Reciprocal synapses between outer hair cells and their afferent terminals: evidence for a local neural network in the mammalian cochlea.

Cochlear outer hair cells (OHCs) serve both as sensory receptors and biological motors. Their sensory function is poorly understood because their afferent innervation, the type-II spiral ganglion cell, has small unmyelinated axons and constitutes only 5% of the cochlear nerve. Reciprocal synapses between OHCs and their type-II terminals, consisting of paired afferent and efferent specialization, have been described in the primate cochlea. Here, we use serial and semi-serial-section transmission electron microscopy to quantify the nature and number of synaptic interactions in the OHC area of adult cats. Reciprocal synapses were found in all OHC rows and all cochlear frequency regions. They were more common among third-row OHCs and in the apical half of the cochlea, where 86% of synapses were reciprocal. The relative frequency of reciprocal synapses was unchanged following surgical transection of the olivocochlear bundle in one cat, confirming that reciprocal synapses were not formed by efferent fibers. In the normal ear, axo-dendritic synapses between olivocochlear terminals and type-II terminals and/or dendrites were as common as synapses between olivocochlear terminals and OHCs, especially in the first row, where, on average, almost 30 such synapses were seen in the region under a single OHC. The results suggest that a complex local neuronal circuitry in the OHC area, formed by the dendrites of type-II neurons and modulated by the olivocochlear system, may be a fundamental property of the mammalian cochlea, rather than a curiosity of the primate ear. This network may mediate local feedback control of, and bidirectional communication among, OHCs throughout the cochlear spiral.

Reciprocal innervation of outer hair cells in a human infant.

Reciprocal synapses are characterized by the presence of both afferent and efferent types of synaptic specializations between two cells. They have been described at the neural poles of outer hair cells (OHCs) in humans with advanced age and two monkey species. Our objective was to study the innervation of the OHCs and determine if reciprocal synapses were present in a young (8-month-old infant) human subject. We studied the synaptic and cytoplasmic morphology of 162 nerve terminals innervating 29 OHCs using serial section transmission electron microscopy. Seventy-six percent of all OHCs were innervated by terminals with reciprocal synapses. This prevalence increased from the first toward the third row (p < 0.001), and 100% of OHCs in the third row demonstrated at least one reciprocal synapse. The prevalence of terminals with reciprocal synapses was higher in the human infant than in older human subjects and was very similar to what has been reported for the chimpanzee. Reciprocal synapses occur in sufficient numbers to be physiologically significant in primates. The nerve terminals were found to segregate into two groups on the basis of their cytoplasmic morphological characteristics: (1) vesicle-rich/neurofilament-poor (VR/NP) and (2) vesicle-poor/neurofilament-rich (VP/NR). All afferent and reciprocal terminals were of the VP/NR variety. The majority of the efferent terminals originated from VR/NP nerve fibers (classical olivocochlear morphology), but 23.5% of the efferent terminals were VP/NR. The hypothesis that peripheral processes of type II spiral ganglion cells form classical afferent, reciprocal, and a number of purely presynaptic terminals on OHCs is discussed. The presence of different types of synaptic specializations on OHCs formed by nerve fibers of the same type (VP/NR) suggests the existence of reciprocal neuronal circuits between OHCs sharing the dendritic arborization of a type II spiral ganglion cell.

Axodendritic and dendrodendritic synapses within outer spiral bundles in a human.

Axodendritic and dendrodendritic synapses have been described at the level of the outer spiral bundle (OSB) (Nadol, J.B., Jr., 1983. Laryngoscope 93, 780-791; Bodian, D., 1978. Proc. Natl. Acad. Sci. USA 75, 4582-4586). The objectives of this study were to quantify these synaptic interactions and to describe their ultrastructural morphology in a young human subject. The temporal bone of an 8-month old infant was processed for transmission electron microscopy and semiserial section reconstructions of the three OSBs were performed. The nerve fibers ((NFs)) forming the OSBs were found to segregate into two morphological groups: (1) vesicle-rich and neurofilament-poor (VR/NP); (2) vesicle-poor and neurofilament-rich (VP/NR). Synapses between VR/NP and VP/NR NFs and synapses between two VP/NR NFs were quantified. Presumed axodendritic synapses (i.e. between VR/NP and VP/NR NFs) were numerous and their numbers decreased from the first towards the third row. Presumed dendrodendritic synapses (i.e. between two VP/NR NFs) were also frequent but their numbers did not vary significantly among different rows. The presence of axodendritic synapses may provide the morphological basis for modulation of the function of the type II spiral ganglion cells (type II's) by the olivocochlear efferent system. Similarly, numerous presumed dendrodendritic synapses may provide a morphological substrate for interaction between dendrites of type II's.