Impact of contraction intensity and ankle joint angle on calf muscle fascicle length and pennation angle during isometric and dynamic contractions.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
22 10 2024
Historique:
received: 27 05 2024
accepted: 08 10 2024
medline: 23 10 2024
pubmed: 23 10 2024
entrez: 22 10 2024
Statut: epublish

Résumé

During muscle contraction, not only are the fascicles shortening but also the pennation angle changes, which leads to a faster contraction of the muscle than of its fascicles. This phenomenon is called muscle gearing, and it has a direct influence on the force output of the muscle. There are few studies showing pennation angle changes during isometric and concentric contractions for different contraction intensities and muscle lengths. Therefore, the aim was to determine these influences over a wide range of contraction intensities and ankle joint angles for human triceps surae. Additionally, the influence of contraction intensity and ankle joint angle on muscle gearing was evaluated. Ten sport students performed concentric and isometric contractions with intensities between 0 and 90% of the maximum voluntary contraction and ankle joint angles from 50° to 120°. During these contractions, the m. gastrocnemius medialis and lateralis and the m. soleus were recorded via ultrasound imaging. A nonlinear relationship between fascicle length and pennation angle was discovered, which can be described with a quadratic fit for each of the muscles during isometric contraction. A nearly identical relationship was detected during dynamic contraction. The muscle gearing increased almost linearly with contraction intensity and ankle joint angle.

Identifiants

pubmed: 39438523
doi: 10.1038/s41598-024-75795-2
pii: 10.1038/s41598-024-75795-2
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

24929

Informations de copyright

© 2024. The Author(s).

Références

Fleming, B. C. & Beynnon, B. D. In vivo measurement of ligament/tendon strains and forces. A review. Ann. Biomed. Eng. 32 (3), 318–328. https://doi.org/10.1023/B:ABME.0000017542.75080.86 (2004).
doi: 10.1023/B:ABME.0000017542.75080.86 pubmed: 15095807
Komi, P. V. Relevance of in vivo force measurements to human biomechanics. J. Biomech. 23, 23–34. https://doi.org/10.1016/0021-9290(90)90038-5 (1990).
doi: 10.1016/0021-9290(90)90038-5 pubmed: 2081741
Kim, W. & Voloshin, A. S. Role of plantar fascia in the load bearing capacity of the human foot. J. Biomech. 28 (9), 1025–1033. https://doi.org/10.1016/0021-9290(94)00163-X (1995).
doi: 10.1016/0021-9290(94)00163-X pubmed: 7559672
Siebert, T., Sust, M., Thaller, S., Tilp, M. & Wagner, H. An improved method to determine neuromuscular properties using force laws – from single muscle to applications in human movements. Hum. Mov. Sci. 26 (2), 320–341. https://doi.org/10.1016/j.humov.2007.01.006 (2007).
doi: 10.1016/j.humov.2007.01.006 pubmed: 17343950
Gordon, A. M., Huxley, A. F. & Julian, F. J. The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J. Physiol. 184 (1), 170–192. https://doi.org/10.1113/jphysiol.1966.sp007909 (1966).
doi: 10.1113/jphysiol.1966.sp007909 pubmed: 5921536 pmcid: 1357553
Hatze, H. A complete set of control equations for the human musculo-skeletal system. J. Biomech. 10 (11–12), 799–805. https://doi.org/10.1016/0021-9290(77)90094-x (1977).
doi: 10.1016/0021-9290(77)90094-x pubmed: 606726
Hatze, H. A comprehensive model for human motion simulation and its application to the take-off phase of the long jump. J. Biomech. 14 (3), 135–142. https://doi.org/10.1016/0021-9290(81)90019-1 (1981).
doi: 10.1016/0021-9290(81)90019-1 pubmed: 7240274
Otten, E. Concepts and models of Functional Architecture in skeletal muscle. Exerc. Sport Sci. Rev. 16 (1), (1988). https://journals.lww.com/acsm-essr/Fulltext/1988/00160/Concepts_and_Models_of_Functional_Architecture_in.6.aspx
Zajac, F. E. Muscle and tendon. Properties, models, scaling, and application to biomechanics and motor control. Crit. Rev. Biomed. Eng. 17 (4), 359–411 (1989).
pubmed: 2676342
Epstein, M. & Herzog, W. Theoretical Models of Skeletal Muscle. Biological and Mathematical Considerations (Wiley, 1998).
Huijing, P. A. Parameter interdependence and success of skeletal muscle modelling. Hum. Mov. Sci. 14 (4–5), 443–486. https://doi.org/10.1016/0167-9457(95)00024-8 (1995).
doi: 10.1016/0167-9457(95)00024-8
Kramer, S. Modellierung der Muskelkontraktion der Plantarflexoren unter Berücksichtigung physiologischer Parameter und der Muskelarchitektur, (2012).
Siebert, T. et al. Three-dimensional muscle Architecture and Comprehensive Dynamic properties of rabbit gastrocnemius, Plantaris and soleus. Input for Simulation studies. PLoS One 10 (6), e0130985. https://doi.org/10.1371/journal.pone.0130985 (2015).
Hill, A. V. The mechanics of active muscle. Proceedings of the Royal Society of London. Series B - Biological Sciences, (1953). https://doi.org/10.1098/rspb.1953.0027
Lichtwark, G. A. & Wilson, A. M. Interactions between the human gastrocnemius muscle and the Achilles tendon during incline, level and decline locomotion. J. Exp. Biol. 209 (Pt 21), 4379–4388. https://doi.org/10.1242/jeb.02434 (2006).
doi: 10.1242/jeb.02434 pubmed: 17050853
Lichtwark, G. A., Bougoulias, K. & Wilson, A. M. Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running. J. Biomech. 40 (1), 157–164. https://doi.org/10.1016/j.jbiomech.2005.10.035 (2007).
doi: 10.1016/j.jbiomech.2005.10.035 pubmed: 16364330
Aggeloussis, N., Giannakou, E., Albracht, K. & Arampatzis, A. Reproducibility of fascicle length and pennation angle of gastrocnemius medialis in human gait in vivo. Gait Posture 31 (1), 73–77. https://doi.org/10.1016/j.gaitpost.2009.08.249 (2010).
doi: 10.1016/j.gaitpost.2009.08.249 pubmed: 19775893
Héroux, M. E., Stubbs, P. W. & Herbert, R. D. Behavior of human gastrocnemius muscle fascicles during ramped submaximal isometric contractions. Physiological Rep. 4 (17). https://doi.org/10.14814/phy2.12947 (2016). e12947.
Narici, M. V. et al. In vivo human gastrocnemius architecture with changing joint angle at rest and during graded isometric contraction. J. Physiol. 496 (1), 287–297 (1996).
doi: 10.1113/jphysiol.1996.sp021685 pubmed: 8910216 pmcid: 1160844
Kawakami, Y., Ichinose, Y. & Fukunaga, T. Architectural and functional features of human triceps surae muscles during contraction. J. Appl. Physiol. 85 (2), 398–404. https://doi.org/10.1152/jappl.1998.85.2.398 (1998).
doi: 10.1152/jappl.1998.85.2.398 pubmed: 9688711
Maganaris, C. N., Baltzopoulos, V. & Sargeant, A. J. In vivo measurements of the triceps surae complex architecture in man. Implications for muscle function. J. Physiol. 512 (Pt 2), 603–614. https://doi.org/10.1111/j.1469-7793.1998.603be.x (1998).
doi: 10.1111/j.1469-7793.1998.603be.x pubmed: 9763648 pmcid: 2231202
Fukunaga, T. et al. Physiological cross-sectional area of human leg muscles based on magnetic resonance imaging. J. Orthop. Res. 10 (6), 926–934. https://doi.org/10.1002/jor.1100100623 (1992).
doi: 10.1002/jor.1100100623
Kubo, K. et al. In vivo dynamics of human medial gastrocnemius muscle-tendon complex during stretch-shortening cycle exercise. Acta Physiol. Scand. 170 (2), 127–135. https://doi.org/10.1046/j.1365-201x.2000.00768.x (2000).
doi: 10.1046/j.1365-201x.2000.00768.x pubmed: 11114950
Fukunaga, T. et al. In vivo behaviour of human muscle tendon during walking. Proc. Biol. Sci. 268 (1464), 229–233. https://doi.org/10.1098/rspb.2000.1361 (2001).
doi: 10.1098/rspb.2000.1361 pubmed: 11217891 pmcid: 1088596
Fukunaga, T., Kawakami, Y., Kubo, K. & Kanehisa, H. Muscle and tendon interaction during human movements. Exerc. Sport Sci. Rev. 30 (3), 106–110. https://doi.org/10.1097/00003677-200207000-00003 (2002).
doi: 10.1097/00003677-200207000-00003 pubmed: 12150568
Cronin, N. J. & Lichtwark, G. The use of ultrasound to study muscle-tendon function in human posture and locomotion. Gait Posture 37 (3), 305–312. https://doi.org/10.1016/j.gaitpost.2012.07.024 (2013).
doi: 10.1016/j.gaitpost.2012.07.024 pubmed: 22910172
Brainerd, E. L. & Azizi, E. Muscle fiber angle, segment bulging and architectural gear ratio in segmented musculature. J. Exp. Biol. 208 (Pt 17), 3249–3261. https://doi.org/10.1242/jeb.01770 (2005).
doi: 10.1242/jeb.01770
Eng, C. M., Azizi, E. & Roberts, T. J. Structural determinants of muscle gearing during dynamic contractions. Integr. Comp. Biol. 58 (2), 207–218. https://doi.org/10.1093/icb/icy054 (2018).
doi: 10.1093/icb/icy054 pubmed: 29889236 pmcid: 6104701
Azizi, E., Brainerd, E. L. & Roberts, T. J. Variable gearing in pennate muscles. Proc. Natl. Acad. Sci. USA. 105 (5), 1745–1750. https://doi.org/10.1073/pnas.0709212105 (2008).
doi: 10.1073/pnas.0709212105 pubmed: 18230734 pmcid: 2234215
Azizi, E. & Roberts, T. J. Geared up to stretch. Pennate muscle behavior during active lengthening. J. Exp. Biol. 217 (Pt 3), 376–381. https://doi.org/10.1242/jeb.094383 (2014).
doi: 10.1242/jeb.094383 pubmed: 24477610 pmcid: 4008126
Holt, N. C., Danos, N., Roberts, T. J. & Azizi, E. Stuck in gear. Age-related loss of variable gearing in skeletal muscle. J. Exp. Biol. 219 (Pt 7), 998–1003. https://doi.org/10.1242/jeb.133009 (2016).
doi: 10.1242/jeb.133009 pubmed: 27030778 pmcid: 4852693
Dick, T. J. M. & Wakeling, J. M. Shifting gears: dynamic muscle shape changes and force-velocity behavior in the medial gastrocnemius. Journal of applied physiology : 123 (6), 1433–1442 https://doi.org/10.1152/japplphysiol.01050.2016 (1985).
Donath, L., Siebert, T., Faude, O. & Puta, C. Correct, fake and absent pre-information does not affect the occurrence and magnitude of the bilateral force deficit. J. Sports Sci. Med. 13 (2), 439–443 (2014).
pubmed: 24790502 pmcid: 3990902
Ertelt, T. & Blickhan, R. Describing force-patterns. A method for an analytic classification using the example of sledge jumps. J. Biomech. 42 (15), 2616–2619. https://doi.org/10.1016/j.jbiomech.2009.07.023 (2009).
doi: 10.1016/j.jbiomech.2009.07.023 pubmed: 19665132
Narici, M. V., Landoni, L. & Minetti, A. E. Assessment of human knee extensor muscles stress from in vivo physiological cross-sectional area and strength measurements. Eur. J. Appl. Physiol. Occup. Physiol. 65 (5), 438–444. https://doi.org/10.1007/BF00243511 (1992).
doi: 10.1007/BF00243511 pubmed: 1425650
Takahashi, K., Shiotani, H., Evangelidis, P. E., Sado, N. & Kawakami, Y. Three-dimensional architecture of human medial gastrocnemius fascicles in vivo: Regional variation and its dependence on muscle size. J. Anat. 241 (6), 1324–1335. https://doi.org/10.1111/joa.13750 (2022).
doi: 10.1111/joa.13750 pubmed: 36004517 pmcid: 9644967
Bolsterlee, B. et al. Three-dimensional architecture of the whole human soleus muscle in vivo. PeerJ https://doi.org/10.7717/peerj.4610 (2018).
doi: 10.7717/peerj.4610 pubmed: 29682414 pmcid: 5910694
Siebert, T., Till, O., Stutzig, N., Günther, M. & Blickhan, R. Muscle force depends on the amount of transversal muscle loading. J. Biomech. 47 (8), 1822–1828. https://doi.org/10.1016/j.jbiomech.2014.03.029 (2014).
doi: 10.1016/j.jbiomech.2014.03.029 pubmed: 24725439
Bolsterlee, B., Gandevia, S. C. & Herbert, R. D. Ultrasound imaging of the human medial gastrocnemius muscle. How to orient the transducer so that muscle fascicles lie in the image plane. J. Biomech. 49 (7), 1002–1008. https://doi.org/10.1016/j.jbiomech.2016.02.014 (2016).
doi: 10.1016/j.jbiomech.2016.02.014 pubmed: 26905734
Siebert, T., Rode, C., Till, O., Stutzig, N. & Blickhan, R. Force reduction induced by unidirectional transversal muscle loading is independent of local pressure. J. Biomech. 49 (7), 1156–1161. https://doi.org/10.1016/j.jbiomech.2016.02.053 (2016).
doi: 10.1016/j.jbiomech.2016.02.053 pubmed: 26976226
Ryan, D. S., Stutzig, N., Siebert, T. & Wakeling, J. M. Passive and dynamic muscle architecture during transverse loading for gastrocnemius medialis in man. J. Biomech. 86, 160–166. https://doi.org/10.1016/j.jbiomech.2019.01.054 (2019).
doi: 10.1016/j.jbiomech.2019.01.054 pubmed: 30792071
Klimstra, M., Dowling, J., Durkin, J. L. & MacDonald, M. The effect of ultrasound probe orientation on muscle architecture measurement. J. Electromyogr. Kinesiology: Official J. Int. Soc. Electrophysiological Kinesiol. 17 (4), 504–514. https://doi.org/10.1016/j.jelekin.2006.04.011 (2007).
doi: 10.1016/j.jelekin.2006.04.011
Bénard, M. R., Becher, J. G., Harlaar, J., Huijing, P. A. & Jaspers, R. T. Anatomical information is needed in ultrasound imaging of muscle to avoid potentially substantial errors in measurement of muscle geometry. Muscle Nerve 39 (5), 652–665. https://doi.org/10.1002/mus.21287 (2009).
doi: 10.1002/mus.21287 pubmed: 19291798
Kwah, L. K., Pinto, R. Z., Diong, J. & Herbert, R. D. Reliability and validity of ultrasound measurements of muscle fascicle length and pennation in humans. A systematic review. J. Appl. Physiol. (Bethesda Md. : 1985. 114 (6), 761–769. https://doi.org/10.1152/japplphysiol.01430.2011 (2013).
doi: 10.1152/japplphysiol.01430.2011
Rana, M. & Wakeling, J. M. In-vivo determination of 3D muscle architecture of human muscle using free hand ultrasound. J. Biomech. 44 (11), 2129–2135. https://doi.org/10.1016/j.jbiomech.2011.05.026 (2011).
doi: 10.1016/j.jbiomech.2011.05.026 pubmed: 21664617
Reinsch, C. H. Smoothing by Spline functions. Numer. Math. 10, 177–183 (1967).
doi: 10.1007/BF02162161
Stutzig, N., Ryan, D., Wakeling, J. M. & Siebert, T. Impact of transversal calf muscle loading on plantarflexion. J. Biomech. 85, 37–42. https://doi.org/10.1016/j.jbiomech.2019.01.011 (2019).
doi: 10.1016/j.jbiomech.2019.01.011 pubmed: 30660380
Reeves, N. D. & Narici, M. V. Behavior of human muscle fascicles during shortening and lengthening contractions in vivo. J. Appl. Physiol. 95 (3), 1090–1096. https://doi.org/10.1152/japplphysiol.01046.2002 (2003).
doi: 10.1152/japplphysiol.01046.2002 pubmed: 12740314
Siebert, T., Screen, H. R. C. & Rode, C. Computational modelling of muscle, tendon, and ligaments biomechanics. Comput. Modelling Biomech. Biotribology Musculoskelet. Syst. 155–186. https://doi.org/10.1016/B978-0-12-819531-4.00008-0 (2021).
Kelp, N. Y. et al. Muscle architecture and shape changes in the gastrocnemii of active younger and older adults. J. Biomech. 129 https://doi.org/10.1016/j.jbiomech.2021.110823 (2021).
Aeles, J., Bolsterlee, B., Kelp, N. Y., Dick, T. J. M. & Hug, F. Regional variation in lateral and medial gastrocnemius muscle fibre lengths obtained from diffusion tensor imaging. J. Anat. 240 (1), 131–144. https://doi.org/10.1111/joa.13539 (2022).
doi: 10.1111/joa.13539 pubmed: 34411299
Sinha, U., Csapo, R., Malis, V., Xue, Y. & Sinha, S. Age-related differences in diffusion tensor indices and fiber architecture in the medial and lateral gastrocnemius. J. Magn. Reson. Imaging: JMRI. 41 (4), 941–953. https://doi.org/10.1002/jmri.24641 (2015).
doi: 10.1002/jmri.24641 pubmed: 24771672
Monte, A. & Zignoli, A. Muscle and tendon stiffness and belly gearing positively correlate with rate of torque development during explosive fixed end contractions. J. Biomech. 114 https://doi.org/10.1016/j.jbiomech.2020.110110 (2021).
Takahashi, K., Shiotani, H., Evangelidis, P. E., Sado, N. & Kawakami, Y. Coronal as well as sagittal fascicle dynamics can bring about a gearing effect in muscle elongation by passive lengthening. Med. Sci. Sports. Exerc. 55 (11), 2035–2044. https://doi.org/10.1249/MSS.0000000000003229 (2023).
doi: 10.1249/MSS.0000000000003229 pubmed: 37418239
Sahrmann, A. S., Vosse, L., Siebert, T., Handsfield, G. G. & Röhrle O. 3D ultrasound-based determination of skeletal muscle fascicle orientations. Biomech. Model. Mechanobiol. https://doi.org/10.1007/s10237-024-01837-3 (2024).
doi: 10.1007/s10237-024-01837-3 pubmed: 38530501 pmcid: 11341646
Sahrmann, A. S., Vosse, L., Siebert, T., Handsfield, G. G. & Röhrle, O. Determination of muscle shape deformations of the tibialis anterior during dynamic contractions using 3D ultrasound. Front. Bioeng. Biotechnol. 12, 1388907. https://doi.org/10.1016/j.jmbbm.2018.04.006 (2024).
doi: 10.1016/j.jmbbm.2018.04.006 pubmed: 38903187 pmcid: 11188672
Randhawa, A., Jackman, M. E. & Wakeling, J. M. Muscle gearing during isotonic and isokinetic movements in the ankle plantarflexors. Eur. J. Appl. Physiol. 113 (2), 437–447. https://doi.org/10.1007/s00421-012-2448-z (2013).
doi: 10.1007/s00421-012-2448-z pubmed: 22777499
Böl, M. et al. Three-dimensional surface geometries of the rabbit soleus muscle during contraction. Input for biomechanical modelling and its validation. Biomech. Model. Mechanobiol. 12 (6), 1205–1220. https://doi.org/10.1007/s10237-013-0476-1 (2013).
doi: 10.1007/s10237-013-0476-1 pubmed: 23417261
Baskin, R. J. & Paolini, P. J. Volume change and pressure development in muscle during contraction. Am. J. Physiol. 213 (4), 1025–1030. https://doi.org/10.1152/ajplegacy.1967.213.4.1025 (1967).
doi: 10.1152/ajplegacy.1967.213.4.1025 pubmed: 6051170
Ryan, D. S., Domínguez, S., Ross, S. A., Nigam, N. & Wakeling, J. M. The Energy of Muscle Contraction. II. Transverse Compression and Work. Front. Physiol. 11, 538522. https://doi.org/10.3389/fphys.2020.538522 (2020).
doi: 10.3389/fphys.2020.538522 pubmed: 33281608 pmcid: 7689187
Dick, T. J. M. & Wakeling, J. M. Geometric models to explore mechanisms of dynamic shape change in skeletal muscle. Royal Soc. open. Sci. 5 (5), 172371. https://doi.org/10.1098/rsos.172371 (2018).
doi: 10.1098/rsos.172371
Schenk, P. et al. A simple geometrical model accounting for 3D muscle architectural changes across muscle lengths. J. Biomech. 103, 109694. https://doi.org/10.1016/j.jbiomech.2020.109694 (2020).
doi: 10.1016/j.jbiomech.2020.109694 pubmed: 32147241
Raiteri, B. J. Aponeurosis behaviour during muscular contraction. A narrative review. Eur. J. Sport Sci. 18 (8), 1128–1138. https://doi.org/10.1080/17461391.2018.1472299 (2018).
doi: 10.1080/17461391.2018.1472299 pubmed: 29806988
Reinhardt, L., Siebert, T., Leichsenring, K., Blickhan, R. & Böl, M. Intermuscular pressure between synergistic muscles correlates with muscle force. J. Exp. Biol. 219 (15), 2311–2319. https://doi.org/10.1242/jeb.135566 (2016).
doi: 10.1242/jeb.135566 pubmed: 27489217
Wick, C., Böl, M., Müller, F., Blickhan, R. & Siebert, T. Packing of muscles in the rabbit shank influences three-dimensional architecture of M. soleus. J. Mech. Behav. Biomed. Mater. 83, 20–27. https://doi.org/10.1016/j.jmbbm.2018.04.006 (2018).
doi: 10.1016/j.jmbbm.2018.04.006 pubmed: 29656240

Auteurs

Corinna Coenning (C)

Institute of Sports Science, Eberhard Karls University, Wilhelmstraße 124, 72074, Tubingen, Germany.

Volker Rieg (V)

Institute of Sports Science, Eberhard Karls University, Wilhelmstraße 124, 72074, Tubingen, Germany. volker.rieg@uni-tuebingen.de.

Tobias Siebert (T)

Department of Motion and Exercise Science, University of Stuttgart, Stuttgart, Germany.
Stuttgart Center of Simulation Science, University of Stuttgart, Stuttgart, Germany.

Veit Wank (V)

Institute of Sports Science, Eberhard Karls University, Wilhelmstraße 124, 72074, Tubingen, Germany.

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