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Cochlear Neuron and Ribbon Synapse: Development, Degeneration, Repair and Regeneration

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Spiral ganglion neurons (SGNs) are bipolar primary neurons in the cochlea that transmit auditory information from the sensory hair cells in the organ of Corti to the brain. There are two types of SGNs: Type I (95%) innervate the inner hair cells (IHCs) and Type II (5%) connect to the outer hair cells in the ...

Spiral ganglion neurons (SGNs) are bipolar primary neurons in the cochlea that transmit auditory information from the sensory hair cells in the organ of Corti to the brain. There are two types of SGNs: Type I (95%) innervate the inner hair cells (IHCs) and Type II (5%) connect to the outer hair cells in the organ of Corti. Each Type I SGN makes one synapse with one IHC but each IHC is innervated by ~10-20 Type I SGNs in rodents. Each of these synapses consists of a single postsynaptic density containing numerous glutamate receptors apposed to a presynaptic ribbon-type active zone of neurotransmitter (glutamate)-filled vesicles in the IHC.

Research over the last three decades has shown that loss of hair cells and/or SGNs is the leading cause of acquired sensorineural hearing loss that affects the quality of life of millions of people. Even if hair cell function is intact, hearing can be impaired by the loss of ribbon synapses between IHCs and SGNs. Such synaptopathy leads to gradual degeneration and ultimately death of SGNs and can occur due to noise overexposure, aging, or certain ototoxic drugs. The consequences of synaptic loss include auditory perceptual dysfunctions leading to difficulty in speech recognition and listening in noisy environments and may be key to the generation of tinnitus or hyperacusis. Moreover, absence of functional SGNs may limit the performance of hearing aids and cochlear implants or any future hair cell regeneration strategies. Thus, the development of methodologies that could be used to maintain, repair, and regenerate SGNs and their synapses on IHCs in damaged ears have significant implications for advancement in cochlear prosthetic technologies and the treatment of hidden-hearing loss, tinnitus, and hyperacusis.

Noise-induced synaptopathy is attributed to excitotoxic damage caused by excessive release of glutamate from overstimulated IHCs and activation of glutamate receptors present on afferent nerve terminals of SGNs. However, whether same mechanism contributes to age- and drug-related synaptopathy and neuropathy is unknown. The downstream mechanism(s) of glutamate-induced excitotoxicity, the reasons for selective susceptibility of a subset of synapses, and mechanism(s) of gradual and heterogeneous degeneration and loss of SGNs remain under investigation. In certain animal species, noise-damaged synapses can undergo spontaneous repair but the relevant cellular and molecular mechanisms remain unidentified. Such studies could be critical in identifying novel strategies to allow neurite outgrowth and repair damaged synapses. Unlike in the brain, the contribution(s) of non-neuronal cells such as Schwann cells, satellite-glial cells, immune cells, pericytes, fibrocytes, and mesenchyme towards SGN-synapse, axon and soma degeneration, maintenance, repair or regeneration is still largely unexplored.

This Research Topic encourages Original Research and Review articles focused on neuronal and non-neuronal cellular and molecular mechanisms of development, degeneration, preservation, repair, and regeneration of SGNs and their synapses on IHC. Clinical and basic research done on humans and animals and focused on transcriptomics, proteomics, and metabolomics is welcome. The aim of this Research Topic is to present comprehensive knowledge on current and emerging advancements on spiral ganglion neurons and cochlear ribbon synapses.  

The covering image represents a middle turn of an adult mouse cochlea showing spiral ganglion neuron somas and axons in magenta and nuclei in green. Credit: Tejbeer Kaur, Creighton University


Keywords: Spiral ganglion neuron, cochlear ribbon synapse, nerve regeneration, synaptogenesis, hearing loss


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