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Abstract
Spontaneous excitatory postsynaptic currents (sEPSCs) measured from the first synapse in the mammalian auditory pathway reach a large mean amplitude with a high level of variance (CV between 0.3 and 1). This has led some to propose that each inner hair cell (IHC) ribbon-type active zone (AZ), on average, releases ∼6 synaptic vesicles (SVs) per sEPSC in a coordinated manner. If true, then the predicted change in membrane capacitance (Cm) for such multivesicular fusion events would equate to ∼300 attofarads (aF). Here, we performed cell-attached Cm measurements to directly examine the size of fusion events at the basolateral membrane of IHCs where the AZs are located. The frequency of events depended on the membrane potential and the expression of Cav1.3, the principal Ca2+-channel type of IHCs. Fusion events averaged 40 aF, which equates to a normal-sized SV with an estimated diameter of 37 nm. The calculated SV volumes showed a high degree of variance (CV > 0.6). These results indicate that SVs fused individually with the plasma membrane during spontaneous and evoked release and SV volume may contribute more variability in EPSC amplitude than previously assumed.
Highlights
Sound information is transmitted from inner hair cells (IHCs) in the cochlea to the brain via spiral ganglion neurons (SGNs)
While not driven by action potentials (APs), mammalian IHCs follow this general description in that (i) the evoked EPSCs (eEPSCs) at the onset of a presynaptic depolarization is often larger than the spontaneous excitatory postsynaptic currents (sEPSCs) and (ii) the mean sEPSC size is relatively constant during changes in event frequency and changes in extracellular Ca2+ levels [9, 10]
The findings suggest that mammalian IHC are not prone to coordinated multivesicular release (cMVR) during spontaneous and sustained exocytosis as suggested [3, 16], but rather release may be dominated by a univesicular release (UVR) scheme
Summary
Sound information is transmitted from inner hair cells (IHCs) in the cochlea to the brain via spiral ganglion neurons (SGNs). The standard approach used to estimate the postsynaptic response to a single SV release event entails measuring postsynaptic currents (PSCs) under conditions of low release probability, e.g., by blocking presynaptic APs with tetrodotoxin These miniature PSCs (mPSCs) are typically equated to the independent fusion of SVs. mPSC amplitude is widely reported to be insensitive to changes in extracellular Ca2+, and this holds true even when the frequency of spontaneous mPSCs is steeply enhanced by elevating extracellular Ca2+ levels [6, 7]. The observed fusion steps in membrane capacitance are consistent with the quantal hypothesis of synaptic transmission in which individual synaptic vesicles undergo exocytosis independently from each other This finding, in conjunction with previous work, raises the exciting possibility that action potential generation can be triggered by the release of a single vesicle at the IHC synapse
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