A TEM study was performed on freshly fixed human spiral ganglions (HSG) collected during skull base surgery. This technique gives well preserved tissue for ultrastructural analysis. Unlike spiral ganglion cells in mature animals so far studied, most HSG cells lack a myelin coat, but are surrounded by a thin rim of Schwann cell (SC) cytoplasm. In the region of maximal innervation density (upper basal and middle turn), HSG cells were frequently ensheathed by the same Schwann cell, forming a "unit-like" structure. In this region the cells often showed signs of physical interaction where the SCs were frequently incompletely developed ("gaps") so that the cell membranes of adjacent ganglion cells (sometimes as many as four in one section plane) were in direct apposition. In one thin section as many as 20 of 100 ganglion cells were found to face the cell membrane, at any point, of an adjacent cell. At these "gaps" in the SC, complexes of cell membrane specializations occurred between individual HSG cells. The same nerve junctions were also found between unmyelinated nerve fibres and the body of large ganglion cells. Our findings may challenge the view that afferent information in the acoustic nerve is conveyed uninterrupted to the CNS at the level of the spiral ganglion.

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Background: The human auditory nerve contains 30,000 nerve fibers (NFs) that relay complex speech information to the brain with spectacular acuity. How speech is coded and influenced by various conditions is not known. It is also uncertain whether human nerve signaling involves exclusive proteins and gene manifestations compared with that of other species. Such information is difficult to determine due to the vulnerable, “esoteric,” and encapsulated human ear surrounded by the hardest bone in the body. We collected human inner ear material for nanoscale visualization combining transmission electron microscopy (TEM), super-resolution structured illumination microscopy (SR-SIM), and RNA-scope analysis for the first time. Our aim was to gain information about the molecular instruments in human auditory nerve processing and deviations, and ways to perform electric modeling of prosthetic devices.Material and Methods: Human tissue was collected during trans-cochlear procedures to remove petro-clival meningioma after ethical permission. Cochlear neurons were processed for electron microscopy, confocal microscopy (CM), SR-SIM, and high-sensitive in situ hybridization for labeling single mRNA transcripts to detect ion channel and transporter proteins associated with nerve signal initiation and conductance.Results: Transport proteins and RNA transcripts were localized at the subcellular level. Hemi-nodal proteins were identified beneath the inner hair cells (IHCs). Voltage-gated ion channels (VGICs) were expressed in the spiral ganglion (SG) and axonal initial segments (AISs). Nodes of Ranvier (NR) expressed Nav1.6 proteins, and encoding genes critical for inter-cellular coupling were disclosed.Discussion: Our results suggest that initial spike generators are located beneath the IHCs in humans. The first NRs appear at different places. Additional spike generators and transcellular communication may boost, sharpen, and synchronize afferent signals by cell clusters at different frequency bands. These instruments may be essential for the filtering of complex sounds and may be challenged by various pathological conditions.

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A three-dimensional model of the cell membrane contact area was made between two large spiral ganglion cells (type 1 cells) from a cell cluster in a normal human cochlea. The freshly fixed cochlea had been removed during skull base surgery, processed, and sectioned for ultrastructural analysis. 400 consecutive serial thin sections were prepared from the apical portion where the nerve cell density is high and cell clusters are numerous. A cell cluster is defined as a conglomerate of two or more nerve cell bodies, surrounded by common Schwann cells. Direct physical contact between ganglion cell membranes (ephapse) was possible, in places where adjacent cells lacked a separating Schwann cell layer (gaps). One such gap was selected, and observed in 57 of 90 consecutive sections. Membrane specializations, observed in 36 sections, were found to be of principally three different types namely: (1) symmetrical, (2) asymmetrical, and (3) asymmetrical subplasmalemmal. The functional properties of these membrane specializations are still unknown. Asymmetrical densities were seen on one or other of the two cell membranes. A graphic model based on serial thin sections was made to illustrate the gap area. Superficially membrane specializations were seen to form small disk-like areas varying in size, the largest measuring 3 x 2 microm. It is speculated whether these unique formations between human spiral ganglion cells, which have not been observed in other species, may constitute interactive electrotonic or ephaptic transmission pathways. These may be in the low-frequency region and may increase plasticity and signal acuity related to the coding of speech.