Weakly electric fish of the genus Eigenmannia were induced to spawn in conditions simulating the tropical rainy season. The skin of embryos of different ages was prepared for histological examination, and whole animals were examined by various histological methods and scanning electron microscopy. It was found that the electrosensory system develops after the first mechanoreceptive lines have formed. The tuberous and ampullary organs initially form adjacent to the lines of the lateral-line system. The tuberous organs develop at a rate 5 times higher than that of the ampullary organs. The rate of development for both classes of electroreceptors is 4 times higher on the head than on the trunk. The first tuberous organs develop on the head at day 7 and on the trunk at day 8. They increase in number and size during the growth of the fish. The ampullary organs begin to form on the head and on the most rostral part of the trunk at day 8. They are deeply sunk into the corium and have the same number of receptor cells as in adults. There are both ampullary and tuberous organs within fields of receptors that are innervated by a single nerve branch.
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.
The somatotopically and functionally organized electrosensory system of gymnotiform teleosts provides a model for the study of the formation of ordered nerve connections. This paper describes the development of the major electrosensory nuclei within the hind- and midbrain. All three main electrosensory nuclei--the electrosensory lateral line lobe (ELL), dorsal torus semicircularis (torus), and tectum--grow by adding cells at their caudolateral borders. Toral and tectal germinal zones arise from lateral ventricular outpocketings that either completely or partially close by maturity. In the ELL before day 5 postspawning, germinal cells form from an initial periventricular germinal zone, then migrate to the caudolateral border of the hindbrain and begin dividing. The ELL grows from two main germinal zones, one for the medial segment, and one for the three lateral tuberous segments. Within each ELL germinal zone, newly formed cells arise from two areas: granular cells arise from a ventral subzone, pyramidal cells are generated more dorsally. Granular cells remain in situ, whereas pyramidal cells may migrate rostromedially. Cells begin differentiating as soon as they are formed. Spherical and pyramidal cells send ascending axons into the internal plexiform layer by day 14-18 and the ELL gradually begins to assume its mature laminar appearance. The ELL grows caudally, preceding the caudal lobe of the cerebellum, which will eventually lie over and fuse with it. Primary electrosensory afferents enter the ELL by day 6; incoming afferents form four fascicles within the ELL, suggesting the formation of separate ELL segments. Unlabelled projections between labelled fields from a single nerve branch filled with HRP on day 7 suggest that somatotopic order is already present at this early age. In the periphery, receptor addition is unordered, occurring along nerve branch pathways. Meanwhile the ELL adds cells in an orderly fashion at its caudolateral border. This suggests that primary afferents shift position caudally with growth to maintain their somatotopic relationships. Because all three central nuclei are in topographic register and grow by adding cells caudally, during growth ELL efferents to the torus and toral efferents to the tectum may utilize passive mechanisms, such as fiber-fiber interactions, to guide axons.
Developmental patterns of electroreceptors in the weakly electric fish Eigenmannia were investigated by histological, histochemical, immunocytochemical, cell kinetic, ultrastructural, and computer-assisted three-dimensional reconstruction methods. The first cell of an electroreceptor primordium is embedded in the stratum germinativum of the epidermis. An unmyelinated, afferent nerve fiber ends near this cell below the basal lamina. Protrusions and vacuole-like inclusions at the basal lamina above the nerve fiber ending suggest a mechanism of nervous induction. The receptor primordium cell subsequently divides into a single cell layer. Within 48 hours, a second apical cell layer forms from the first, and, thus, the primordium differentiates into an apical layer of presumptive receptor cells and a basal layer of presumptive supporting cells. While the two layers further differentiate into mature receptor and supporting cells, the afferent fiber penetrates the basal lamina, sprouts, and forms a synapse with each receptor cell. Transitory fibers also project along the receptor cells to the top of the developing electroreceptor but degenerate during development. Synapses are smaller in early developmental stages compared to older stages, and pre- and postsynaptic vesicles are more abundant and widely distributed in younger stages. Moreover, presynaptic ribbons are longer and are interconnected at their apical ends. Supporting cells continue to divide during further maturation and form new receptor cells. The number of receptor cells per tuberous organ increases during the first 4 days of electroreceptor development and plateaus when the fish are 9 days old. It declines again when organs begin to divide into clusters.
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