Reciprocal synapses between inner hair cell spines and afferent dendrites in the organ of corti of the mouse

We provide, for the first time, ultrastructural evidence for the differentiation of reciprocal synapses between afferent dendrites of spiral ganglion neurons and inner hair cells. Cochlear synaptogenesis of inner hair cells in the mouse occurs in two phases: before and after the onset of hearing at 9-10 postnatal (PN) days. In the first phase, inner hair cells acquire afferent innervation (1-5 PN). Reciprocal synapses form around 9-10 PN on spinous processes emitted by inner hair cells into the dendritic terminals, predominantly in conjunction with ribbon afferent synapses. During the second phase, which lasts up to 14 PN, synaptogenesis is led by the olivocochlear fibers of the lateral bundle, which induce the formation of compound and spinous synapses. The afferent dendrites themselves also develop recurrent presynaptic spines or form mounds of synaptic vesicles apposed directly across inner hair cell ribbon synapses. Thus, in the adult 2-month mouse, afferent dendrites of spiral ganglion neurons are not only postsynaptic but also presynaptic to inner hair cells, providing a synaptic loop for an immediate feedback response. Reciprocal synapses, together with triadic, converging, and serial synapses, are an integral part of the afferent ribbon synapse complex. We define the neuronal circuitry of the inner hair cell and propose that these minicircuits form synaptic trains that provide the neurological basis for local cochlear encoding of the initial acoustic signals.