreceptors but were absent in the zone of ELL that receives input from ampullary electroreceptors, indicating markedly different processing for these two types of input. J. Comp. Neurol. 483:124-142, 2005. (c) 2005 Wiley-Liss, Inc.     

Larval electroreceptors in the epidermis of mormyrid fish: I. Tuberous organs of type A and B

Two types of larval electroreceptors, type A and B, are described in the epidermis of the head of larvae of three mormyrid species, Campylomormyrus cassaicus, Mormyrus rume proboscirostris and Pollimyrus isidori, bred in captivity. In each of these electroreceptor organs, a single sensory cell is found inside an intraepidermal cavity, sitting on a platform of accessory cells. The cavity is filled with microvilli originating both from the sensory cell and from the epidermal covering cells lining the intraepidermal cavity. These two types of tuberous larval electroreceptors differ in their distribution in the epidermis of the head, in the composition of their accessory cells, and by their innervation. The innervation found in type B organs is similar to that already described for electroreceptors of adult mormyrids. The sensorineural junction is composed of primary afferent terminal boutons, which contact the base of the sensory cell. Opposite each terminal bouton, a ribbon-like synaptic bar surrounded by vesicles is found in the cytoplasm of the sensory cell. In contrast, the base of the sensory cell in type A larval electroreceptors is not contacted by nervous terminal boutons, but instead forms closed appositions with specialized prolongations of accessory cells of the platform. The base of the sensory cell presents membrane evaginations, with hemispheric synaptic structures and few synaptic vesicles. These two types of electroreceptor organs degenerate at the time of the degeneration of the larval electric organ and the functional differentiation of the adult electric organ. The functional role of two tuberous electroreceptor types is examined.     

Gain control in the electrosensory system mediated by descending inputs to the electrosensory lateral line lobe

The electrosensory lateral line lobe (ELLL) of weakly electric fish, the primary electrosensory processing station, receives a large descending input from the midbrain in addition to the input from the electroreceptor afferents. The role of a major component of this descending input in determining the properties of ELLL output neurons was investigated. The descending input was reduced or eliminated by microinjections of the local anesthetic lidocaine or by small lesions. This treatment increased the responses of the ELLL output neurons to suprathreshold stimuli by about 300% and also increased the size of the neurons' receptive fields for moving electrolocation targets and the resolution with which they encode target distance. The neurons' threshold sensitivity and tuning to amplitude modulation frequency were unchanged by removal of the descending input. The results of this study show that this portion of the descending input to the ELLL normally mediates an inhibition that controls the responsiveness of ELLL output neurons. This descending input could function as a gain control mechanism, allowing the animal to modulate the sensitivity of the electrosensory system in response to changing environmental conditions.     

Unitary giant synapses embracing a single neuron at the convergent site of time-coding pathways of an electric fish, Gymnarchus niloticus

Phase-locking neurons in the electrosensory lateral line lobe (ELL) of a weakly electric fish, Gymnarchus niloticus, fire an action potential in response to each cycle of the sinusoidal electrosensory signal (350-500 Hz) created by the fish's own electric organ. The exact firing times of the phase-locking neurons are altered (time-shifted) by capacitance of electrolocation objects or by electric organ discharges of other individuals. The magnitude of the time shifts depends on the location of the neurons' receptive field on the skin; thus, time disparities arise between the firing of phase-locking neurons. To compute these disparities, there should be a site where these phase-locking neurons converge. In this study we morphologically identified a novel cell type, which we named the "ovoidal cell", that receives the convergent projections of phase-locking neurons in the inner cell layer (ICL) of the ELL. We labeled these neurons with biocytin and examined them by light and electron microscopy. The giant cells and the S-type primary afferents, two types of phase-locking neurons, respectively terminate on the soma via chemical synapses and on the dendrite of the ovoidal cells via mixed synapses. Each terminal of the giant cells embraces the soma of an ovoidal cell, covering as much as 84% of the somatic membrane. The giant cell terminals and ovoidal cell somata were immunoreactive to SV2, a synaptic vesicle protein, but the S-afferent terminals were not, even though they contain numerous synaptic vesicles. The dendrite of the ovoidal cells also contacts the pyramidal cells of the ICL, which are known to be sensitive to time disparities. The anatomical connections of the phase-locking neurons to the ovoidal cells strongly suggest that they are involved in computing time disparity.