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 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.

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Publication Details

Journal
Cell Reports
Published
2024-08-23
DOI
https://doi.org/10.1016/j.celrep.2024.114651
Citations
4
Primary Topic
Hearing Loss and Rehabilitation
Type
article
Field-Weighted Citation Impact
1.37

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article

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

I. Lorena Arancibia‐Cárcamo, Jonathan Lezmy, David Attwell, Anwen Bullen et al.
4 citations
Cell Reports
Hearing Loss and Rehabilitation
1.37
article

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

I. Lorena Arancibia‐Cárcamo, Jonathan Lezmy, David Attwell, Anwen Bullen, Daniel J. Jagger, Katie E. Smith
article en
4 citations

Abstract

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.

Cell ReportsVol. 43(9)
Smith Institute (GB), The Francis Crick Institute (GB), University College London (GB)
Biotechnology and Biological Sciences Research Council
Zero hunger
Openalex Percentile: Top 20%
Hearing Loss and Rehabilitation
1.37
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Developmental shaping of node of Ranvier geometry contributes to spike timing maturation in primary auditory afferents — I. Lorena Arancibia‐Cárcamo, Jonathan Lezmy, et al. · Cell Reports (2024) | TGRS Research Map | TGRS