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Force response to rapid length change during contraction and rigor in skinned smooth muscle of guinea-pig taenia coli

Arheden, Håkan LU and Hellstrand, Per LU (1991) In Journal of Physiology 442. p.601-630
Abstract
1. Mechanical transients in fibre bundles of skinned smooth muscle of guinea-pig taenia coli at 21-22 degrees C were investigated by recording tension responses to length changes of up to 9%, complete within 0.3 ms. 2. The length-force relationship, recorded continuously during rapid stretch of a Ca(2+)-activated contracted muscle, was linear up to at least 2.5 times the isometric force, corresponding to a stretch of about 1%. The slope of the relationship (stiffness) increased with the velocity of stretch. 3. During rapid release (about 120 muscle lengths s-1) the length-force relationship was linear down to about 50% of the initial isometric force, reached at about 80 microseconds after the beginning of the release. At lower force the... (More)
1. Mechanical transients in fibre bundles of skinned smooth muscle of guinea-pig taenia coli at 21-22 degrees C were investigated by recording tension responses to length changes of up to 9%, complete within 0.3 ms. 2. The length-force relationship, recorded continuously during rapid stretch of a Ca(2+)-activated contracted muscle, was linear up to at least 2.5 times the isometric force, corresponding to a stretch of about 1%. The slope of the relationship (stiffness) increased with the velocity of stretch. 3. During rapid release (about 120 muscle lengths s-1) the length-force relationship was linear down to about 50% of the initial isometric force, reached at about 80 microseconds after the beginning of the release. At lower force the length-force relationship was concave upwards. The linear portion extrapolated to zero force at about -0.008 muscle lengths. In large releases the length-force plot approached the force baseline under an acute angle, and negative force was transiently exerted. 4. When the muscle was stretched back to the initial length after a shortening step, force transiently rose above the isometric force, but decayed back within a few milliseconds. Stiffness at the time of restretch was compared with that in the initial shortening step by plotting force vs. length, and was found to be decreased to 63% within 0.3 ms of a step to zero force. Stiffness decreased further with time at zero force, and after 256 ms was about 29% of the isometric value. 5. In rigor, caused by the introduction of ATP-free solution during the plateau of isometric contraction, fibre tension decreased to about 30% of the active tension, whereas stiffness relative to force increased; 82% of the initial stiffness in rigor was detected in a restretch immediately after a shortening step, decreasing to 59% at 256 ms. When the fibre was activated at suboptimal [Ca2+] to cause the same force as in rigor, stiffness was lower than in rigor and decreased more after a release. 6. After completion of a release-stretch cycle, stiffness was rapidly restored to the same value as in isometric contraction. Test stretches at different points in time after completion of the cycle revealed that most of the stiffness had been restored within 1 ms of the restretch, occurring concomitantly with a decay in force.7. The shape of the length-force relationship during a release was analysed using a model consisting of a linear (cross-bridge) elasticity in series with an exponential (passive) elasticity and assuming no detachment of cross-bridges during release. In rigor the exponential element contributed 40% of the total compliance of the fibre. The model, although closely fitting the data, could not account for the results using an exponential elasticity with unaltered properties during activation at optimal and suboptimal [Ca2"] and in rigor.

8. The results suggest rapid detachment of some of the attached cross-bridges during and after a shortening step to slack length. Detachment of strongly bound cross-bridges may occur during a restretch, if it causes a strain on the attached crossbridges exceeding their working range. During the restretch, and on return to isometric contraction after the restretch, cross-bridges rapidly reattach in strongly

bound configurations. (Less)
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published
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Journal of Physiology
volume
442
pages
601 - 630
publisher
The Physiological Society
external identifiers
  • pmid:1798045
  • scopus:0026063315
ISSN
1469-7793
language
English
LU publication?
yes
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6b84af66-a12a-44b7-9c00-d7a47b31a477 (old id 1105931)
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http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1179907
date added to LUP
2008-08-04 14:17:36
date last changed
2017-01-01 07:23:20
@article{6b84af66-a12a-44b7-9c00-d7a47b31a477,
  abstract     = {1. Mechanical transients in fibre bundles of skinned smooth muscle of guinea-pig taenia coli at 21-22 degrees C were investigated by recording tension responses to length changes of up to 9%, complete within 0.3 ms. 2. The length-force relationship, recorded continuously during rapid stretch of a Ca(2+)-activated contracted muscle, was linear up to at least 2.5 times the isometric force, corresponding to a stretch of about 1%. The slope of the relationship (stiffness) increased with the velocity of stretch. 3. During rapid release (about 120 muscle lengths s-1) the length-force relationship was linear down to about 50% of the initial isometric force, reached at about 80 microseconds after the beginning of the release. At lower force the length-force relationship was concave upwards. The linear portion extrapolated to zero force at about -0.008 muscle lengths. In large releases the length-force plot approached the force baseline under an acute angle, and negative force was transiently exerted. 4. When the muscle was stretched back to the initial length after a shortening step, force transiently rose above the isometric force, but decayed back within a few milliseconds. Stiffness at the time of restretch was compared with that in the initial shortening step by plotting force vs. length, and was found to be decreased to 63% within 0.3 ms of a step to zero force. Stiffness decreased further with time at zero force, and after 256 ms was about 29% of the isometric value. 5. In rigor, caused by the introduction of ATP-free solution during the plateau of isometric contraction, fibre tension decreased to about 30% of the active tension, whereas stiffness relative to force increased; 82% of the initial stiffness in rigor was detected in a restretch immediately after a shortening step, decreasing to 59% at 256 ms. When the fibre was activated at suboptimal [Ca2+] to cause the same force as in rigor, stiffness was lower than in rigor and decreased more after a release. 6. After completion of a release-stretch cycle, stiffness was rapidly restored to the same value as in isometric contraction. Test stretches at different points in time after completion of the cycle revealed that most of the stiffness had been restored within 1 ms of the restretch, occurring concomitantly with a decay in force.7. The shape of the length-force relationship during a release was analysed using a model consisting of a linear (cross-bridge) elasticity in series with an exponential (passive) elasticity and assuming no detachment of cross-bridges during release. In rigor the exponential element contributed 40% of the total compliance of the fibre. The model, although closely fitting the data, could not account for the results using an exponential elasticity with unaltered properties during activation at optimal and suboptimal [Ca2"] and in rigor.<br/><br>
8. The results suggest rapid detachment of some of the attached cross-bridges during and after a shortening step to slack length. Detachment of strongly bound cross-bridges may occur during a restretch, if it causes a strain on the attached crossbridges exceeding their working range. During the restretch, and on return to isometric contraction after the restretch, cross-bridges rapidly reattach in strongly<br/><br>
bound configurations.},
  author       = {Arheden, Håkan and Hellstrand, Per},
  issn         = {1469-7793},
  language     = {eng},
  pages        = {601--630},
  publisher    = {The Physiological Society},
  series       = {Journal of Physiology},
  title        = {Force response to rapid length change during contraction and rigor in skinned smooth muscle of guinea-pig taenia coli},
  volume       = {442},
  year         = {1991},
}