Evidence on epimuscular myofascial force transmission (EMFT) was shown for undissected muscle in situ. We hypothesize that global length changes of gastrocnemius muscle-tendon complex in vivo will cause sizable and heterogeneous local strains within all muscles of the human lower leg. Our goal is to test this hypothesis. A method was developed and validated using high-resolution 3D magnetic resonance image sets and Demons nonrigid registration algorithm for performing large deformation analyses. Calculation of strain tensors per voxel in human muscles in vivo allowed quantifying local heterogeneous tissue deformations and volume changes. After hip and knee movement (Δ knee angle ≈ 25 deg) but without any ankle movement, local lengthening within m. gastrocnemius was shown to occur simultaneously with local shortening (maximally by +34.2% and −32.6%, respectively) at different locations. Moreover, similar local strains occur also within other muscles, despite being kept at constant muscle-tendon complex length. This is shown for synergistic m. soleus and deep flexors, as well as for antagonistic anterior crural and peroneal muscle groups: minimum peak lengthening and shortening equaled 23.3% and 25.54%, respectively despite global isometric conditions. These findings confirm our hypothesis and show that in vivo, muscles are in principle not independent mechanically.
References
1.
Tidball
, J. G.
, 1991
, “Myotendinous Junction Injury in Relation to Junction Structure and Molecular Composition
,” Exerc. Sport Sci. Rev.
, 19
, pp. 419
–445
.10.1249/00003677-199101000-000122.
Berthier
, C.
, and Blaineau
, S.
, 1997
, “Supramolecular Organization of the Subsarcolemmal Cytoskeleton of Adult Skeletal Muscle Fibers. A Review
,” Biol. Cell
, 89
(7
), pp. 413
–434
.10.1016/S0248-4900(97)89313-63.
Huijing
, P. A.
, 1999
, “Muscle as a Collagen Fiber Reinforced Composite: A Review of Force Transmission in Muscle and Whole Limb
,” J. Biomech.
, 32
(4
), pp. 329
–345
.10.1016/S0021-9290(98)00186-94.
Yucesoy
, C. A.
, Koopman
, B. H.
, Huijing
, P. A.
, and Grootenboer
, H. J.
, 2002
, “Three-Dimensional Finite Element Modeling of Skeletal Muscle Using a Two-Domain Approach: Linked Fiber-Matrix Mesh Model
,” J. Biomech.
, 35
(9
), pp. 1253
–1262
.10.1016/S0021-9290(02)00069-65.
Street
, S. F.
, 1983
, “Lateral Transmission of Tension in Frog Myofibers: A Myofibrillar Network and Transverse Cytoskeletal Connections Are Possible Transmitters
,” J. Cell Physiol.
, 114
(3
), pp. 346
–364
.10.1002/jcp.10411403146.
Huijing
, P. A.
, 2009
, “Epimuscular Myofascial Force Transmission: A Historical Review and Implications for New Research. International Society of Biomechanics Muybridge Award Lecture, Taipei, 2007
,” J. Biomech.
, 42
(1
), pp. 9
–21
.10.1016/j.jbiomech.2008.09.0277.
Huijing
, P. A.
, and Baan
, G. C.
, 2001
, “Extramuscular Myofascial Force Transmission Within the Rat Anterior Tibial Compartment: Proximo-Distal Differences in Muscle Force
,” Acta Physiol. Scand.
, 173
(3
), pp. 297
–311
.10.1046/j.1365-201X.2001.00911.x8.
Yucesoy
, C. A.
, Koopman
, B. H.
, Baan
, G. C.
, Grootenboer
, H. J.
, and Huijing
, P. A.
, 2003
, “Extramuscular Myofascial Force Transmission: Experiments and Finite Element Modeling
,” Arch. Physiol. Biochem.
, 111
(4
), pp. 377
–388
.10.3109/138134503123313376309.
Yucesoy
, C. A.
, Koopman
, B. H.
, Baan
, G. C.
, Grootenboer
, H. J.
, and Huijing
, P. A.
, 2003
, “Effects of Inter- and Extramuscular Myofascial Force Transmission on Adjacent Synergistic Muscles: Assessment by Experiments and Finite-Element Modeling
,” J. Biomech.
, 36
(12
), pp. 1797
–1811
.10.1016/S0021-9290(03)00230-610.
Yucesoy
, C. A.
, Baan
, G. C.
, Koopman
, B. H.
, Grootenboer
, H. J.
, and Huijing
, P. A.
, 2005
, “Pre-Strained Epimuscular Connections Cause Muscular Myofascial Force Transmission to Affect Properties of Synergistic EHL and EDL Muscles of the Rat
,” ASME J. Biomech. Eng.
, 127
(5
), pp. 819
–828
.10.1115/1.199252311.
Norkin
, C. C.
, and White
, D. J.
, 1995
, Measurement of Joint Motion: A Guide to Goniometry
, F. A. Davis, Philadelphia, PA
.12.
Weis
, J.
, Ericsson
, A.
, and Hemmingsson
, A.
, 1998
, “Chemical Shift Artifact-Free Imaging: A New Option in MRI?
,” Magn. Reson. Imaging
, 16
(7
), pp. 839
–844
.10.1016/S0730-725X(98)00006-X13.
Thirion
, J. P.
, 1998
, “Image Matching As a Diffusion Process: An Analogy With Maxwell's Demons
,” Med. Image Anal.
, 2
(3
), pp. 243
–260
.10.1016/S1361-8415(98)80022-414.
Moglo
, K. E.
, and Shirazi-Adl
, A.
, 2005
, “Cruciate Coupling and Screw-Home Mechanism in Passive Knee Joint During Extension–Flexion
,” J. Biomech.
, 38
(5
), pp. 1075
–1083
.10.1016/j.jbiomech.2004.05.03315.
Matsumoto
, M.
, and Nishimura
, T.
, 1998
, “Mersenne Twister: A 623-Dimensionally Equidistributed Uniform Pseudo-Random Number Generator
,” ACM Trans. Model. Comput. Simul.
, 8
(1
), pp. 3
–30
.10.1145/272991.27299516.
Huijing
, P. A.
, Yaman
, A.
, Ozturk
, C.
, and Yucesoy
, C. A.
, 2011
, “Effects of Knee Joint Angle on Global and Local Strains Within Human Triceps Surae Muscle: MRI Analysis Indicating In Vivo Myofascial Force Transmission Between Synergistic Muscles
,” Surg. Radiol. Anat.
, 33
(10
), pp. 869
–879
.10.1007/s00276-011-0863-117.
Ozturk
, C.
, and McVeigh
, E. R.
, 2000
, “Four-Dimensional B-Spline Based Motion Analysis of Tagged MR Images: Introduction and In Vivo Validation
,” Phys. Med. Biol.
, 45
(6
), pp. 1683
–1702
.10.1088/0031-9155/45/6/31918.
Hioki
, S.
, Fukubayashi
, T.
, Ikeda
, K.
, Niitsu
, M.
, and Ochiai
, N.
, 2003
, “Effect of Harvesting the Hamstrings Tendon for Anterior Cruciate Ligament Reconstruction on the Morphology and Movement of the Hamstrings Muscle: A Novel MRI Technique
,” Knee Surg. Sports Traumatol. Arthrosc.
, 11
(4
), pp. 223
–227
.10.1007/s00167-003-0361-z19.
Finni
, T.
, Hodgson
, J. A.
, Lai
, A. M.
, Edgerton
, V. R.
, and Sinha
, S.
, 2003
, “Nonuniform Strain of Human Soleus Aponeurosis-Tendon Complex During Submaximal Voluntary Contractions In Vivo
,” J. Appl. Physiol.
, 95
(2
), pp. 829
–837
.20.
Lee
, H. D.
, Finni
, T.
, Hodgson
, J. A.
, Lai
, A. M.
, Edgerton
, V. R.
, and Sinha
, S.
, 2006
, “Soleus Aponeurosis Strain Distribution Following Chronic Unloading In Humans: An In Vivo MR Phase-Contrast Study
,” J. Appl. Physiol.
, 100
(6
), pp. 2004
–2011
.10.1152/japplphysiol.01085.200521.
Zhong
, X.
, Epstein
, F. H.
, Spottiswoode
, B. S.
, Helm
, P. A.
, and Blemker
, S. S.
, 2008
, “Imaging Two-Dimensional Displacements and Strains in Skeletal Muscle During Joint Motion by Cine Dense MR
,” J. Biomech.
, 41
(3
), pp. 532
–540
.10.1016/j.jbiomech.2007.10.02622.
Ledesma-Carbayo
, M. J.
, Bajo
, A.
, Santa Marta
, C.
, Perez-David
, E.
, Caso
, I.
, Garcia-Fernandez
, M. A.
, Santos
, A.
, and Desco
, M.
, 2006
, “Cardiac motion analysis from cine MR sequences using non-rigid registration techniques
,” Comput. Cardiol.
, 2006
, pp. 65
–68
. Available at http://ieeexplore.ieee.org/xpls/abs_all.jsp?arnumber=451178923.
Mansi
, T.
, Peyrat
, J.-M.
, Sermesant
, M.
, Delingette
, H.
, Blanc
, J.
, Boudjemline
, Y.
, and Ayache
, N.
, 2009
, “Physically-Constrained Diffeomorphic Demons for the Estimation of 3D Myocardium Strain From Cine-MRI
,” Proceedings of the 5th International Conference on Functional Imaging and Modeling of the Heart
, Springer
, Nice, France
, pp. 201
–210
.24.
Cachier
, P.
, Pennec
, X.
, and Ayache
, N.
, 1999
, “Fast Non-Rigid Matching by Gradient Descent: Study and Improvement of the ‘Demons’ Algorithm
,” No. RR-3706, INRIA.25.
Kroon
, D. J.
, and Slump
, C. H.
, 2009
, “MRI Modality Transformation in Demon Registration
,” Proceedings of the Sixth IEEE International Conference on Symposium on Biomedical Imaging
, IEEE
, Boston, MA
, pp. 963
–966
.26.
Wang
, H.
, Dong
, L.
, O'Daniel
, J.
, Mohan
, R.
, Garden
, A. S.
, Ang
, K. K.
, Kuban
, D. A.
, Bonnen
, M.
, Chang
, J. Y.
, and Cheung
, R.
, 2005
, “Validation of an Accelerated ‘Demons’ Algorithm for Deformable Image Registration in Radiation Therapy
,” Phys. Med. Biol.
, 50
(12
), pp. 2887
–2905
.10.1088/0031-9155/50/12/01127.
Ledesma-Carbayo
, M. J.
, Santos
, A.
, Kybic
, J.
, Mahia-Casado
, P.
, Garcia-Fernandez
, M. A.
, Malpica
, N.
, Perez-David
, E.
, and Desco
, M.
, 2004
, “Myocardial Strain Analysis of Echocardiographic Sequences Using Nonrigid Registration
,” Comput. Cardiol.
, 31
, pp. 313
–316
.28.
Ledesma-Carbayo
, M. J.
, Kybic
, J.
, Desco
, M.
, Santos
, A.
, Suhling
, M.
, Hunziker
, P.
, and Unser
, M.
, 2005
, “Spatio-Temporal Nonrigid Registration for Ultrasound Cardiac Motion Estimation
,” IEEE Trans. Med. Imaging
, 24
(9
), pp. 1113
–1126
.10.1109/TMI.2005.85205029.
Ledesma-Carbayo
, M. J.
, Mahía-Casado
, P.
, Santos
, A.
, Pérez-David
, E.
, García-Fernández
, M. A.
, and Desco
, M.
, 2006
, “Cardiac Motion Analysis From Ultrasound Sequences Using Nonrigid Registration: Validation Against Doppler Tissue Velocity
,” Ultrasound Med. Biol.
, 32
(4
), pp. 483
–490
.10.1016/j.ultrasmedbio.2005.12.00630.
Klein
, A.
, Andersson
, J.
, Ardekani
, B. A.
, Ashburner
, J.
, Avants
, B.
, Chiang
, M. C.
, Christensen
, G. E.
, Collins
, D. L.
, Gee
, J.
, Hellier
, P.
, Song
, J. H.
, Jenkinson
, M.
, Lepage
, C.
, Rueckert
, D.
, Thompson
, P.
, Vercauteren
, T.
, Woods
, R. P.
, Mann
, J. J.
, and Parsey
, R. V.
, 2009
, “Evaluation of 14 Nonlinear Deformation Algorithms Applied to Human Brain MRI Registration
,” Neuroimage
, 46
(3
), pp. 786
–802
.10.1016/j.neuroimage.2008.12.03731.
Chang
, J.
, Suh
, T. S.
, and Lee
, D. S.
, 2009
, “Development of a Deformable Lung Phantom for the Evaluation of Deformable Registration
,” J. Appl. Clin. Med. Phys.
, 36
(6
), p. 2458
.10.1118/1.318122532.
Fedorov
, A.
, Billet
, E.
, Prastawa
, M.
, Gerig
, G.
, Radmanesh
, A.
, Warfield
, S. K.
, Kikinis
, R.
, and Chrisochoides
, N.
, 2008
, “Evaluation of Brain MRI Alignment With the Robust Hausdorff Distance Measures
,” Adv. Visual Comput. Pt I
, 5358
, pp. 594
–603
.10.1007/978-3-540-89639-533.
Vercauteren
, T.
, Pennec
, X.
, Perchant
, A.
, and Ayache
, N.
, 2009
, “Diffeomorphic Demons: Efficient Non-Parametric Image Registration
,” Neuroimage
, 45
(1 Suppl
), pp. S61
–S72
.10.1016/j.neuroimage.2008.10.04034.
Rohlfing
, T.
, Maurer
, C. R.
, Jr., Bluemke
, D. A.
, and Jacobs
, M. A.
, 2003
, “Volume-Preserving Nonrigid Registration of MR Breast Images Using Free-Form Deformation With an Incompressibility Constraint
,” IEEE Trans. Med. Imaging
, 22
(6
), pp. 730
–741
.10.1109/TMI.2003.81479135.
Swammerdam
, J.
, 1737
, Bybel der natuure door Jan Swammerdam, Amsteldammer, of, Historie der Insecten [Microform]: tot Zeekere Zoorten Gebracht: Door Voorbeelden, Ontleedkundige Onderzoekingen van Veelerhande Kleine Gediertens, Als ook Door Kunstige Kopere Plaaten Opgeheldert: Verrykt met ontelbaare Waarnemingen van Nooit Ontdekte Zeldzaamheden in de Natuur / Alles in de Hollandsche, des Auteurs Moedertaale, Beschreven; Hier by komt een Voorreeden, Waar in het Leven van Den Auteur Beschreven is Door Herman Boerhaave; de Latynsche Overzetting Heeft Bezorgt Hieronimus David Gaubius, I. Severinus, B. Vander Aa, Pieter Vander Aa, Leyden.36.
Baskin
, R. J.
, and Paolini
, P. J.
, 1966
, “Muscle Volume Changes
,” J. Gen. Physiol.
, 49
(3
), pp. 387
–404
.10.1085/jgp.49.3.38737.
Huyghe
, J. M.
, Arts
, T.
, van Campen
, D. H.
, and Reneman
, R. S.
, 1992
, “Porous Medium Finite Element Model of the Beating Left Ventricle
,” Am. J. Physiol.
, 262
(4 Pt 2
), pp. H1256
–H1267
.38.
Wisnes
, A.
, and Kirkebø
, A.
, 1976
, “Regional Distribution of Blood Flow in Calf Muscles of Rat During Passive Stretch and Sustained Contraction
,” Acta Physiol. Scand.
, 96
(2
), pp. 256
–266
.10.1111/j.1748-1716.1976.tb10194.x39.
Sejersted
, O. M.
, and Hargens
, A. R.
, 1995
, “Intramuscular Pressures for Monitoring Different Tasks and Muscle Conditions
,” Adv. Exp. Med. Biol.
, 384
, pp. 339
–350
.40.
Valic
, Z.
, Buckwalter
, J. B.
, and Clifford
, P. S.
, 2005
, “Muscle Blood Flow Response to Contraction: Influence of Venous Pressure
,” J. Appl. Physiol.
, 98
(1
), pp. 72
–76
.10.1152/japplphysiol.00151.200441.
Stranden
, E.
, and Kroese
, A. J.
, 1998
, “Venodynamics in Healthy Subjects and in Patients With Venous Dysfunction
,” Scope Phlebol. Lymphol.
, 5
, pp. 4
–12
. Available at http://www.strteknikk.no/venopulse/Stranden%20Venodynamics%2004.pdf42.
Maas
, H.
, Baan
, G. C.
, and Huijing
, P. A.
, 2001
, “Intermuscular Interaction Via Myofascial Force Transmission: Effects of Tibialis Anterior and Extensor Hallucis Longus Length on Force Transmission From Rat Extensor Digitorum Longus Muscle
,” J. Biomech.
, 34
(7
), pp. 927
–940
.10.1016/S0021-9290(01)00055-043.
Yucesoy
, C. A.
, Maas
, H.
, Koopman
, B. H.
, Grootenboer
, H. J.
, and Huijing
, P. A.
, 2006
, “Mechanisms Causing Effects of Muscle Position on Proximo-Distal Muscle Force Differences in Extra-Muscular Myofascial Force Transmission
,” Med. Eng. Phys.
, 28
(3
), pp. 214
–226
.10.1016/j.medengphy.2005.06.00444.
Passerieux
, E.
, Rossignol
, R.
, Letellier
, T.
, and Delage
, J. P.
, 2007
, “Physical Continuity of the Perimysium From Myofibers to Tendons: Involvement in Lateral Force Transmission in Skeletal Muscle
,” J. Struct. Biol.
, 159
(1
), pp. 19
–28
.10.1016/j.jsb.2007.01.02245.
Yucesoy
, C. A.
, 2010
, “Epimuscular Myofascial Force Transmission Implies Novel Principles for Muscular Mechanics
,” Exerc. Sport Sci. Rev.
, 38
(3
), pp. 128
–134
.10.1097/JES.0b013e3181e372ef46.
Maas
, H.
, Baan
, G. C.
, Huijing
, P. A.
, Yucesoy
, C. A.
, Koopman
, B. H. F. J. M.
, and Grootenboer
, H. J.
, 2003
, “The Relative Position of EDL Muscle Affects the Length of Sarcomeres Within Muscle Fibers: Experimental Results and Finite-Element Modeling
,” ASME J. Biomech. Eng.
, 125
(5
), pp. 745
–753
.10.1115/1.161561947.
Huijing
, P. A.
, van de Langenberg
, R. W.
, Meesters
, J. J.
, and Baan
, G. C.
, 2007
, “Extramuscular Myofascial Force Transmission Also Occurs Between Synergistic Muscles and Antagonistic Muscles
,” J. Electromyogr. Kinesiol.
, 17
(6
), pp. 680
–689
.10.1016/j.jelekin.2007.02.00548.
Rijkelijkhuizen
, J. M.
, Meijer
, H. J. M.
, Baan
, G. C.
, and Huijing
, P. A.
, 2007
, “Myofascial Force Transmission Also Occurs Between Antagonistic Muscles Located Within Opposite Compartments of the Rat Lower Hind Limb
,” J. Electromyogr. Kinesiol.
, 17
(6
), pp. 690
–697
.10.1016/j.jelekin.2007.02.00449.
Yucesoy
, C. A.
, Baan
, G.
, and Huijing
, P. A.
, 2010
, “Epimuscular Myofascial Force Transmission Occurs in the Rat Between the Deep Flexor Muscles and Their Antagonistic Muscles
,” J. Electromyogr. Kinesiol.
, 20
(1
), pp. 118
–126
.10.1016/j.jelekin.2008.09.01250.
Kubo
, K.
, Kanehisa
, H.
, Kawakami
, Y.
, and Fukunaga
, T.
, 2001
, “Influence of Static Stretching on Viscoelastic Properties of Human Tendon Structures In Vivo
,” J. Appl. Physiol.
, 90
(2
), pp. 520
–527
.51.
Nourbakhsh
, M. R.
, and Kukulka
, C. G.
, 2004
, “Relationship Between Muscle Length and Moment Arm on EMG Activity of Human Triceps Surae Muscle
,” J. Electromyogr. Kinesiol.
, 14
(2
), pp. 263
–273
.10.1016/S1050-6411(03)00076-252.
Stejskal
, E. O.
, and Tanner
, J. E.
, 1965
, “Spin Diffusion Measurements: Spin Echoes in the Presence of a Time-Dependent Field Gradient
,” J. Chem. Phys.
, 42
(1
), pp. 288
–292
.10.1063/1.169569053.
Le Bihan
, D.
, Mangin
, J. F.
, Poupon
, C.
Clark
, C. A.
, Pappata
, S.
Molko
, N.
, and Chabriat
, H.
, 2001
, “Diffusion Tensor Imaging: Concepts and Applications
,” J. Magn. Reson. Imaging
, 13
(4
), pp. 534
–546
.10.1002/jmri.107654.
Heemskerk
, A. M.
, Strijkers
, G. J.
, Vilanova
, A.
, Drost
, M. R.
, and Nicolay
, K.
, 2005
, “Determination of Mouse Skeletal Muscle Architecture Using Three-Dimensional Diffusion Tensor Imaging
,” Magn. Reson. Med.
, 53
(6
), pp. 1333
–1340
.10.1002/mrm.2047655.
Budzik
, J.
, Le Thuc
, V.
, Demondion
, X.
, Morel
, M.
, Chechin
, D.
, and Cotten
, A.
, 2007
, “In Vivo MR Tractography of Thigh Muscles Using Diffusion Imaging: Initial Results
,” Eur. Radiol.
, 17
(12
), pp. 3079
–3085
.10.1007/s00330-007-0713-z56.
Yaman
, A.
, Baan
, G. C.
, Huijing
, P. A.
, Ozturk
, C.
, and Yucesoy
, C. A.
, 2009
, “In Vivo Human Muscle MRI Shows Myofascial Force Transmission Induced Serial Inhomogeneity of Sarcomere Lengths
,” Workshop on Multi-Scale Muscle Mechanics
, Woods Hole, MA
.57.
Hatakenaka
, M.
, Yabuuchi
, H.
, Sunami
, S.
, Kamitani
, T.
, Takayama
, Y.
, Nishikawa
, K.
, and Honda
, H.
, 2010
, “Joint Position Affects Muscle Proton Diffusion: Evaluation With a 3-T MR Ssystem
,” AJR Am. J. Roentgenol.
, 194
(2
), pp. W208
–W211
.10.2214/AJR.09.316758.
Yu
, W. S.
, Kilbreath
, S. L.
, Fitzpatrick
, R. C.
, and Gandevia
, S. C.
, 2007
, “Thumb and Finger Forces Produced by Motor Units in the Long Flexor of the Human Thumb
,” J. Physiol.
, 583
(3
), pp. 1145
–1154
.10.1113/jphysiol.2007.13564059.
Bojsen-Moller
, J.
, Schwartz
, S.
, Kalliokoski
, K. K.
, Finni
, T.
, and Magnusson
, S. P.
, 2010
, “Intermuscular Force Transmission Between Human Plantarflexor Muscles In Vivo
,” J. Appl. Physiol.
, 109
(6
), pp. 1608
–1618
.10.1152/japplphysiol.01381.200960.
Maas
, H.
, and Sandercock
, T. G.
, 2008
, “Are Skeletal Muscles Independent Actuators? Force Transmission From Soleus Muscle in the Cat
,” J. Appl. Physiol.
, 104
(6
), pp. 1557
–1567
.10.1152/japplphysiol.01208.2007Copyright © 2013 by ASME
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