Synaptic studies inform the functional diversity of cochlear afferents☆

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Abstract

Type I and type II cochlear afferents differ markedly in number, morphology and innervation pattern. The predominant type I afferents transmit the elemental features of acoustic information to the central nervous system. Excitation of these large diameter myelinated neurons occurs at a single ribbon synapse of a single inner hair cell. This solitary transmission point depends on efficient vesicular release that can produce large, rapid, suprathreshold excitatory postsynaptic potentials. In contrast, the many fewer, thinner, unmyelinated type II afferents cross the tunnel of Corti, turning basally for hundreds of microns to form contacts with ten or more outer hair cells. Although each type II afferent is postsynaptic to many outer hair cells, transmission from each occurs by the infrequent release of single vesicles, producing receptor potentials of only a few millivolts. Analysis of membrane properties and the site of spike initiation suggest that the type II afferent could be activated only if all its presynaptic outer hair cells were maximally stimulated. Thus, the details of synaptic transfer inform the functional distinctions between type I and type II afferents. High efficiency transmission across the inner hair cell's ribbon synapse supports detailed analyses of the acoustic world. The much sparser transfer from outer hair cells to type II afferents implies that these could respond only to the loudest, sustained sounds, consistent with previous reports from in vivo recordings. However, type II afferents could be excited additionally by ATP released during acoustic stress of cochlear tissues.

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