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Spatial Gradients in the Size of Inner Hair Cell Ribbons Emerge Before the Onset of Hearing in Rats

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Abstract

The size and locations of pre-synaptic ribbons and glutamate receptors within and around inner hair cells are correlated with auditory afferent response features such as the spontaneous discharge rate (SR), threshold, and dynamic range of sound intensity representation (the so-called SR-groups). To test if the development of these spatial gradients requires experience with sound intensity, we quantified the size and spatial distribution of synaptic ribbons from the inner hair cells of neonatal rats before and after the onset of hearing (from post-natal day (P) 3 to P33). To quantify ribbon size, we used high resolution fluorescence confocal microscopy and 3-D reconstructions of immunolabeled ribbons. The size, density, and spatial distribution of ribbons changed during development. At P3, ribbons were densely clustered near the basal/modiolar face of the hair cell where low SR-groups preferentially contact adult hair cells. By P12, the disparity in ribbon count was less striking and ribbons were equally likely to occupy both faces. At all ages before P12, ribbons were larger on the modiolar face than on the pillar face. These differences initially grew larger with age but collapsed around the onset of hearing. Between P12 and P33, the spatial gradients remained small and began to re-emerge around P33. Even by P12, we did not find spatial gradients in the size of the post-synaptic glutamate receptors as is found on afferent terminals contacting adult inner hair cells. These results suggest that spatial gradients in ribbon size develop in the absence of sensory experience.

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Acknowledgements

This work was funded by the NIH-National Institute of Deafness and Communication Disorders grants RO3 DC012652 (to RK), P30 DC10743 (to the House Research Institute) and by the University of Southern California. We acknowledge Saya Yusa for her contribution to the preliminary studies that preceded this work. We thank Li Zhang for providing access to the confocal microscope, Seth Ruffins and USC Stem Cell Imaging Center for providing training and access to the Imaris Software and Laurel Fisher for advice on statistics. We thank Alexander Markowitz, Christopher Ventura, Neil Segil, and three anonymous reviewers for their valuable comments on this manuscript.

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  1. Rick and Tina Caruso Department of Otolaryngology & Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA, 90089, USA

    Radha Kalluri & Maya Monges-Hernandez

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  1. Radha Kalluri
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  2. Maya Monges-Hernandez
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Correspondence to Radha Kalluri.

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Kalluri, R., Monges-Hernandez, M. Spatial Gradients in the Size of Inner Hair Cell Ribbons Emerge Before the Onset of Hearing in Rats. JARO 18, 399–413 (2017). https://doi.org/10.1007/s10162-017-0620-1

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