Abstract
Ribbon synapses of cochlear hair cells undergo pruning and maturation before the hearing onset. In the central nervous system (CNS), synaptic pruning was mediated by microglia, the brain-resident macrophages, via activation of the complement system. Whether a similar mechanism regulates ribbon synapse pruning is currently unknown. In this study, we report that the densities of cochlear macrophages surrounding hair cells were highest at around P8, corresponding well to the completion of ribbon synaptic pruning by P8–P9. Surprisingly, using multiple genetic mouse models, we found that postnatal pruning of the ribbon synapses and auditory functions were unaffected by the knockout of the complement receptor 3 (CR3) or by ablations of macrophages expressing either LysM or Cx3cr1. Our results suggest that unlike microglia in the CNS, macrophages in the cochlea do not mediate pruning of the cochlear ribbon synapses.
Highlights
Hearing involves neural transmission mediated by the ribbon synapses between the auditory hair cells and spiral ganglion neurons (SGNs)
These results indicate that while cochlear synapses continued to refine and mature until hearing onset, the pruning of ribbon synapses was largely completed by P8 in the mouse cochlea
Ribbon synapses play a crucial role in transmitting soundevoked signals from the sensory hair cells to the SGNs
Summary
Hearing involves neural transmission mediated by the ribbon synapses between the auditory hair cells and spiral ganglion neurons (SGNs). From P6 to P12, the immature synapses would either be enhanced or eliminated, leading to about a 50% reduction in the total number of synapses (Delacroix and Malgrange, 2015; Brown et al, 2017) This process, termed synaptic pruning, involves neurite refinement and retraction of the immature SGN terminals (Barclay et al, 2011). As the ribbon synapses mature at the 2nd postnatal week, the Cav1.3-dependent Ca2+ current reduces, which contributes to increased exocytosis. Such maturation of synaptic exocytosis is important for encoding continuous and finely graded signals necessary for the temporal acuity and fidelity of acoustic information (Brandt et al, 2005; Frank et al, 2010; Delacroix and Malgrange, 2015)
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