Interactions between connected half-sarcomeres produce emergent mechanical behavior in a mathematical model of muscle

Most reductionist theories of muscle attribute a fiber's mechanical properties to the scaled behavior of a single half-sarcomere. Mathematical models of this type can explain many of the known mechanical properties of muscle but have to incorporate a passive mechanical component that becomes ap...

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Bibliographic Details
Published in:PLoS computational biology 2009-11, Vol.5 (11), p.e1000560-e1000560
Main Author: Campbell, Kenneth S
Format: Article
Language:English
Subjects:
Actins - physiology
Animal experimentation
Animals
Behavior
Biomechanical Phenomena - physiology
Biophysics/Theory and Simulation
Computational Biology/Systems Biology
Computer Simulation
Computer-generated environments
Experiments
Linear Models
Mathematical models
Mathematics
Models, Biological
Myofibrils - physiology
Myosins - physiology
Nonlinear Dynamics
Parameter estimation
Personal computers
Physiology/Motor Systems
Physiology/Muscle and Connective Tissue
Psoas Muscles - physiology
Rabbits
Sarcomeres - physiology
Software
Stress, Mechanical
Studies
System theory
Systems Biology - methods
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Summary:Most reductionist theories of muscle attribute a fiber's mechanical properties to the scaled behavior of a single half-sarcomere. Mathematical models of this type can explain many of the known mechanical properties of muscle but have to incorporate a passive mechanical component that becomes approximately 300% stiffer in activating conditions to reproduce the force response elicited by stretching a fast mammalian muscle fiber. The available experimental data suggests that titin filaments, which are the mostly likely source of the passive component, become at most approximately 30% stiffer in saturating Ca2+ solutions. The work described in this manuscript used computer modeling to test an alternative systems theory that attributes the stretch response of a mammalian fiber to the composite behavior of a collection of half-sarcomeres. The principal finding was that the stretch response of a chemically permeabilized rabbit psoas fiber could be reproduced with a framework consisting of 300 half-sarcomeres arranged in 6 parallel myofibrils without requiring titin filaments to stiffen in activating solutions. Ablation of inter-myofibrillar links in the computer simulations lowered isometric force values and lowered energy absorption during a stretch. This computed behavior mimics effects previously observed in experiments using muscles from desmin-deficient mice in which the connections between Z-disks in adjacent myofibrils are presumably compromised. The current simulations suggest that muscle fibers exhibit emergent properties that reflect interactions between half-sarcomeres and are not properties of a single half-sarcomere in isolation. It is therefore likely that full quantitative understanding of a fiber's mechanical properties requires detailed analysis of a complete fiber system and cannot be achieved by focusing solely on the properties of a single half-sarcomere.
ISSN:1553-7358
1553-734X
1553-7358
DOI:10.1371/journal.pcbi.1000560