Time course of structural changes in regenerating electroreceptors of a weakly electric fish

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Abstract
We examined the regenerating electroreceptors of the weakly electric fish Sternopygus by light and electron microscopy to search for possible structural correlates of known physiological changes that occur during regeneration (Zakon: J. Neurosci. 6(11): 3297–3308, 1986) and to compare them with developing electroreceptors in larval fish (Vischer: Brain Behav. Evol. 33:223–236). Nine days after removal of a patch of cheek skin, new skin had filled the wound and undifferentiated precursor cell clusters were located in the epidermis just above the dermis. Nerve fibers were present near most, but not all, cell clusters. A few recognizable tuberous and ampullary precursor organs were seen at this time. Tuberous organs were composed of a group of large cells surrounded by smaller cells without a lumen and showed the beginning of a cellular plug. Ampullary organs appeared as a ball of cells with a small lumen opening into a nascent canal. Degenerating cells were found within organs, and sometimes entire organs degenerated. These were not innervated. By 2 weeks the large cells of the tuberous organ were developing into sensory cells, while the smaller cells were forming the capsule wall and the underlying basal cells. The characteristic tuberous organ canal filled with loosely packed epidermal cells was evident. The sensory cells of the ampullary organs were visible within the epithelial layer at the base of the lumen, and the large synaptic discs were beginning to form. The sensory cells and postsynaptic terminals contained numerous vesicles. The presynaptic vesicles, which appear in normal receptor cells, remained throughout regeneration and presumably underlie transmitter release. The postsynaptic vesicles appeared transiently in large numbers but declined to adult values by 4 weeks. We presume that these may serve a trophic role. By 3 weeks, organs generally appeared mature and began dividing into daughter organs. The formation of individual receptor organs during regeneration is similar to that observed in development. Receptor organs continued dividing until the appropriate number of organs per afferent was reached for the size of the fish. Although the organization of the receptors appeared generally normal, there were a few anomalies. Some afferents sent sprouts into the epidermis, and, as a result of such sprouting, some of these afferents innervated multiple organs over a greater distance than normal. This was first seen early in regeneration and persisted for as long as 5 months. In addition, as many as 20% of all tuberous units were innervated by two axons, which is significantly more than normal. Within a doubly innervated organ, each sensory cell was innervated by only one of the afferents. These anomalous innervation patterns may be the result of regenerating afferents attempting to establish rapidly their correct innervation of a number of sensory organs. To explain the degeneration of the receptor cells as well as the anomolous innervation patterns, we propose that (1) receptor organ formation occurs not through the transformation of epithelial cells, but of a limited number of precursor cells (basal cells?), into organs; (2) once formed, these organs are critically dependent on innervation for their survival; and (3) competition between afferents in dually innervated organs occurs at the level of the single sensory cell.

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