Dynamic MR Imaging of the Skeletal Musculature: From Static Measures to a Dynamic Assessment of the Muscular (Loco-) Motion

Part of the Medical Radiology book series (MEDRAD)


The muscle–tendon is a complex structure and involves the complex interplay of passive and active elements, fiber architecture that ultimately determines the force transmission and muscle mechanics. The ability to noninvasively image the muscle–tendon complex during contractions provides an unprecedented tool to study the normal physiology and its changes under different conditions (e.g., in normal aging, sarcopenia, limb disuse and muscle atrophy, and muscle diseases such as dystrophy). We describe the development of sophisticated MR imaging sequences that can directly map muscle motion (velocity), or muscle tissue displacement. A brief overview of imaging sequences, post processing is provided as a background to the technology. The derivation of 1D, 2D and 3D strain, and strain rate maps is outlined underlying the ability to extract the complete 3D strain tensor from appropriate MR datasets. The MR-compatible device to enable different muscle motion is described in detail; this piece is critical for the successful implementation of functional muscle dynamics using MRI. Velocity and strain distributions in the normal lower leg muscles, in the forearm are presented. These studies highlight the heterogeneous strain distributions and the link to connective tissue distribution in the muscles as well as to the geometry of the fibers (fiber length, pennation angle, and curvature differences along the length the muscle aponeurosis). These studies have also identified inter- and intra-fascicular heterogeneities in strain and in novel indices such as the architectural gear ratio. Tendon dynamics can also be mapped using the velocity-encoded data and force-dependent length changes, stiffness, and the transition point from linear to nonlinear behavior of the force-length (F-L) curve in human Achilles tendon are discussed. The applications of these elegant MR techniques to altered muscle conditions are presented; however the number of studies is limited. The application of MR dynamic muscle imaging with the velocity encoded-phase contrast imaging to subjects with Achilles tendon rupture and chronic unloading under controlled conditions are presented. In both applications, the utility of the technique in identifying muscle functional and structural changes indicate that this is a valuable tool awaiting widespread clinical implementation. This chapter concludes with technical developments in this area of MR imaging where 2D and 3D strain tensor mappings are outlined. These developments offer exciting possibilities to explore muscle structure and functional relationships. Coupled with diffusion tensor imaging to extract muscle fiber architecture, dynamic 3D muscle imaging will enable the detailed understanding of muscle physiology in normal and altered conditions.


Achilles Tendon Isometric Contraction Medial Gastrocnemius Strain Rate Tensor Pennation Angle 


  1. Aagaard P, Andersen JL, Dyhre-Poulsen P, Leffers AM, Wagner A, Magnusson SP, Halkjaer-Kristensen J, Simonsen EB (2001) A mechanism for increased contractile strength of human pennate muscle in response to strength training: changes in muscle architecture. J Physiol 534:613–623. PMID-11454977Google Scholar
  2. Akima H, Kawakami Y, Kubo K, Sekiguchi C, Ohshima H, Miyamoto A, Fukunaga T (2000) Effect of short-duration spaceflight on thigh and leg muscle volume. Med Sci Sports Exerc 32:1743–1747. PMID-11039647Google Scholar
  3. Abe T, Fukashiro S, Harada Y, Kawamoto K (2001) Relationship between sprint performance and muscle fascicle length in female sprinters. J Physiol Anthropol Appl Human Sci 20:141–147. PMID-11385937Google Scholar
  4. Axel L, Dougherty L (1989) Heart wall motion: improved method of spatial modulation of magnetization for MR imaging. Radiology 171:841–845PubMedGoogle Scholar
  5. Benjamin M, Ralphs JR (1997) Tendons and ligaments—an overview. Histol Histopathol 12:1135–1144. doi: 10.1016/j.ejcb.2006.06.002 PubMedGoogle Scholar
  6. Biewener AA, Corning WR, Tobalske BW (1998) In vivo pectoralis muscle force-length behavior during level flight in pigeons (Columba livia) J Exp Biol 201(Pt 24):3293–3307 PMID-9817827Google Scholar
  7. Blemker SS, Pinsky PM, Delp SL (2005) A 3D model of muscle reveals the causes of nonuniform strains in the biceps brachii. J Biomech 38:657–665. doi: 10.1016/j.jbiomech.2004.04.009 PubMedCrossRefGoogle Scholar
  8. Brossmann J, Muhle C, Schroder C, Melchert UH, Bull CC, Spielmann RP, Heller M (1993) Patellar tracking patterns during active and passive knee extension: evaluation with motion-triggered cine MR imaging. Radiology 187:205–212. PMID-8451415Google Scholar
  9. Caiozzo VJ, Baker MJ, Herrick RE, Tao M, Baldwin KM (1994) Effect of spaceflight on skeletal muscle: mechanical properties and myosin isoform content of a slow muscle. J Appl Physiol 76:1764–1773PubMedCrossRefGoogle Scholar
  10. Drace JE, Pelc NJ (1994a) Measurement of skeletal muscle motion in vivo with phase-contrast MR imaging. J Magn Reson Imaging 4:157–163PubMedCrossRefGoogle Scholar
  11. Drace JE, Pelc NJ (1994b) Skeletal muscle contraction: analysis with use of velocity distributions from phase-contrast MR imaging. Radiology 193:423–429PubMedGoogle Scholar
  12. Drace JE, Pelc NJ (1994c) Tracking the motion of skeletal muscle with velocity-encoded MR imaging. J Magn Reson Imaging 4:773–778PubMedCrossRefGoogle Scholar
  13. Drace JE, Pelc NJ (1994d) Elastic deformation in tendons and myotendinous tissue: measurement by phase-contrast MR imaging. Radiology 191:835–839PubMedGoogle Scholar
  14. Englund EK, Elder CP, Xu Q, Ding Z, Damon BM (2011) Combined diffusion and strain tensor MRI reveals a heterogeneous, planar pattern of strain development during isometric muscle contraction. Am J Physiol Regul Integr Comp Physiol 300:R1079–R1090. doi: 10.1152/ajpregu.0 0474.2010PubMedCentralPubMedCrossRefGoogle Scholar
  15. Edgerton VR, Roy RR (1996) Neuromuscular adaptations to actual and simulated spaceflight. In: Handbook of physiology, environmental phsyiology. Am Physiol Soc Bethesda, MD p 721–763Google Scholar
  16. Finni T, Hodgson JA, Lai AM, Edgerton VR, Sinha S (2003a) Nonuniform strain of human soleus aponeurosis-tendon complex during submaximal voluntary contractions in vivo. J Appl Physiol 95:829–837. doi: 10.1152/japplphysiol.0 0775.2002PubMedGoogle Scholar
  17. Finni T, Hodgson JA, Lai AM, Edgerton VR, Sinha S (2003b) Mapping of movement in the isometrically contracting human soleus muscle reveals details of its structural and functional complexity. J Appl Physiol 95:2128–2133. doi: 10.1152/japplphysiol.0 0596.2003PubMedGoogle Scholar
  18. Finni T, Hodgson JA, Lai AM, Edgerton VR, Sinha S (2006) Muscle synergism during isometric plantarflexion in achilles tendon rupture patients and in normal subjects revealed by velocity-encoded cine phase-contrast MRI. 21:67–74, Clin Biomech (Bristol, Avon). doi: 10.1016/j.clinbiomech.2005.08.007
  19. Finni T, Havu M, Sinha S, Usenius JP, Cheng S (2008) Mechanical behavior of the quadriceps femoris muscle tendon unit during low-load contractions. J Appl Physiol 104:1320–1328. doi: 10.1152/japplphysiol.0 1069.2007PubMedCrossRefGoogle Scholar
  20. Fukunaga T, Ichinose Y, Ito M, Kawakami Y, Fukashiro S (1997) Determination of fascicle length and pennation in a contracting human muscle in vivo. J Appl Physiol 82:354–358. PMID-9029238Google Scholar
  21. Fukunaga T, Kubo K, Kawakami Y, Fukashiro S, Kanehisa H, Maganaris CN (2001) In vivo behaviour of human muscle tendon during walking. Proc Biol Sci 268:229–233. doi: 10.1098/rspb.2000.1361 Google Scholar
  22. Garrett WE Jr (1996) Muscle strain injuries. Am J Sports Med 24(Suppl):S2S88. PMID: 8947416Google Scholar
  23. Greenleaf JE, Bulbulian R, Bernauer EM, Haskell WL, Moore T (1989) Exercise-training protocols for astronauts in microgravity. J Appl Physiol 67:2191–2204PubMedGoogle Scholar
  24. Griffiths RI (1991) Shortening of muscle fibres during stretch of the active cat medial gastrocnemius muscle: the role of tendon compliance J Physiol 436:219–236. PMID-2061831Google Scholar
  25. Hodgson JA, Finni T, Lai AM, Edgerton VR, Sinha S (2006) Influence of structure on the tissue dynamics of the human soleus muscle observed in MRI studies during isometric contractions. J Morphol 267:584–601. doi: 10.1002/jmor.10421 PubMedCrossRefGoogle Scholar
  26. Jenkyn TR, Koopman B, Huijing P, Lieber RL, Kaufman KR (2002) Finite element model of intramuscular pressure during isometric contraction of skeletal muscle. Phys Med Biol 47:4043–4061PubMedCrossRefGoogle Scholar
  27. Jaspers RT, Brunner R, Pel JJ, Huijing, PA (1999) Acute effects of intramuscular aponeurotomy on rat gastrocnemius medialis: force transmission, muscle force and sarcomere length. J Biomech 32:71–79. PMID-10050953Google Scholar
  28. Jaspers RT, Brunner R, Baan GC, Huijing PA (2002) Acute effects of intramuscular aponeurotomy and tenotomy on multitendoned rat EDL: indications for local adaptation of intramuscular connective tissue. Anat Rec 266:123–135. PMID-11788946Google Scholar
  29. Kawakami Y, Abe T, Fukunaga T (1993) Muscle-fiber pennation angles are greater in hypertrophied than in normal muscles. J Appl Physiol 74:2740–2744. PMID-8365975Google Scholar
  30. Kawakami Y, Muraoka Y, Kubo K, Suzuki Y, Fukunaga T (2000) Changes in muscle size and architecture following 20 days of bed rest. J Gravit Physiol 7:53–59. PMID-12124185Google Scholar
  31. Kibler WB (1990) Clinical aspects of muscle injury. Med Sci Sports Exerc 22:450–452. PMID-2402204Google Scholar
  32. Kinugasa R, Shin D, Yamauchi J, Mishra C, Hodgson JA, Edgerton VR, Sinha S (2008) Phase-contrast MRI reveals mechanical behavior of superficial and deep aponeuroses in human medial gastrocnemius during isometric contraction. J Appl Physiol 105:1312–1320. doi: 10.1152/japplphysiol.9 0440.2008PubMedCentralPubMedCrossRefGoogle Scholar
  33. Kinugasa R, Hodgson JA, Edgerton VR, Shin DD, Sinha S (2010) Reduction in tendon elasticity from unloading is unrelated to its hypertrophy. J Appl Physiol 109:870–877. doi: 10.1152/japplphysiol.0 0384.2010PubMedCentralPubMedCrossRefGoogle Scholar
  34. Kinugasa R, Hodgson JA, Edgerton VR, Sinha S (2012) Asymmetric deformation of contracting human gastrocnemius muscle. J Appl Physiol 112:463–470. doi: 10.1152/japplphysiol.0 0666.2011PubMedCentralPubMedCrossRefGoogle Scholar
  35. Lee HD, Finni T, Hodgson JA, Lai AM, Edgerton VR, Sinha S (2006) Soleus aponeurosis strain distribution following chronic unloading in humans: an in vivo MR phase-contrast study. J Appl Physiol 100:2004–2011. doi: 10.1152/japplphysiol.0 1085.2005PubMedCrossRefGoogle Scholar
  36. Lingamneni A, Hardy PA, Powell KA, Pelc NJ, White RD (1995) Validation of cine phase-contrast MR imaging for motion analysis. J Magn Reson Imaging 5:331–338. PMID-7633111Google Scholar
  37. Lieber RL (1993) Skeletal muscle architecture: implications for muscle function and surgical tendon transfer. J Hand Ther 6:105–113. PMID-8343877Google Scholar
  38. Narici MV, Binzoni T, Hiltbrand E, Fasel J, Terrier F, Cerretelli P (1996) In vivo human gastrocnemius architecture with changing joint angle at rest and during graded isometric contraction. J Physiol 496(Pt 1):287–297. PMID-8910216Google Scholar
  39. Narici M, Cerretelli P (1998) Changes in human muscle architecture in disuse-atrophy evaluated by ultrasound imaging. J Gravit Physiol 5:P73-P74. PMID-11542371Google Scholar
  40. Narici MV, Reeves ND, Morse CI, Maganaris CN (2004) Muscular adaptations to resistance exercise in the elderly. J Musculoskelet Neuronal Interact 4:161–164. PMID-15615118Google Scholar
  41. Niitsu M, Campeau NG, Holsinger BA, Riederer SJ, Ehman RL (1992) Tracking motion with tagged rapid gradient-echo magnetizationprepared MR imaging. J Magn Reson Imaging 2:155–163. PMID-1562766Google Scholar
  42. Noonan TJ, Best TM, Seaber AV, Garrett WE Jr (1994) Identification of a threshold for skeletal muscle injury. Am J Sports Med 22:257–261. PMID-8198196Google Scholar
  43. Pappas GP, Asakawa DS, Delp SL, Zajac FE, Drace JE (2002) Nonuniform shortening in the biceps brachii during elbow flexion. J Appl Physiol 92:2381–2389. doi: 10.1152/japplphysiol.0 0843.2001PubMedGoogle Scholar
  44. Pipe JG, Boes JL, Chenevert TL (1991) Method for measuring three-dimensional motion with tagged MR-imaging. Radiology 181:591–595. PMID-1924810Google Scholar
  45. Proske U, Morgan DL (1987) Tendon stiffness: methods of measurement and significance for the control of movement. A rev J Biomech 20:75–82. PMID-3558432Google Scholar
  46. Reeves ND, Maganaris CN, Ferretti G, Narici MV (2005) Influence of 90 day simulated microgravity on human tendon mechanical properties and the effect of resistive countermeasures. J Appl Physiol 98:2278–2286. doi: 10.1152/japplphysiol.0 1266.2004PubMedCrossRefGoogle Scholar
  47. Riley DA, Bain JL, Thompson JL, Fitts RH, Widrick JJ, Trappe SW, Trappe TA, Costill DL (2000) Decreased thin filament density and length in human atrophic soleus muscle fibers after spaceflight. J Appl Physiol 88:567–572. PMID-10658024Google Scholar
  48. Roberts TJ, Marsh RL, Weyand PG, Taylor CR (1997) Muscular force in running turkeys: the economy of minimizing work. Science 275:1113–1115. PMID-9027309Google Scholar
  49. Sheehan FT, Zajac FE, Drace JE (1999) In vivo tracking of the human patella using cine phase contrast magnetic resonance imaging. J Biomech Eng. 121:650–656. PMID-10633267Google Scholar
  50. Sheehan FT, Drace JE (2000) Human patellar tendon strain. A noninvasive, in vivo study. Clin Orthop Relat Res 370:201–207. PMID-10660714Google Scholar
  51. Shellock FG, Stone KR, Crues JV (1999) Development and clinical application of kinematic MRI of the patellofemoral joint using an extremity MR system. Med Sci Sports Exerc. 31:788–791. PMID-10378904Google Scholar
  52. Shin DD, Hodgson JA, Edgerton VR, Sinha S (2009) In vivo intramuscular fascicle-aponeuroses dynamics of the human medial gastrocnemius during plantarflexion and dorsiflexion of the foot. J Appl Physiol 107:1276–1284. doi: 10.1152/japplphysiol.9 1598.2008PubMedCentralPubMedCrossRefGoogle Scholar
  53. Shin D, Finni T, Ahn S, Hodgson JA, Lee HD, Edgerton VR, Sinha S (2008) In vivo estimation and repeatability of force-length relationship and stiffness of the human achilles tendon using phase contrast MRI. J Magn Reson Imaging 28:1039–1045. doi: 10.1002/jmri.21533 PubMedCentralPubMedCrossRefGoogle Scholar
  54. Sinha S, Hodgson JA, Finni T, Lai AM, Grinstead J, Edgerton VR (2004) Muscle kinematics during isometric contraction: development of phase contrast and spin tag techniques to study healthy and atrophied muscles. J Magn Reson Imaging 20:1008–1019. doi: 10.1002/jmri.20210 PubMedCrossRefGoogle Scholar
  55. Sinha S, Shin DD, Hodgson JA, Kinugasa R, Edgerton VR (2012) Computer-controlled, MR-compatible foot-pedal device to study dynamics of the muscle tendon complex under isometric, concentric, and eccentric contractions. J Magn Reson Imaging 36:498–504. doi: 10.1002/jmri.23617 PubMedCrossRefGoogle Scholar
  56. Sinha S, Moghadassi A, Malis V, Sinha U (2013) Dynamic functional imaging of quadriceps and hamstring muscles under isometric and active extension-flexion contraction. In: Proceedings of the international society mgnetic resonance medicine, 21:3481, Salt Lake, Utah, April 20–26Google Scholar
  57. Steffen JM, Musacchia XJ (1986) Spaceflight effects on adult rat muscle protein, nucleic acids, and amino acids. Am J Physiol Regul Integr Comp Physiol 251:R1059–R1063. PMID-2431627Google Scholar
  58. Widrick JJ, Knuth ST, Norenberg KM, Romatowski JG, Bain JL, Riley DA, Karhanek M, Trappe SW, Trappe TA, Costill DL, Fitts RH (1999) Effect of a 17 day spaceflight on contractile properties of human soleus muscle fibres. J Physiol 516:915–930. PMID-2431627Google Scholar
  59. Yucesoy CA, Koopman BH, Huijing PA, Grootenboer HJ (2002) Three-dimensional finite element modeling of skeletal muscle using a two domain approach: linked fiber-matrix mesh model. J Biomech 35:1253–1262. pii:S0021929002000696Google Scholar
  60. Zhong X, Epstein FH, Spottiswoode BS, Helm PA, Blemker SS (2008) Imaging two-dimensional displacements and strains in skeletal muscle during joint motion by cine DENSE MR. J Biomech 41(3):532–540. doi: 10.1016/j.jbiomech.2007.10.026 PubMedCentralPubMedCrossRefGoogle Scholar
  61. Zerhouni E, Parish D, Rogers W, Yang A, Shapiro E (1988) Human heart: tagging with MR imaging—a method for noninvasive assessment of myocardial motion. Radiology 169:59–63PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of RadiologyUniversity of CaliforniaSan DiegoUSA
  2. 2.Department of PhysicsSan Diego State UniversitySan DiegoUSA

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