Inner ear sensory synapses faithfully transduce information over a wide range of stimulus intensities for prolonged periods of time. The efficiency of such demanding and stringent exocytotic activity depends on the presence of specialised presynaptic ribbons in the sensory hair cells. Ribbons are electron dense structures able to tether a large number of releasable vesicles at the synaptic active zone and can maintain high rates of vesicle release. Calcium entry through CaV1. 3 (L-type) Ca2+ channels in response to cell depolarization causes local increases in Ca2+ at the ribbon synapses, which is detected by the exocytotic Ca2+ sensors. At ribbon synapses of mature vestibular hair cells (VHCs), the coupling between Ca2+ channels and the exocytotic Ca2+ sensor remains unclear. We studied the Ca2+ dependence of exocytosis and the release kinetics of different vesicle pool populations in mature synaptotagmin-4 (Syt-4) mouse VHCs using patch-clamp capacitance measurements under physiological recording conditions. Exocytosis in adult Type II VHCs showed a high order dependence on Ca2+ entry, which contrasts with the linear Ca2+ dependence observed in adult mammalian auditory inner hair cells (IHCs). The synaptic properties of mature Type II VHCs, including the characteristics of the Ca2+ current and dynamics of vesicle release, were not affected by an absence of Syt-4. By contrast, the release of synaptic vesicles from Type I VHCs was very small in both Syt-4 control and KO cells, even for long voltage steps, which prevented us from uncovering the Ca2+ dependence of release. Our findings show that the coupling between Ca2+ influx and neurotransmitter release at VHC ribbon synapses at Type II VHCs is described by a non-linear relation that is likely to be more appropriate for the faithful encoding of low frequency vestibular information, consistent with that observed in very low frequency mammalian IHCs. On the other hand synaptic vesicle release at mature Type I VHCs was very small suggesting that these cells favour faster non-quantal transmission in order to drive the most rapid reflex in the body, the vestibular-ocular reflex.

The Properties of Synaptic Transmission in Adult Mammalian Vestibular Hair Cells Differs Between Type I and Type II Cells

Paolo Spaiardi;Sergio Masetto;
2019-01-01

Abstract

Inner ear sensory synapses faithfully transduce information over a wide range of stimulus intensities for prolonged periods of time. The efficiency of such demanding and stringent exocytotic activity depends on the presence of specialised presynaptic ribbons in the sensory hair cells. Ribbons are electron dense structures able to tether a large number of releasable vesicles at the synaptic active zone and can maintain high rates of vesicle release. Calcium entry through CaV1. 3 (L-type) Ca2+ channels in response to cell depolarization causes local increases in Ca2+ at the ribbon synapses, which is detected by the exocytotic Ca2+ sensors. At ribbon synapses of mature vestibular hair cells (VHCs), the coupling between Ca2+ channels and the exocytotic Ca2+ sensor remains unclear. We studied the Ca2+ dependence of exocytosis and the release kinetics of different vesicle pool populations in mature synaptotagmin-4 (Syt-4) mouse VHCs using patch-clamp capacitance measurements under physiological recording conditions. Exocytosis in adult Type II VHCs showed a high order dependence on Ca2+ entry, which contrasts with the linear Ca2+ dependence observed in adult mammalian auditory inner hair cells (IHCs). The synaptic properties of mature Type II VHCs, including the characteristics of the Ca2+ current and dynamics of vesicle release, were not affected by an absence of Syt-4. By contrast, the release of synaptic vesicles from Type I VHCs was very small in both Syt-4 control and KO cells, even for long voltage steps, which prevented us from uncovering the Ca2+ dependence of release. Our findings show that the coupling between Ca2+ influx and neurotransmitter release at VHC ribbon synapses at Type II VHCs is described by a non-linear relation that is likely to be more appropriate for the faithful encoding of low frequency vestibular information, consistent with that observed in very low frequency mammalian IHCs. On the other hand synaptic vesicle release at mature Type I VHCs was very small suggesting that these cells favour faster non-quantal transmission in order to drive the most rapid reflex in the body, the vestibular-ocular reflex.
2019
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/11571/1461764
Citazioni
  • ???jsp.display-item.citation.pmc??? ND
  • Scopus ND
  • ???jsp.display-item.citation.isi??? ND
social impact