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The Journal of Neuroscience, April 1, 1998, 18(7):2581-2591

Sensory Cells Determine Afferent Terminal Morphology in Cross-Innervated Electroreceptor Organs: Implications for Hair Cells

Harold Zakon, Ying Lu, and Pedro Weisleder

Department of Zoology and Center for Developmental Biology, Patterson Laboratory, University of Texas, Austin, Texas 78712

Type I and type II hair cells of the vestibular system are innervated by afferents that form calyceal and bouton terminals, respectively. These cannot be experimentally cross-innervated in the inner ear to determine how they influence each other. However, analogous organs are accessible for transplantation and cross-innervation in the brown ghost electric fish. These fish possess three types of electroreceptor organs. Of these, the sensory receptors of the type I tuberous organ are S-100- and parvalbumin-positive with a calbindin-positive afferent that forms a large calyx around the organ. Neither the sensory receptors nor the afferents of the ampullary organs label with these antibodies, and the afferent branches form a single large bouton beneath each receptor cell. In controls, when cut ampullary afferents reinnervate transplanted ampullary organs, they have characteristic calbindin-negative terminals with large boutons. When type I tuberous afferents reinnervate ampullary organs, receptor cells remain S-100- and parvalbumin-negative, and the tuberous afferents still express calbindin. The nerve terminals, however, make large ampullary-like boutons on the receptor cells. These results suggest that (1) afferent terminal morphology is dictated by the receptor organ; (2) expression of calbindin by the afferent is not suppressed by innervation of the incorrect end organ; (3) ampullary organs generate ampullary receptor cells although innervated by tuberous afferents; and (4) ampullary receptor cells can be trophically supported by tuberous afferents.

Key words: tuberous organ; ampullary organ; hair cells; vestibular; cochlear; electric fish

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Copyright © 1998 Society for Neuroscience  0270-6474/98/1872581-11$05.00/0

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