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Biophysical Journal 85:818-827 (2003)
© 2003 The Biophysical Society

Instabilities in the Transient Response of Muscle

Andrej Vilfan and Thomas Duke

Cavendish Laboratory, Cambridge CB3 0HE, United Kingdom

Correspondence: Address reprint requests to Andrej Vilfan, J. Stefan Institute, Jamova 39, 1000 Ljubljana, Slovenia. Tel.: 386-1-4773-900; Fax: 386-1-4263269; E-mail: andrej.vilfan{at}ijs.si.

We investigate the isometric transient response of muscle using a quantitative stochastic model of the actomyosin cycle based on the swinging lever-arm hypothesis. We first consider a single pair of filaments, and show that when values of parameters such as the lever-arm displacement and the cross-bridge elasticity are chosen to provide effective energy transduction, the T2 curve (the tension recovered immediately after a step displacement) displays a region of negative slope. If filament compliance and the discrete nature of the binding sites are taken into account, the negative slope is diminished, but not eliminated. This implies that there is an instability in the dynamics of individual half sarcomeres. However, when the symmetric nature of whole sarcomeres is taken into account, filament rearrangement becomes important during the transient: as tension is recovered, some half sarcomeres lengthen whereas others shorten. This leads to a flat T2 curve, as observed experimentally. In addition, we investigate the isotonic transient response and show that for a range of parameter values the model displays damped oscillations, as recently observed in experiments on single muscle fibers. We conclude that it is essential to consider the collective dynamics of many sarcomeres, rather than the dynamics of a single pair of filaments, when interpreting the transient response of muscle.




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