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Tuning of Ranvier node and internode properties in myelinated axons to adjust action potential timing

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  • Marc C. Ford

    (Ludwig-Maximilians-Universität Munich
    Physiology and Pharmacology, University College London)

  • Olga Alexandrova

    (Ludwig-Maximilians-Universität Munich)

  • Lee Cossell

    (Physiology and Pharmacology, University College London)

  • Annette Stange-Marten

    (Ludwig-Maximilians-Universität Munich)

  • James Sinclair

    (Ludwig-Maximilians-Universität Munich)

  • Conny Kopp-Scheinpflug

    (Ludwig-Maximilians-Universität Munich)

  • Michael Pecka

    (Ludwig-Maximilians-Universität Munich)

  • David Attwell

    (Physiology and Pharmacology, University College London)

  • Benedikt Grothe

    (Ludwig-Maximilians-Universität Munich)

Abstract

Action potential timing is fundamental to information processing; however, its determinants are not fully understood. Here we report unexpected structural specializations in the Ranvier nodes and internodes of auditory brainstem axons involved in sound localization. Myelination properties deviated significantly from the traditionally assumed structure. Axons responding best to low-frequency sounds had a larger diameter than high-frequency axons but, surprisingly, shorter internodes. Simulations predicted that this geometry helps to adjust the conduction velocity and timing of action potentials within the circuit. Electrophysiological recordings in vitro and in vivo confirmed higher conduction velocities in low-frequency axons. Moreover, internode length decreased and Ranvier node diameter increased progressively along the distal axon segments, which simulations show was essential to ensure precisely timed depolarization of the giant calyx of Held presynaptic terminal. Thus, individual anatomical parameters of myelinated axons can be tuned to optimize pathways involved in temporal processing.

Suggested Citation

  • Marc C. Ford & Olga Alexandrova & Lee Cossell & Annette Stange-Marten & James Sinclair & Conny Kopp-Scheinpflug & Michael Pecka & David Attwell & Benedikt Grothe, 2015. "Tuning of Ranvier node and internode properties in myelinated axons to adjust action potential timing," Nature Communications, Nature, vol. 6(1), pages 1-14, November.
  • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms9073
    DOI: 10.1038/ncomms9073
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    Cited by:

    1. Jenea M. Bin & Daumante Suminaite & Silvia K. Benito-Kwiecinski & Linde Kegel & Maria Rubio-Brotons & Jason J. Early & Daniel Soong & Matthew R. Livesey & Richard J. Poole & David A. Lyons, 2024. "Importin 13-dependent axon diameter growth regulates conduction speeds along myelinated CNS axons," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Alberto Lazari & Piergiorgio Salvan & Lennart Verhagen & Michiel Cottaar & Daniel Papp & Olof Jens van der Werf & Bronwyn Gavine & James Kolasinski & Matthew Webster & Charlotte J. Stagg & Matthew F. , 2022. "A macroscopic link between interhemispheric tract myelination and cortico-cortical interactions during action reprogramming," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Mable Lam & Koji Takeo & Rafael G. Almeida & Madeline H. Cooper & Kathryn Wu & Manasi Iyer & Husniye Kantarci & J. Bradley Zuchero, 2022. "CNS myelination requires VAMP2/3-mediated membrane expansion in oligodendrocytes," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    4. Yide Zhang & Binglin Shen & Tong Wu & Jerry Zhao & Joseph C. Jing & Peng Wang & Kanomi Sasaki-Capela & William G. Dunphy & David Garrett & Konstantin Maslov & Weiwei Wang & Lihong V. Wang, 2022. "Ultrafast and hypersensitive phase imaging of propagating internodal current flows in myelinated axons and electromagnetic pulses in dielectrics," Nature Communications, Nature, vol. 13(1), pages 1-12, December.

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