Developmental shaping of node of Ranvier geometry contributes to spike timing maturation in primary auditory afferents

Sound is encoded by action potentials in spiral ganglion neurons (SGNs), the auditory afferents from the cochlea. Rapid action potential transmission along SGNs is crucial for quick reactions to sounds, and binaural differences in action potential arrival time at the SGN output synapses enable sound...

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Veröffentlicht in:Cell reports (Cambridge) 2024-09, Vol.43 (9), p.114651, Article 114651
Hauptverfasser: Smith, Katie E., Lezmy, Jonathan, Arancibia-Cárcamo, I. Lorena, Bullen, Anwen, Jagger, Daniel J., Attwell, David
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Sprache:eng
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Zusammenfassung:Sound is encoded by action potentials in spiral ganglion neurons (SGNs), the auditory afferents from the cochlea. Rapid action potential transmission along SGNs is crucial for quick reactions to sounds, and binaural differences in action potential arrival time at the SGN output synapses enable sound localization based on interaural time or phase differences. SGN myelination increases conduction speed but other cellular changes may contribute. We show that nodes of Ranvier along peripherally and centrally directed SGN neurites form around hearing onset, but peri-somatic nodes mature later. There follows an adjustment of nodal geometry, notably a decrease in length and increase in diameter. Computational modeling predicts this increases conduction speed by >4%, and that four additional myelin wraps would be required on internodes to achieve the same conduction speed increase. We propose that nodal geometry changes optimize signal conduction for mature sound coding and decrease the energy needed for myelination. [Display omitted] •We characterize development of the myelinated axons from the mouse cochlea to the brain•Myelination of the soma in this pathway speeds action potential propagation significantly•Nodes of Ranvier change morphology during development to speed propagation•Speeding by node shape changes is equivalent to adding four more myelin wraps to the axon Spiral ganglion neurons (SGNs) transmit auditory information from the cochlea to the brain. Smith et al. show that, in the mouse, this transmission is speeded both by myelination of the SGN soma and by developmental changes in the node of Ranvier geometry.
ISSN:2211-1247
2211-1247
DOI:10.1016/j.celrep.2024.114651