Evidence for a medial K+ recycling pathway from inner hair cells

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Abstract

K+ effluxed from outer hair cells and their nerves is thought to flow laterally to strial marginal cells for recycling into scala media. Observations reported here provide evidence that K+ effluxed from inner hair cells and inner radial nerves travels medially through border cells, inner sulcus cells (ISCs), limbal fibrocytes and interdental cells (IDCs) for return to endolymph. Morphologic features of ISCs in the medial route resembled those of Hensen and Claudius cells in the lateral indicating an ion transport role for ISCs like that of Hensen and Claudius cells. Na,K-ATPase in plasmalemma of IDCs testified to their capacity to resorb and transport K+ through their known gap junctions. IDCs were differentiated into three subgroups. The most lateral IDCs formed short and long columns. Long columns contacted the medialmost ISC inferiorly and the undersurface of the tectorial membrane superiorly providing thereby a potential transcellular route for K+ transit from ISCs to endolymph. Short columns faced inner sulcus below and tectorial membrane above and accordingly possessed cells with opposite polarity at the bottom and top of the column. Short columns thus appeared situated to resorb electrolytes from limbal stroma for release into inner sulcus and beneath tectorial membrane at opposite ends of the column. The central IDCs were positioned for resorbing and transporting K+ effluxing from the Na,K-ATPase-rich stellate fibrocytes which spread toward the IDCs from near the inner sulcus. The most medial IDCs lined cup-like invaginations near the attachment of Reissner's membrane and lay apposed to light fibrocytes located between supralimbal fibrocytes and the medial IDCs. Content of Na,K-ATPase and position in the K+ transport route likened the limbal stellate fibrocytes to the spiral ligament type II fibrocytes and supralimbal fibrocytes to suprastrial fibrocytes in the lateral wall. From content of creatine kinase and position in the transport path, limbal light fibrocytes appeared analogous to spiral ligament type I fibrocytes. The additional finding that limbal fibrocytes showed unchanged or upregulated Na,K-ATPase immunoreactivity in aged gerbils with strial atrophy provided further evidence for an independent medial transport route and for the survival of inner hair cells in presbyacusis.

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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