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Volume 17, Number 1, Issue of January 1, 1997 pp. 428-437
Copyright ©1997 Society for Neuroscience

Unique Postsynaptic Signaling at the Hair Cell Efferent Synapse Permits Calcium to Evoke Changes on Two Time Scales

Received July 12, 1996; revised Oct. 15, 1996; accepted Oct. 15, 1996.

T. S. Sridhar^{1, 2}, M. C. Brown^{1, 2, 3}, and W. F. Sewell^{1, 2, 4}

¹ Department of Otolaryngology, Eaton-Peabody Laboratory, Massachusetts Eye and Ear Infirmary, Boston, Massachusetts 02114-3096, ² Department of Otology and Laryngology, Harvard Medical School, Boston, Massachusetts 02115, ³ Harvard-MIT Division of Health Sciences and Technology, Cambridge, Massachusetts 02139, and ⁴ The Program in Neurosciences, Harvard Medical School, Boston, Massachusetts 02115

The cholinergic efferent fibers to the outer hair cells (OHCs) of the mammalian cochlea suppress sound-evoked activity of the auditory nerve on two time scales via one nicotinic receptor. A rapid action (tens of milliseconds) is responsible for modulating auditory nerve responses to acoustic stimulation. A slower action (tens of seconds) may protect the ear from acoustic overstimulation. The rapid action is likely caused by calcium influx through the nicotinic receptor that leads to opening of calcium-activated potassium (K_Ca) channels, but the mechanism of the slower action has not been explained. To investigate this mechanism, we perfused the cochlea with agents that alter intracellular calcium release and uptake. Both fast and slow effects were enhanced by perfusion of the cochlea with ryanodine, an agonist of calcium-induced calcium release (CICR). Antagonists of sarcoplasmic/endoplasmic reticulum calcium ATPase (SERCA), cyclopiazonic acid, and thapsigargin (1) selectively enhanced the magnitude of slow effects, (2) prevented the diminution of slow effects with continued efferent stimulation, and (3) spread the range of frequencies over which slow effects were observed. We propose that the slow effect is attributable to release of calcium from the subsurface cisterna of the OHC, perhaps triggered by CICR from the synaptic cisterna; the two time scales of efferent action may result from the unique arrangement of the two cisternae in the baso-lateral region of the OHC.

Key words: cochlea; outer hair cell; cyclopiazonic acid; subsurface cisterna; ryanodine; acetylcholine

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