Treffer: Regional heterogeneities of oligodendrocytes underlie biased Ranvier node spacing along single axons in sound localization circuit.
Title:
Regional heterogeneities of oligodendrocytes underlie biased Ranvier node spacing along single axons in sound localization circuit.
Authors:
Egawa R; Department of Cell Physiology, Graduate School of Medicine, Nagoya University, Nagoya, Japan., Hiraga K; Department of Cell Physiology, Graduate School of Medicine, Nagoya University, Nagoya, Japan., Matsui R; Department of Biological Sciences, Graduate School of Medicine, Kyoto University, Sakyo-ku, Kyoto, Japan., Watanabe D; Department of Biological Sciences, Graduate School of Medicine, Kyoto University, Sakyo-ku, Kyoto, Japan., Kuba H; Department of Cell Physiology, Graduate School of Medicine, Nagoya University, Nagoya, Japan.
Source:
ELife [Elife] 2025 Dec 23; Vol. 14. Date of Electronic Publication: 2025 Dec 23.
Publication Type:
Journal Article
Language:
English
Journal Info:
Publisher: eLife Sciences Publications, Ltd Country of Publication: England NLM ID: 101579614 Publication Model: Electronic Cited Medium: Internet ISSN: 2050-084X (Electronic) Linking ISSN: 2050084X NLM ISO Abbreviation: Elife Subsets: MEDLINE
Imprint Name(s):
Original Publication: Cambridge, UK : eLife Sciences Publications, Ltd., 2012-
MeSH Terms:
References:
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Proc Natl Acad Sci U S A. 2007 Jan 16;104(3):1027-32. (PMID: 17209010)
Nat Rev Neurosci. 2021 Jan;22(1):7-20. (PMID: 33239761)
Biol Cybern. 2008 Jun;98(6):541-59. (PMID: 18491165)
J Neurol Sci. 1980 Feb;45(1):29-41. (PMID: 7359166)
J Neurol Sci. 1995 Nov;133(1-2):119-27. (PMID: 8583214)
J Neurosci. 2005 Feb 23;25(8):1924-34. (PMID: 15728832)
Dev Neurobiol. 2018 Feb;78(2):68-79. (PMID: 28834358)
Neuron. 2021 Apr 21;109(8):1258-1273. (PMID: 33621477)
J Neurosci. 1992 May;12(5):1698-708. (PMID: 1578264)
Cell Rep. 2016 Apr 26;15(4):761-773. (PMID: 27149850)
Nat Methods. 2021 Apr;18(4):374-377. (PMID: 33795878)
Nature. 1997 Apr 17;386(6626):724-8. (PMID: 9109490)
Prog Neurobiol. 1993 Mar;40(3):319-84. (PMID: 8441812)
Front Neural Circuits. 2013 Oct 11;7:162. (PMID: 24130520)
Nat Rev Neurosci. 2015 Dec;16(12):756-67. (PMID: 26585800)
Mech Dev. 2000 Dec;99(1-2):143-8. (PMID: 11091082)
J Neurosci. 2023 Jan 18;43(3):359-372. (PMID: 36639893)
PLoS One. 2012;7(11):e48730. (PMID: 23144948)
Front Cell Dev Biol. 2022 Oct 24;10:1030486. (PMID: 36393856)
J Comp Physiol Psychol. 1948 Feb;41(1):35-9. (PMID: 18904764)
Elife. 2019 Nov 19;8:. (PMID: 31742557)
J Neurosci. 2024 Jan 3;44(1):. (PMID: 37989591)
Mol Cell Neurosci. 2000 Dec;16(6):740-53. (PMID: 11124894)
J Neurosci. 1990 Oct;10(10):3227-46. (PMID: 2213141)
Nat Commun. 2020 Oct 30;11(1):5497. (PMID: 33127910)
Science. 2014 Apr 18;344(6181):319-24. (PMID: 24744380)
Front Cell Neurosci. 2021 Oct 08;15:721376. (PMID: 34690700)
Nat Neurosci. 2013 Oct;16(10):1370-2. (PMID: 23995069)
J Comp Neurol. 2007 May 20;502(3):400-13. (PMID: 17366608)
Cold Spring Harb Perspect Biol. 2015 Sep 09;8(3):a020495. (PMID: 26354894)
Science. 1967 Mar 31;155(3770):1692-3. (PMID: 6020297)
Proc Natl Acad Sci U S A. 2015 Jan 20;112(3):E321-8. (PMID: 25561543)
J Biol Chem. 2002 Aug 9;277(32):28996-9004. (PMID: 12036953)
J Neurosci. 2014 Apr 2;34(14):4914-9. (PMID: 24695710)
J Morphol. 1951 Jan;88(1):49-92. (PMID: 24539719)
Dev Cell. 2015 Feb 23;32(4):459-68. (PMID: 25710532)
Nat Neurosci. 2014 Dec;17(12):1673-81. (PMID: 25362471)
Nat Neurosci. 2015 May;18(5):628-30. (PMID: 25849985)
J Neurosci. 2010 Jan 6;30(1):70-80. (PMID: 20053889)
Dev Neurosci. 2003 Mar-Aug;25(2-4):116-26. (PMID: 12966210)
J Neurocytol. 1998 Apr;27(4):271-80. (PMID: 10640185)
J Neurosci. 2018 Mar 21;38(12):2967-2980. (PMID: 29439165)
J Neurosci. 1996 Aug 15;16(16):4914-22. (PMID: 8756423)
J Neurosci Methods. 2008 Mar 30;169(1):55-64. (PMID: 18206245)
J Exp Biol. 2022 Mar 1;225(5):. (PMID: 35156129)
Nat Methods. 2012 Jun 28;9(7):676-82. (PMID: 22743772)
Glia. 2024 Apr;72(4):794-808. (PMID: 38174817)
Science. 2020 Dec 18;370(6523):. (PMID: 33335032)
Front Cell Neurosci. 2022 Oct 13;16:1025012. (PMID: 36313617)
Science. 2014 May 2;344(6183):1252304. (PMID: 24727982)
Cell. 2014 Jan 16;156(1-2):277-90. (PMID: 24439382)
Curr Protoc Neurosci. 2019 Apr;87(1):e64. (PMID: 30791212)
Science. 2021 Nov 12;374(6569):eaba6905. (PMID: 34618550)
J Neurosci. 2013 May 29;33(22):9402-7. (PMID: 23719808)
Neuron. 2005 Jan 6;45(1):55-67. (PMID: 15629702)
Neuron. 2020 Aug 19;107(4):617-630.e6. (PMID: 32559415)
Nat Neurosci. 2024 Aug;27(8):1545-1554. (PMID: 38849524)
Elife. 2018 Dec 19;7:. (PMID: 30566077)
Curr Biol. 2016 Jun 6;26(11):1447-55. (PMID: 27161502)
Nature. 2006 Dec 21;444(7122):1069-72. (PMID: 17136099)
Front Cell Neurosci. 2022 Nov 14;16:1041853. (PMID: 36451655)
Nature. 2012 Jul 12;487(7406):235-8. (PMID: 22722837)
Neurosci Lett. 2020 Jan 10;715:134593. (PMID: 31678373)
Curr Biol. 2015 Sep 21;25(18):2411-6. (PMID: 26320951)
J Neurosci. 2000 Jul 1;20(13):4864-70. (PMID: 10864943)
Glia. 2016 Apr;64(4):487-94. (PMID: 26556176)
Proc Natl Acad Sci U S A. 2012 Jan 24;109(4):1299-304. (PMID: 22160722)
Neuron. 2013 May 8;78(3):469-82. (PMID: 23664614)
Cell Rep. 2022 Feb 15;38(7):110366. (PMID: 35172135)
Nat Commun. 2015 Aug 25;6:8073. (PMID: 26305015)
PLoS One. 2017 Jan 6;12(1):e0169611. (PMID: 28060929)
Physiol Behav. 2005 Oct 15;86(3):297-305. (PMID: 16202434)
Science. 2016 Jun 10;352(6291):1326-1329. (PMID: 27284195)
PLoS Biol. 2019 Mar 27;17(3):e3000202. (PMID: 30917112)
Glia. 2019 Oct;67(10):1797-1805. (PMID: 30968471)
Proc Natl Acad Sci U S A. 2011 Jan 25;108(4):1531-6. (PMID: 21205896)
J Neurosci. 2020 Aug 26;40(35):6709-6721. (PMID: 32719016)
Proc Natl Acad Sci U S A. 2007 Jan 16;104(3):1027-32. (PMID: 17209010)
Nat Rev Neurosci. 2021 Jan;22(1):7-20. (PMID: 33239761)
Biol Cybern. 2008 Jun;98(6):541-59. (PMID: 18491165)
J Neurol Sci. 1980 Feb;45(1):29-41. (PMID: 7359166)
J Neurol Sci. 1995 Nov;133(1-2):119-27. (PMID: 8583214)
J Neurosci. 2005 Feb 23;25(8):1924-34. (PMID: 15728832)
Dev Neurobiol. 2018 Feb;78(2):68-79. (PMID: 28834358)
Neuron. 2021 Apr 21;109(8):1258-1273. (PMID: 33621477)
J Neurosci. 1992 May;12(5):1698-708. (PMID: 1578264)
Cell Rep. 2016 Apr 26;15(4):761-773. (PMID: 27149850)
Nat Methods. 2021 Apr;18(4):374-377. (PMID: 33795878)
Nature. 1997 Apr 17;386(6626):724-8. (PMID: 9109490)
Grant Information:
22K19358 Japan Science and Technology Agency; 23K05986 Japan Science and Technology Agency; 17K07039 Japan Science and Technology Agency; 19H04747 Japan Science and Technology Agency; 24H00584 Japan Science and Technology Agency; 20K15915 Japan Science and Technology Agency; 21H02577 Japan Science and Technology Agency; United Kingdom WT_ Wellcome Trust
Contributed Indexing:
Keywords: 3D morphometry; brainstem auditory circuit; chicken; interaural time difference; internodal length; neuroscience; oligodendrocyte heterogeneity; oligodendrogenesis
Entry Date(s):
Date Created: 20251223 Date Completed: 20251223 Latest Revision: 20251226
Update Code:
20251226
PubMed Central ID:
PMC12726825
DOI:
10.7554/eLife.106415
PMID:
41432370
Database:
MEDLINE
Weitere Informationen
Spacing of Ranvier nodes along myelinated axons is a critical determinant of conduction velocity, influencing spike arrival timing and hence neural circuit function. In the chick brainstem auditory circuit, the pattern of nodal spacing varies regionally along single axons, enabling precise binaural integration for sound localization. Using this model, we investigated the potential factors underlying the biased nodal spacing pattern. 3D morphometry revealed that these axons were almost fully myelinated by oligodendrocytes exhibiting distinct morphologies and cell densities across regions after hearing onset. The structure of axons did not affect internodal length. Inhibiting vesicular release from the axons did not affect internodal length or oligodendrocyte morphology, but caused unmyelinated segments on the axons by suppressing oligodendrogenesis near the presynaptic terminals. These results suggest that the regional heterogeneity in the intrinsic properties of oligodendrocytes is a prominent determinant of the biased nodal spacing pattern in the sound localization circuit, while activity-dependent signaling supports the pattern by ensuring adequate oligodendrocyte density. Our findings highlight the importance of oligodendrocyte heterogeneity in fine-tuning neural circuit function.
(© 2025, Egawa et al.)
RE, KH, RM, DW, HK No competing interests declared