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Open Access Research article

Synaptic profiles during neurite extension, refinement and retraction in the developing cochlea

Lin-Chien Huang135, Meagan Barclay13, Kevin Lee13, Saša Peter13, Gary D Housley4, Peter R Thorne123 and Johanna M Montgomery13*

Author Affiliations

1 Department of Physiology, Faculty of Medical and Health Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand

2 Section of Audiology, Faculty of Medical and Health Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand

3 Centre for Brain Research, Faculty of Medical and Health Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand

4 Department of Physiology & Translational Neuroscience Facility, School of Medical Sciences, University of New South Wales, Sydney, NSW, 2052, Australia

5 Present address: Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA, 92037, USA

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Neural Development 2012, 7:38  doi:10.1186/1749-8104-7-38

Published: 7 December 2012

Abstract

Background

During development, excess synapses form between the central and peripheral nervous systems that are then eliminated to achieve correct connectivity. In the peripheral auditory system, the developing type I spiral ganglion afferent fibres undergo a dramatic re-organisation, initially forming connections with both sensory inner hair cells (IHCs) and outer hair cells (OHCs). The OHC connections are then selectively eliminated, leaving sparse innervation by type II afferent fibres, whilst the type I afferent synapses with IHCs are consolidated.

Results

We examined the molecular makeup of the synaptic contacts formed onto the IHCs and OHCs during this period of afferent fibre remodelling. We observed that presynaptic ribbons initially form at all the afferent neurite contacts, i.e. not only at the expected developing IHC-type I fibre synapses but also at OHCs where type I fibres temporarily contact. Moreover, the transient contacts forming onto OHCs possess a broad set of pre- and postsynaptic proteins, suggesting that functional synaptic connections are formed prior to the removal of type I fibre innervation. AMPA-type glutamate receptor subunits were transiently observed at the base of the OHCs, with their downregulation occurring in parallel with the withdrawal of type I fibres, dispersal of presynaptic ribbons, and downregulation of the anchoring proteins Bassoon and Shank. Conversely, at developing type I afferent IHC synapses, the presence of pre- and postsynaptic scaffold proteins was maintained, with differential plasticity in AMPA receptor subunits observed and AMPA receptor subunit composition changing around hearing onset.

Conclusions

Overall our data show a differential balance in the patterns of synaptic proteins at developing afferent IHC versus OHC synapses that likely reflect their stable versus transient fates.

Keywords:
Cochlea; Synapse; Glutamate receptors; Synaptic ribbons; Hair cells; Spiral ganglion