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The Journal of Neuroscience, July 30, 2003, 23(17):6894-6903

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Presynaptic Calcium Stores Modulate Afferent Release in Vestibular Hair Cells

Andrea Lelli,^1,4 Paola Perin,² Marta Martini,³ Catalin D. Ciubotaru,^1,4 Ivo Prigioni,² Paolo Valli,² Maria L. Rossi,³ and Fabio Mammano^1,4,5

¹Venetian Institute of Molecular Medicine, via Giuseppe Orus 2, 35129 Padua, Italy, ²Department of Cell and Molecular Physiological and Pharmacological Sciences, University of Pavia, via Forlanini 6, 27100 Pavia, Italy, ³Department of Biology, Section of Physiology and Biophysics and Center for Neurosciences, University of Ferrara, via Borsari 46, 44100 Ferrara, Italy, ⁴National Institute of Physics of Matter, and ⁵Department of Physics, University of Padua, via Marzolo 8, 35129 Padua, Italy

Hair cells, the mechanoreceptors of the acoustic and vestibular system, are presynaptic to primary afferent neurons of the eighth nerve and excite neural activity by the release of glutamate. In the present work, the role played by intracellular Ca²⁺ stores in afferent transmission was investigated, at the presynaptic level, by monitoring changes in the intracellular Ca²⁺ concentration ([Ca²⁺]_i) in vestibular hair cells, and, at the postsynaptic level, by recording from single posterior canal afferent fibers. Application of 1-10 mM caffeine to hair cells potentiated Ca²⁺ responses evoked by depolarization at selected Ca²⁺ hot spots, and also induced a graded increase in cell membrane capacitance (C_m), signaling exocytosis of the transmitter. Ca²⁺ signals evoked by caffeine peaked in a region located 10 µm from the base of the hair cell. [Ca²⁺]_i increases, similarly localized, were observed after 500 msec depolarizations, but not with 50 msec depolarizations, suggesting the occurrence of calcium-induced calcium release (CICR) from the same stores. Both Ca²⁺ and C_m responses were inhibited after incubation with ryanodine (40 µM) for 8-10 min. Consistent with these results, afferent transmission was potentiated by caffeine and inhibited by ryanodine both at the level of action potentials and of miniature EPSPs (mEPSPs). Neither caffeine nor ryanodine affected the shape and amplitude of mEPSPs, indicating that both drugs acted at the presynaptic level. These results strongly suggest that endogenous modulators of the CICR process will affect afferent activity elicited by mechanical stimuli in the physiological frequency range.

Key words: calcium-induced calcium release; ryanodine receptor; exocytosis; voltage-activated Ca²⁺ channels; calcium hot spots; labyrinth; frog; synapse; afferent discharge; patch clamp; fluorescence microscopy

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Received Feb. 28, 2003; revised May. 29, 2003; accepted Jun. 9, 2003.

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