Longitudinal and transversal propagation of excitation along the tubular system of rat fast-twitch muscle fibres studied by high speed confocal microscopy

Edwards, Joshua N., Cully, Tanya R., Shannon, Thomas R., Stephenson, D. George and Launikonis, Bradley S. (2012) Longitudinal and transversal propagation of excitation along the tubular system of rat fast-twitch muscle fibres studied by high speed confocal microscopy. Journal of Physiology, 590 3: 475-491. doi:10.1113/jphysiol.2011.221796

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Author Edwards, Joshua N.
Cully, Tanya R.
Shannon, Thomas R.
Stephenson, D. George
Launikonis, Bradley S.
Title Longitudinal and transversal propagation of excitation along the tubular system of rat fast-twitch muscle fibres studied by high speed confocal microscopy
Journal name Journal of Physiology   Check publisher's open access policy
ISSN 0022-3751
1469-7793
Publication date 2012-02-01
Year available 2011
Sub-type Article (original research)
DOI 10.1113/jphysiol.2011.221796
Volume 590
Issue 3
Start page 475
End page 491
Total pages 17
Place of publication Oxford, United Kingdom
Publisher Wiley-Blackwell Publishing
Collection year 2013
Language eng
Formatted abstract
Mammalian skeletal muscle fibres possess a tubular (t-) system that consists of regularly spaced transverse elements which are also connected in the longitudinal direction. This tubular network provides a pathway for the propagation of action potentials (APs) both radially and longitudinally within the fibre, but little is known about the actual radial and longitudinal AP conduction velocities along the tubular network in mammalian skeletal muscle fibres. The aim of this study was to track AP propagation within the t-system network of fast-twitch rat muscle fibres with high spatio-temporal resolution when the t-system was isolated from the surface membrane. For this we used high speed confocal imaging of AP-induced Ca2+ release in contraction-suppressed mechanically skinned fast-twitch fibres where the t-system can be electrically excited in the absence of the surface membrane. Supramaximal field pulses normally elicited a synchronous AP-induced release of Ca2+ along one side of the fibre axis which propagated uniformly across the fibre. In some cases up to 80 or more adjacent transverse tubules failed to be excited by the field pulse, while adjacent areas responded with normal Ca2+ release. In these cases a continuous front of Ca2+ release with an angle to the scanning line was observed due to APs propagating longitudinally. From these observations the radial/transversal and longitudinal AP conduction velocities along the tubular network deeper in the fibre under our conditions (19 ± 1°C) ranged between 8 and 11 μm ms−1 and 5 to 9 μm ms−1, respectively, using different methods of estimation. The longitudinal propagation of APs appeared to be markedly faster closer to the edge of the fibre, in agreement with the presence of dense longitudinal connections immediately below the surface of the fibre and more sparse connections at deeper planes within the fibre. During long trains of closely spaced field pulses the AP-elicited Ca2+ releases became non-synchronous along the fibre axis. This is most likely caused by local tubular K+ accumulation that produces local depolarization and local slowing of AP propagation. Longitudinally propagating APs may reduce such inhomogeneities by exciting areas of delayed AP onset. Clearly, the longitudinal tubular pathways within the fibre for excitation are used as a safety mechanism in situations where a local depolarization obstructs immediate excitation from the sarcolemma. Results obtained from this study also provide an explanation for the pattern of contractures observed in rippling muscle disease.
Q-Index Code C1
Q-Index Status Confirmed Code
Institutional Status UQ
Additional Notes Published online before print December 12, 2011

Document type: Journal Article
Sub-type: Article (original research)
Collections: Official 2013 Collection
School of Biomedical Sciences Publications
 
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