The Energy of Muscle Contraction. I. Tissue Force and Deformation During Fixed-End Contractions.

3D MRI contraction deformation energy finite element model muscle tissue

Journal

Frontiers in physiology
ISSN: 1664-042X
Titre abrégé: Front Physiol
Pays: Switzerland
ID NLM: 101549006

Informations de publication

Date de publication:
2020
Historique:
received: 03 01 2020
accepted: 18 06 2020
entrez: 28 9 2020
pubmed: 29 9 2020
medline: 29 9 2020
Statut: epublish

Résumé

During contraction the energy of muscle tissue increases due to energy from the hydrolysis of ATP. This energy is distributed across the tissue as strain-energy potentials in the contractile elements, strain-energy potential from the 3D deformation of the base-material tissue (containing cellular and extracellular matrix effects), energy related to changes in the muscle's nearly incompressible volume and external work done at the muscle surface. Thus, energy is redistributed through the muscle's tissue as it contracts, with only a component of this energy being used to do mechanical work and develop forces in the muscle's longitudinal direction. Understanding how the strain-energy potentials are redistributed through the muscle tissue will help enlighten why the mechanical performance of whole muscle in its longitudinal direction does not match the performance that would be expected from the contractile elements alone. Here we demonstrate these physical effects using a 3D muscle model based on the finite element method. The tissue deformations within contracting muscle are large, and so the mechanics of contraction were explained using the principles of continuum mechanics for large deformations. We present simulations of a contracting medial gastrocnemius muscle, showing tissue deformations that mirror observations from magnetic resonance imaging. This paper tracks the redistribution of strain-energy potentials through the muscle tissue during fixed-end contractions, and shows how fibre shortening, pennation angle, transverse bulging and anisotropy in the stress and strain of the muscle tissue are all related to the interaction between the material properties of the muscle and the action of the contractile elements.

Identifiants

pubmed: 32982762
doi: 10.3389/fphys.2020.00813
pmc: PMC7487973
doi:

Types de publication

Journal Article

Langues

eng

Pagination

813

Informations de copyright

Copyright © 2020 Wakeling, Ross, Ryan, Bolsterlee, Konno, Domínguez and Nigam.

Références

J Biomech. 2016 Oct 3;49(14):3200-3207
pubmed: 27544621
Muscle Nerve. 2000 Nov;23(11):1647-66
pubmed: 11054744
J Appl Physiol (1985). 2002 Jun;92(6):2381-9
pubmed: 12015351
J Biomech. 2002 Sep;35(9):1253-62
pubmed: 12163314
J R Soc Interface. 2015 Aug 6;12(109):20150365
pubmed: 26156300
J Mech Behav Biomed Mater. 2016 Sep;62:468-480
pubmed: 27281164
J Exp Biol. 2005 Sep;208(Pt 17):3249-61
pubmed: 16109887
J Muscle Res Cell Motil. 1994 Jun;15(3):299-308
pubmed: 7929795
IEEE Trans Med Imaging. 2010 Jan;29(1):196-205
pubmed: 19923044
Physiology (Bethesda). 2019 Nov 1;34(6):402-408
pubmed: 31577172
PeerJ. 2016 Jul 28;4:e2260
pubmed: 27547566
Int J Biomed Imaging. 2014;2014:352910
pubmed: 25328509
Eur J Appl Physiol Occup Physiol. 1988;57(3):327-35
pubmed: 3371342
PLoS Comput Biol. 2010 Dec 02;6(12):e1001018
pubmed: 21152002
Curr Opin Cell Biol. 1999 Feb;11(1):18-25
pubmed: 10047523
J Biomech. 2012 Oct 11;45(15):2673-9
pubmed: 22954714
J Physiol. 1998 Oct 15;512 ( Pt 2):603-14
pubmed: 9763648
Comput Methods Biomech Biomed Engin. 2014;17(3):217-29
pubmed: 22515574
J Biomech Eng. 2001 Apr;123(2):170-5
pubmed: 11340878
PLoS Comput Biol. 2012;8(11):e1002770
pubmed: 23166482
Physiol Rep. 2016 Sep;4(17):
pubmed: 27604399
Front Physiol. 2016 Mar 15;7:95
pubmed: 27014093
Comput Methods Biomech Biomed Eng Imaging Vis. 2016;4(2):73-85
pubmed: 28748126
PLoS One. 2013 Sep 03;8(9):e73021
pubmed: 24019889
Philos Trans R Soc Lond B Biol Sci. 2003 Sep 29;358(1437):1453-60
pubmed: 14561336
Biomech Model Mechanobiol. 2017 Oct;16(5):1729-1741
pubmed: 28516387
Nat Rev Neurosci. 2002 May;3(5):395-400
pubmed: 11988778
Ergonomics. 1980 Apr;23(4):351-7
pubmed: 7202390
J Biomech. 2017 May 24;57:69-78
pubmed: 28433388
Biomech Model Mechanobiol. 2017 Oct;16(5):1633-1643
pubmed: 28432448
Biomech Model Mechanobiol. 2013 Nov;12(6):1205-20
pubmed: 23417261
J Mech Behav Biomed Mater. 2013 Jun;22:84-94
pubmed: 23587721
Crit Rev Biomed Eng. 1989;17(4):359-411
pubmed: 2676342
J Appl Physiol (1985). 2017 Apr 1;122(4):727-738
pubmed: 28104754
J Exp Biol. 2018 Aug 1;221(Pt 15):
pubmed: 29844202
Eur J Appl Physiol. 2013 Feb;113(2):437-47
pubmed: 22777499
Comput Math Methods Med. 2012;2012:848630
pubmed: 23227110
J Biomech. 2019 Mar 27;86:160-166
pubmed: 30792071
PLoS Comput Biol. 2018 Apr 16;14(4):e1006123
pubmed: 29659583
J Appl Physiol (1985). 2014 Aug 15;117(4):363-9
pubmed: 24994884
J Biomech. 2011 Feb 24;44(4):771-3
pubmed: 21092966
J Biomech. 2005 Apr;38(4):657-65
pubmed: 15713285
J Biomech. 2011 Jan 4;44(1):109-15
pubmed: 20889156
Am J Physiol Cell Physiol. 2013 Aug 1;305(3):C241-52
pubmed: 23761627
Monogr Physiol Soc. 1985;41:1-357
pubmed: 3843415
Magn Reson Med. 2002 Jul;48(1):97-104
pubmed: 12111936
J Theor Biol. 2012 Apr 7;298:116-21
pubmed: 22251888
Comput Methods Biomech Biomed Engin. 2008 Oct;11(5):489-504
pubmed: 19230146
J Morphol. 1993 Nov;218(2):167-80
pubmed: 8263946
J Biomech. 2018 Jan 3;66:57-62
pubmed: 29154088
J Biomech. 2007;40(15):3363-72
pubmed: 17602693
Integr Comp Biol. 2009 Jul;49(1):51-8
pubmed: 21120110
Integr Comp Biol. 2018 Aug 1;58(2):232-250
pubmed: 29726964
J Appl Biomech. 2013 Jun;29(3):360-4
pubmed: 22927518
J Biomech. 2011 May 17;44(8):1618-20
pubmed: 21450292
J Appl Physiol (1985). 2017 Dec 1;123(6):1433-1442
pubmed: 28860176
Ergeb Anat Entwicklungsgesch. 1965;38:115-42
pubmed: 5319094
J Biomech. 2019 Mar 27;86:71-78
pubmed: 30739766
Clin Biomech (Bristol, Avon). 2015 Mar;30(3):269-75
pubmed: 25638688
Proc Natl Acad Sci U S A. 2008 Feb 5;105(5):1745-50
pubmed: 18230734
J Appl Physiol (1985). 2013 Jul 1;115(1):116-25
pubmed: 23640593
Biol Lett. 2017 Jan;13(1):
pubmed: 28123108
Biophys J. 1991 Apr;59(4):926-33
pubmed: 2065192
J Biomech. 2010 May 7;43(7):1243-50
pubmed: 20189180
J Biomech. 2016 May 3;49(7):1156-1161
pubmed: 26976226
Clin Orthop Relat Res. 1983 Oct;(179):275-83
pubmed: 6617027
PLoS One. 2013 Nov 15;8(11):e80713
pubmed: 24348913
Front Physiol. 2014 Aug 13;5:298
pubmed: 25232341
J Theor Biol. 2015 Oct 7;382:57-63
pubmed: 26073723
Biol Lett. 2016 Jun;12(6):
pubmed: 27354711
J Mech Behav Biomed Mater. 2012 May;9:163-83
pubmed: 22498294
J Mech Behav Biomed Mater. 2016 Oct;63:207-219
pubmed: 27429070
J Appl Physiol (1985). 2019 May 1;126(5):1492-1501
pubmed: 30571285
J Appl Physiol (1985). 1998 Aug;85(2):398-404
pubmed: 9688711
J Biomech. 2018 Oct 5;79:15-20
pubmed: 30195849
Philos Trans R Soc Lond B Biol Sci. 2011 May 27;366(1570):1554-64
pubmed: 21502126
J Theor Biol. 2000 Sep 7;206(1):131-49
pubmed: 10968943
Biol Lett. 2008 Feb 23;4(1):41-4
pubmed: 17986428

Auteurs

James M Wakeling (JM)

Department of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, BC, Canada.
Department of Mathematics, Simon Fraser University, Burnaby, BC, Canada.

Stephanie A Ross (SA)

Department of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, BC, Canada.

David S Ryan (DS)

Department of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, BC, Canada.

Bart Bolsterlee (B)

Neuroscience Research Australia, Randwick, NSW, Australia.
University of New South Wales, Graduate School of Biomedical Engineering, Randwick, NSW, Australia.

Ryan Konno (R)

Department of Physics and Astronomy, University of British Columbia, Vancouver, BC, Canada.

Sebastián Domínguez (S)

Department of Mathematics, Simon Fraser University, Burnaby, BC, Canada.

Nilima Nigam (N)

Department of Mathematics, Simon Fraser University, Burnaby, BC, Canada.

Classifications MeSH