Type I vestibular hair cells are contacted by an unusual calyx nerve terminal that envelopes the entire basolateral membrane. In addition, they express a signature low-voltage activated outward K+ current (IK,L) that dominates the membrane conductance. The functional meaning of IK,L and of the afferent calyx is still enigmatic. It has been speculated that the calyx is responsible for K+ accumulation in the synaptic cleft and that this accumulation cooperates with vesicular synaptic release in sustaining afferent transmission. By combining the patch-clamp whole-cell configuration with the whole crista preparation, we have recorded the current and voltage responses of mouse semicircular canal Type I and Type II hair cells in situ. epolarizing voltage steps elicited in many Type I hair cells the conventional large and sustained outward K+ current. However, in a notable percentage (51%) of Type I hair cells, the outward K+ current showed an evident time-dependent relaxation. In these cells, moreover, upon repolarization to -40 mV, the instantaneous current was inward, reversing to outward slowly with time. A reasonable explanation for the above results is that during large outward K+ currents, K+ accumulates around Type I hair cells, thus shifting the K+ reversal potential (VrevK+) toward more positive values. Since we never observed such effects when recording from Type II hair cells, we hypothesized that the presence of a residual nerve calyx was responsible for K+ accumulation. We also found that by using voltage protocols that increased extracellular K+ accumulation, IK,L deactivation was slowed down. Similar results, i.e. VrevK+ rightward shift and IK,L deactivation slowdown, were obtained by local perfusion of the preparation with an extracellular solution enriched in K+. In conclusion, our results provide electrophysiological evidence for an increased K+ concentration in the synaptic cleft between Type I hair cell and its calyx ending during outward K+ current activation. The resulting depolarization might be aimed at reinforcing and prolonging Ca2+ channels activation and thus afferent transmission during slow head movements detected by vestibular organs.

Evidence for K+ accumulation around mammalian vestibular Type I hair cells: An electrophysiological study.

TAVAZZANI, ELISA;RUSSO, GIANCARLO;MASETTO, SERGIO;PRIGIONI, IVO
2012-01-01

Abstract

Type I vestibular hair cells are contacted by an unusual calyx nerve terminal that envelopes the entire basolateral membrane. In addition, they express a signature low-voltage activated outward K+ current (IK,L) that dominates the membrane conductance. The functional meaning of IK,L and of the afferent calyx is still enigmatic. It has been speculated that the calyx is responsible for K+ accumulation in the synaptic cleft and that this accumulation cooperates with vesicular synaptic release in sustaining afferent transmission. By combining the patch-clamp whole-cell configuration with the whole crista preparation, we have recorded the current and voltage responses of mouse semicircular canal Type I and Type II hair cells in situ. epolarizing voltage steps elicited in many Type I hair cells the conventional large and sustained outward K+ current. However, in a notable percentage (51%) of Type I hair cells, the outward K+ current showed an evident time-dependent relaxation. In these cells, moreover, upon repolarization to -40 mV, the instantaneous current was inward, reversing to outward slowly with time. A reasonable explanation for the above results is that during large outward K+ currents, K+ accumulates around Type I hair cells, thus shifting the K+ reversal potential (VrevK+) toward more positive values. Since we never observed such effects when recording from Type II hair cells, we hypothesized that the presence of a residual nerve calyx was responsible for K+ accumulation. We also found that by using voltage protocols that increased extracellular K+ accumulation, IK,L deactivation was slowed down. Similar results, i.e. VrevK+ rightward shift and IK,L deactivation slowdown, were obtained by local perfusion of the preparation with an extracellular solution enriched in K+. In conclusion, our results provide electrophysiological evidence for an increased K+ concentration in the synaptic cleft between Type I hair cell and its calyx ending during outward K+ current activation. The resulting depolarization might be aimed at reinforcing and prolonging Ca2+ channels activation and thus afferent transmission during slow head movements detected by vestibular organs.
2012
File in questo prodotto:
Non ci sono file associati a questo prodotto.

I documenti in IRIS sono protetti da copyright e tutti i diritti sono riservati, salvo diversa indicazione.

Utilizza questo identificativo per citare o creare un link a questo documento: https://hdl.handle.net/11571/915634
Citazioni
  • ???jsp.display-item.citation.pmc??? ND
  • Scopus ND
  • ???jsp.display-item.citation.isi??? ND
social impact