Sensory cells determine afferent terminal morphology in cross-innervated electroreceptor organs: implications for hair cells.
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.
Zakon
H
H
Department of Zoology and Center for Developmental Biology, Patterson Laboratory, University of Texas, Austin, Texas 78712, USA.
Lu
Y
Y
Weisleder
P
P
D000818:Animals; D015415:Biomarkers; D064026:Calbindins; D004555:Electric Fish / Q000502:physiology*; D004557:Electric Organ / Q000033:anatomy & histology / Q000166:cytology* / Q000637:transplantation; D005145:Face / Q000294:innervation / Q000601:surgery; D018069:Hair Cells, Vestibular / Q000737:chemistry / Q000166:cytology* / Q000648:ultrastructure; D008854:Microscopy, Electron; D009411:Nerve Endings / Q000502:physiology; D009419:Nerve Tissue Proteins / Q000032:analysis; D010320:Parvalbumins / Q000032:analysis; D064030:S100 Calcium Binding Protein G / Q000032:analysis; D009418:S100 Proteins / Q000032:analysis
D015415:Biomarkers; D064026:Calbindins; D009419:Nerve Tissue Proteins; D010320:Parvalbumins; D064030:S100 Calcium Binding Protein G; D009418:S100 Proteins