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Structural and Ultrastructural Changes to Type I Spiral Ganglion Neurons and Schwann Cells in the Deafened Guinea Pig Cochlea

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Abstract

Sensorineural hearing loss is commonly caused by damage to cochlear sensory hair cells. Coinciding with hair cell degeneration, the peripheral fibres of type I spiral ganglion neurons (SGNs) that normally form synaptic connections with the inner hair cell gradually degenerate. We examined the time course of these degenerative changes in type I SGNs and their satellite Schwann cells at the ultrastructural level in guinea pigs at 2, 6, and 12 weeks following aminoglycoside-induced hearing loss. Degeneration of the peripheral fibres occurred prior to the degeneration of the type I SGN soma and was characterised by shrinkage of the fibre followed by retraction of the axoplasm, often leaving a normal myelin lumen devoid of axoplasmic content. A statistically significant reduction in the cross-sectional area of peripheral fibres was evident as early as 2 weeks following deafening (p < 0.001, ANOVA). This was followed by a decrease in type I SGN density within Rosenthal’s canal that was statistically significant 6 weeks following deafening (p < 0.001, ANOVA). At any time point examined, few type I SGN soma were observed undergoing degeneration, implying that once initiated, soma degeneration was rapid. While there was a significant reduction in soma area as well as changes to the morphology of the soma, the ultrastructure of surviving type I SGN soma appeared relatively normal over the 12-week period following deafening. Satellite Schwann cells exhibited greater survival traits than their type I SGN; however, on loss of neural contact, they reverted to a non-myelinating phenotype, exhibiting an astrocyte-like morphology with the formation of processes that appeared to be searching for new neural targets. In 6- and 12-week deafened cochlea, we observed cellular interaction between Schwann cell processes and residual SGNs that distorted the morphology of the SGN soma. Understanding the response of SGNs, Schwann cells, and the complex relationship between them following aminoglycoside deafening is important if we are to develop effective therapeutic techniques designed to rescue SGNs.

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Acknowledgements

We are grateful for contributions made by Cong Ho, Anna Friedhuber, Marie Camilleri, Nicole Critch, Alison Neil, Stephen Asquith, Sarah Ellis, Maria Clarke, Prue Nielsen, and Ella Trang. The authors would like to acknowledge the funding support from the NIDCD (HHS-N-263-2007-00053-c and R01DC015031) and the NHMRC (GNT1064375). The Bionics Institute acknowledges the support it receives from the Victorian Government through its Operational Infrastructure Support Program.

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Authors and Affiliations

  1. The Bionics Institute, 384-388 Albert Street, East Melbourne, Victoria, 3002, Australia

    Andrew K. Wise, Remy Pujol, Thomas G. Landry, James B. Fallon & Robert K. Shepherd

  2. Department of Medical Bionics, University of Melbourne, Melbourne, Australia

    Andrew K. Wise, James B. Fallon & Robert K. Shepherd

  3. INSERM Unit 1051, INM, Montpellier, France

    Remy Pujol

  4. Department of Otolaryngology, University of Melbourne, Melbourne, Australia

    Andrew K. Wise & James B. Fallon

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Correspondence to Andrew K. Wise.

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The experimental procedures were approved by the Animal Research Ethics Committee of the Royal Victorian Eye and Ear Hospital in accordance with the National Institutes of Health Guidelines for the Care and Use of Laboratory Animals and conformed to the Code of Practice of the National Health and Medical Research Council of Australia.

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Role of Authors

All authors had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: AKW, RP, TGL, JBF, and RKS. Acquisition of data: AKW, RP, and TGL. Analysis and interpretation of data: AKW, RP, TGL, JBF, and RKS. Drafting of the manuscript: AKW, RP, TGL, JBF, and RKS. Critical revision of the manuscript for important intellectual content: AKW, RP, TGL, JBF, and RKS. Statistical analysis: AKW and TGL. Obtained funding: RKS and AKW. Study supervision: AKW.

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Wise, A.K., Pujol, R., Landry, T.G. et al. Structural and Ultrastructural Changes to Type I Spiral Ganglion Neurons and Schwann Cells in the Deafened Guinea Pig Cochlea. JARO 18, 751–769 (2017). https://doi.org/10.1007/s10162-017-0631-y

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