Dataset Information

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

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.

SUBMITTER: Ford MC

PROVIDER: S-EPMC4560803 | biostudies-literature | 2015 Aug

REPOSITORIES: biostudies-literature

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

Ford Marc C MC Alexandrova Olga O Cossell Lee L Stange-Marten Annette A Sinclair James J Kopp-Scheinpflug Conny C Pecka Michael M Attwell David D Grothe Benedikt B

Nature communications 20150825

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 ...[more]

PMID: 26305015

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Project description:The mechanisms that govern node of Ranvier organization, stability, and long-term maintenance remain to be fully elucidated. One of the molecular components of the node is the cytoskeletal scaffolding protein, ankyrin G (AnkG), which interacts with multiple members of the nodal complex. The role of AnkG in nodal organization and maintenance is still not clearly defined as to whether AnkG functions as an initial nodal organizer or whether it functions as a nodal stabilizer after the nodal complex has been assembled. Using a mouse model system, we report here that perinatal and juvenile neuronal ablation of AnkG has differential consequences on nodal stability. Early loss of AnkG creates immature nodes with abnormal morphology, which undergo accelerated destabilization within a month, resulting in rapid voltage-gated sodium (NaV) channel and βIV spectrin loss with reduced effects on neurofascin 186. On the other hand, late ablation of AnkG from established nodal complexes leads to slow but progressive nodal destabilization over 10 months, primarily affecting βIV spectrin, followed by NaV channels, with modest impact on neurofascin 186. We also show that ankyrin R and βI spectrin are not sufficient to prevent nodal disorganization after AnkG ablation. Additionally, nodal disorganization in both early and late AnkG mutants is accompanied by axonal pathology and neurological dysfunction. Together, our results suggest that AnkG plays an indispensable role in the maturation and long-term stabilization of the newly assembled nodal complex, and that loss of AnkG after nodal stabilization does not lead to rapid nodal disassembly but to loss of specific nodal components in a time-dependent manner.SIGNIFICANCE STATEMENT Nodes of Ranvier are the myelin-free gaps along myelinated axons that allow fast communication between neurons and their target cells by propagating action potentials in a saltatory manner. The cytoskeletal scaffolding protein ankyrin G (AnkG) has been thought to play an important role in node formation; however, its precise role in nodal assembly, stability, and maintenance is still not clear. By using spatiotemporal ablation of AnkG, we report its differential role in nodal maturation and stabilization. We show that early AnkG-deficient nodes fail to mature and undergo rapid destabilization. In contrast, nodes that assemble with AnkG are much more stable and undergo gradual disintegration with sequential loss of nodal components in the absence of AnkG.

Dataset Information

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

Publications

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

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