Evidence for a medial K+ recycling pathway from inner hair cells
Introduction
Function of cochlear hair cells depends on opening of acoustically activated K+ channels in stereocilia and a depolarizing apical influx of K+. Subsequent flux of K+ through apical cytoplasm and across the basolateral plasmalemma would expose the hair cell to excessive K+ unless its accumulation were dissipated. Uptake of K+ by Deiters cells and forwarding of the ions through lateral supporting cells, outer sulcus cells and spiral ligament fibrocytes to strial marginal cells (Schulte and Steel, 1994; Spicer and Schulte, 1994a, Spicer and Schulte, 1994b, Spicer and Schulte, 1996; Kikuchi et al., 1995) avoids excessive ion build-up beneath the outer hair cells (OHCs) and serves in cycling K+ back to endolymph. The perception of such electrolyte recycling accords with knowledge that K+ supplying the Na,K-ATPase pump of the strial marginal cells derives from perilymph rather than blood (Konishi et al., 1978; Wada et al., 1979; Marcus, 1986; Salt and Konishi, 1986).
On the other hand, attention has not been paid to the need for a means of preventing the K+ accumulation that could result from activity of inner hair cells (IHCs) and their afferent neurons. It seems plausible to postulate a transcellular route for K+ flow away from IHCs like that in effect for OHCs. Whether ions effluxing from the IHCs and the OHCs follow the same lateral route has not been determined. However, several considerations point rather to a shorter more direct path in the medial direction from IHCs.
The present report addresses the question of medial K+ cycling by inquiry into the morphologic characteristics, interrelationships and content of ion transport mediators in cells of the proposed medial pathway. The findings provide a basis for modeling such activity by these cells (Fig. 1) and serve additionally to distinguish three types of interdental cells that apparently function differently and three classes of limbal fibrocytes thought to participate in different ways to medial ion flow. Because the ion transport capacity of spiral ligament fibrocytes decreases in senescent gerbils with presbyacusis (Gratton and Spicer, 1996), the effect of aging on Na,K-ATPase immunoreactivity of limbal fibrocytes was investigated as a further means of assessing their electrolyte transport activity.
Section snippets
Animals
Inner ears were obtained from 20 Mongolian gerbils (Meriones unguiculatus) of either gender between 3 and 6 months of age and five gerbils between 33 and 36 months of age. The animals were born and raised in a quiet vivarium, and the 3–6-month-old animals from this colony have shown normal hearing (Schmiedt, 1989; Mills et al., 1990). The handling of animals was approved by the Animal Care and Use Review Committee of the Medical University of South Carolina under NIH Grant R01 DC00713.
Morphological studies
Inner
Inner sulcus cells
The lateralmost ISC viewed in a toluidine blue stained thick section lay in close apposition laterally to the border cell (Fig. 2). The border cell neighbored along its lateral surface the IHC and joined both the hair cell and ISC apically where tight junction connections have been described (Kimura, 1975; Santi, 1988). The basal region of the border cell also contacted nerve fibers beneath the hair cell and processes of the inner phalangeal cell that neighbored the IHC laterally.
The inner
Dispersal of K+ effluxing from hair cells
In the course of generating acoustic and silent currents, cochlear hair cells release a steady flow of K+ basolaterally (Zidanic and Brownell, 1994). Substantial evidence attests to a mechanism for dissipating a K+ build-up around OHCs by directing flow of the ion transcellularly through the spiral ligament to strial marginal cells. Na,K-ATPase in cells of this lateral pathway (Schulte and Adams, 1989), ultrastructural features of the cells attesting to their cooperative interrelationships (
Acknowledgements
The authors thank Mrs. Nancy Smythe and Mrs. Barbara Schmiedt for their technical assistance and Mrs. Leslie Harrelson for her editorial assistance. This work was supported by Grants R01 DC00713 and P01 DC00422 from the National Institute on Deafness and Other Communication Disorders, National Institutes of Health.
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