Reciprocal Innervation of Outer Hair Cells in a Human Infant

Abstract

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 ®rst 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 suf®cient numbers to be physiologically signi®cant in primates. The nerve terminals were found to segregate into two groups on the basis of their cytoplasmic morphological characteristics: (1) vesicle-rich/neuro®lament-poor (VR/NP) and (2) vesicle-poor/neuro®lament-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 ®bers (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 ®bers 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.

Olivocochlear Efferents: Anatomy, Physiology, Function, and the Measurement of Efferent Effects in Humans

“…The presence of Na ϩ channels in outer-spiral-bundle fibers suggests that they may support action potentials (Hossain, Antic, Yang, et al, 2005). MOC fibers synapse directly on the cell bodies of the type II auditory nerve fibers and on the outer-spiral-bundle axons under OHCs (reviewed by Thiers, Burgess, & Nadol, 2002). Thus, MOC efferents appear to act, in part, through the outer-spiral-bundle network.…”

Cochlear efferents in developing adult and pathological conditions

“…One such CICR mechanism has also been identified in the developing IHCs and adult OHCs, involving the near-membrane postsynaptic cistern facing the efferent terminals, as calcium store (Lioudyno et al 2004;Fuchs 2014). In addition, GABA B metabotropic receptors may act on type II afferents to regulate OHC activity through reciprocal synapses (Thiers et al 2002(Thiers et al , 2008Maison et al 2009). It is thus tempting to propose that the medial efferent olivocochlear bundle controls cochlear amplification through hyperpolarization of OHCs (Murugasu and Russell 1996).…”

Frequency tuning of medial-olivocochlear-efferent acoustic reflexes in humans as functions of probe frequency

“…MOC fibers that innervate OHCs over 20% of cochlear length have not been found in cats and guinea pigs but were occasionally found in mice and rats (Robertson and Gummer 1985;Liberman and Brown 1986;Brown 1987;1989;Brown et al 1991;Warr and Boche 2003) and could possibly be present in humans. Another intriguing possibility is that the spread of MOC effect comes about not from the direct MOC innervation of OHCs but from the MOC innervation of Type II auditory afferents, which then change cochlear mechanical properties via Type II reciprocal synapses on OHCs (Thiers et al 2002;. Of these possibilities, a widening of MOC-fiber tuning seems the most likely, but more work is needed on this issue.…”