Functional and architectural complexity within and between muscles: Regional variation and intermuscular force transmission

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 366, Issue 1570, 2011, Pages 1477-1487

  Higham, Timothy E ^a   Biewener, Andrew A ^b  

^a CLEMSON UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

Guinea fowl; Heterogeneity; Locomotion; Muscle architecture; Muscle mechanics; Running

Indexed keywords

BIOMECHANICS; GAMEBIRD; HETEROGENEITY; LOCOMOTION; MUSCLE;

NUMIDA MELEAGRIS;

EID: 79955401304     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2010.0359     Document Type: Article

References (73)

1. Biewener, A. A. 2003 Animal locomotion eds P. Willmer & D. Norman. Oxford, UK: Oxford University Press.
2. Nishikawa, K. C. et al. 2007 Neuromechanics: an integrative approach for understanding motor control. Integr. Comp. Biol. 47, 16-54. doi:10.1093/icb/icm024
3. Alexander, R. M. 2003 Principles of animal locomotion. Princeton, NJ: Princeton University Press.
4. Vogel, S. 2001 Prime mover: a natural history of muscle. New York, NY: W.W. Norton & Company, Inc.
5. Pettigrew, J. B. 1874 Animal locomotion or walking, swimming and flying with a dissertation on aeronautics. New York, NY: D. Appleton & Company.
6. Marey, E. J. 1901 Animal mechanism: a treatise on terrestrial and aerial locomotion. New York, NY: D. Appleton & Company.
7. Higham, T. E. & Biewener, A. A. 2008 Integration within and between muscles during terrestrial locomotion: effects of incline and speed. J. Exp. Biol. 211, 2303-2316. doi:10.1242/jeb.016139
8. Higham, T. E., Biewener, A. A. & Wakeling, J. M. 2008 Functional diversification within and between muscle synergists during locomotion. Biol. Lett. 4, 41-44. doi:10.1098/rsbl.2007.0472
9. English, A. W. 1984 An electromyographic analysis of compartments in cat lateral gastrocnemius muscle during unrestrained locomotion. J. Neurophysiol. 52, 114-125.
10. Soman, A., Hedrick, T. L. & Biewener, A. A. 2005 Regional patterns of pectoralis fascicle strain in the pigeon Columba livia during level flight. J. Exp. Biol. 208, 771-786. doi:10.1242/jeb.01432
11. Pappas, G. P., Asakawa, D. S., Delp, S. L., Zajac, F. E. & Drace, J. E. 2002 Nonuniform shortening in the biceps brachii during elbow flexion. J. Appl. Physiol. 92, 2381-2389. doi:10.1152/japplphysiol.00843.2001
12. Thompson, J. T., Szczepanski, J. A. & Brody, J. 2008 Mechanical specialization of the obliquely striated circular mantle muscle fibres of the long-finned squid Doryteuthis pealeii. J. Exp. Biol. 211, 1463-1474. doi:10.1242/jeb.017160
13. Ahn, A. N., Monti, R. J. & Biewener, A. A. 2003 In vivo and in vitro heterogeneity of segment length changes in the semimembranosus muscle of the toad. J. Physiol. 549, 877-888. doi:10.1113/jphysiol.2002.038018
14. Wakeling, J. M. 2009 The recruitment of different compartments within a muscle depends on the mechanics of the movement. Biol. Lett. 5, 30-34. doi:10.1098/rsbl. 2008.0459
15. Nelson, F. E. & Jayne, B. C. 2001 The effects of speed on the in vivo activity and length of a limb muscle during the locomotion of the iguanian lizard Dipsosaurus dorsalis. J. Exp. Biol. 204, 3507-3522.
16. Roy, R. R., Hutchison, D. L., Pierotti, D. J., Hodgson, J. A. & Edgerton, V. R. 1991 EMG patterns of rat ankle extensors and flexors during treadmill locomotion and swimming. J. Appl. Physiol. 70, 2522-2529.
17. Ritruechai, P., Weller, R. & Wakeling, J. M. 2008 Regional variations in muscle anatomy in the equine lognissimus dorsi. Equine Vet. J. 40, 246-251. doi:10.2746/042516408X273675
18. Prilutsky, B. I., Herzog, W. & Allinger, T. L. 1996 Mechanical power and work of cat soleus, gastrocnemius and plantaris muscles during locomotion: possible functional significance of muscle design and force patterns. J. Exp. Biol. 199, 801-814.
19. Herzog, W., Zatsiorsky, V., Prilutsky, B. I. & Leonard, T. R. 1994 Variations in force-time histories of cat gastrocnemius, soleus and plantaris for consecutive walking steps. J. Exp. Biol. 191, 19-36.
20. Prilutsky, B. I., Herzog, W. & Allinger, T. L. 1997 Forces of individual cat ankle extensor muscles during locomotion predicted using static optimization. J. Biomech. 30, 1025-1033. doi:10.1016/S0021-92909700068-7
21. Daley, M. A. & Biewener, A. A. 2003 Muscle force- length dynamics during level versus incline locomotion: a comparison of in vivo performance of two guinea fowl ankle extensors. J. Exp. Biol. 206, 2941-2958. doi:10.1242/jeb.00503
22. Herbert, R. D., Hoang, P. D. & Gandevia, S. C. 2008 Are muscles mechanically independent? J. Appl. Physiol. 104, 1549-1550. doi:10.1152/japplphysiol.90511.2008
23. Huijing, P. A. 2003 Muscular force transmission necessitates a multilevel integrative approach to the analysis of function of skeletal muscle. Exerc. Sport Sci. Rev. 31, 167-175. doi:10.1097/00003677-200310000-00003
24. Huijing, P. A. & Baan, G. C. 2001 Myofascial force transmission causes interaction between adjacent muscles and connective tissue: effects of blunt dissection and compartmental fasciotomy on length force characteristics of rat extensor digitorum longus muscle. Arch. Physiol. Biochem. 109, 97-109. doi:10.1076/apab.109.2.97.4269
25. Huijing, P. A. & Baan, G. C. 2003 Myofascial force transmission: muscle relative position and length determine agonist and synergist muscle force. J. Appl. Physiol. 94, 1092-1107. doi:10.1152/japplphysiol.00173.2002
26. Maas, H. & Sandercock, T. G. 2008 Are skeletal muscles independent actuators? Force transmission from soleus muscle in the cat. J. Appl. Physiol. 104, 1557-1567. doi:10.1152/japplphysiol.01208.2007
27. Ellerby, D. J. & Marsh, R. L. 2010 The mechanical function of linked muscles in the guinea fowl hind limb. J. Exp. Biol. 213, 2201-2208. doi:10.1242/jeb.038406
28. Herring, S.W., Grimm, A. F. & Grimm, B. R. 1979 Functional heterogeneity in amultipinnatemuscle.Am. J. Anat. 154, 563-576. doi:10.1002/aja.1001540410
29. Hodson-Tole, E. F. & Wakeling, J. M. 2007 Variations in motor unit recruitment patterns occur within and between muscles in the running rat Rattus norvegicus. J. Exp. Biol. 210, 2333-2345. doi:10.1242/jeb.004457
30. Chanaud, C. M. & Macpherson, J. M. 1991 Functionally complex muscles of the cat hindlimb. III. Differential activation within biceps femoris during postural perturbations. Exp. Brain Res. 85, 271-280. doi:10.1007/BF00229406
31. Herrel, A., Schaerlaeken, V., Ross, C., Meyers, J. J., Nishikawa, K. C., Abdala, V., Manzano, A. & Aerts, P. 2008 Electromyography and the evolution of motor control: limitations and insights. Integr. Comp. Biol. 48, 261-271. doi:10.1093/icb/icn025
32. Phanachet, I., Whittle, T., Wanigaratne, K., Klineberg, I. J., Sessle, B. J. & Murray, G. M. 2003 Functional heterogeneity in the superior head of the human lateral pterygoid. J. Dent. Res. 82, 106-111. doi:10.1177/154405910308200206
33. Carrasco, D. I., Lawrence, J. & English, A.W. 1999 Neuromuscular compartments of cat lateral gastrocnemius produce different torques about the ankle joint. Motor Control 3, 436-446.
34. Korfage, J. A.M., Koolstra, J. H., Langenbach, G. E. J. & van Eijden, T. M. G. J. 2005 Fiber-type composition of the human jaw muscles. I. Origin and functional significance of fiber-type diversity. J. Dent. Res. 84, 774-783. doi:10.1177/154405910508400901
35. Wang, L. & Kernell, D. 2000 Proximo-distal organization and fibre type regionalization in rat hindlimb muscles. J. Muscle Res. Cell Motil. 21, 587-598. doi:10.1023/A:1026584307999
36. Mu, L. & Sanders, I. 2001 Neuromuscular compartments and fiber-type regionalization in the human inferior pharyngeal constrictor muscle. Anat. Rec. 264, 367-377. doi:10.1002/ar.10020
37. Chanaud, C. M., Pratt, C. A. & Loeb, G. E. 1991 Functionally complex muscles of the cat hindlimb. II. Mechanical and architectural heterogeneity within the biceps femoris. Exp. Brain Res. 85, 257-270. doi:10.1007/BF00229405
38. van Eijden, T. M. G. J. & Raadsheer, M. C. 1992 Heterogeneity of fiber and sarcomere length in the human masseter muscle. Anat. Rec. 232, 78-84. doi:10.1002/ar.1092320109
39. Stark, H. & Schilling, N. 2010 A novel method of studying fascicle architecture in relaxed and contracted muscles. J. Biomech. 43, 2897-2903. doi:10.1016/j.jbiomech.2010.07.031
40. Lichtwark, G. A., Bougoulias, K. & Wilson, A. M. 2007 Muscle fascicle and series elastic element length changes along the length of the human gastocnemius during walking and running. J. Biomech. 40, 157-164. doi:10.1016/j.jbiomech.2005.10.035
41. Drost, M. R., Maenhout, M., Willems, P. J. B., Oomens, C. W. J., Baaijens, F. P. T. & Hesselink, M. K. C. 2003 Spatial and temporal heterogeneity of superficial muscle strain during in situ fixed-end contractions. J. Biomech. 36, 1055-1063. doi:10.1016/S0021-92900200461-X
42. Konow, N., Thexton, A. J., Crompton, A. W. & German, R. Z. 2010 Regional differences in length-change and electromyographic heterogeneity in sternohyoid muscle during infant mammalian swallowing. J. Appl. Physiol. 109, 439-448. doi:10.1152/japplphysiol.00353.2010
43. Blemker, S. S., Asakawa, D. S., Gold, G. E. & Delp, S. L. 2007 Image-based musculoskeletal modeling: applications, advances, and future opportunities. J. Magn. Reson. Imaging 25, 441-451. doi:10.1002/jmri.20805
44. Blemker, S. S., Pinsky, P. M. & Delp, S. L. 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
45. De Ruiter, C. J., Habets, P. E. M. H., De Haan, A. & Sargeant, A. J. 1996 In vivo IIX and IIB fiber recruitment in gastrocnemius muscle of the rat is compartment related. J. Appl. Physiol. 81, 933-942.
46. Scholle, H. C., Schumann, N. P., Biedermann, F., Stegeman, D. F., Graßme, R., Roeleveld, K., Schilling, N. & Fisher, M. S. 2001 Spatiotemporal surface EMG characteristics from rat triceps brachii muscle during treadmill locomotion indicate selective recruitment of functionally distinct muscle regions. Exp. Brain Res. 138, 26-36. doi:10.1007/s002210100685
47. Hoffer, J. A., Loeb, G. E., Sugano, N., Marks, W. B., O'Donovan, M. J. & Pratt, C. A. 1987 Cat hindlimb motoneurons during locomotion. III. Functional segregation in sartorius. J. Neurophysiol. 57, 554-562.
48. De Ruiter, C. J., De Haan, A. & Sargeant, A. J. 1995 Physiological characteristics of two extreme muscle compartments in gastrocnemius medialis of the anaesthetized rat. Acta Physiol. Scand. 153, 313-324. doi:10.1111/j.1748-1716.1995.tb09869.x
49. Monti, R. J., Roy, R. R. & Edgerton, V. R. 2001 Role of motor unit structure in defining function. Muscle Nerve 24, 848-866. doi:10.1002/mus.1083
50. Weeks, O. I. & English, A. W. 1985 Compartmentalization of the cat lateral gastrocnemius motor nucleus. J. Comp. Neurol. 235, 255-267. doi:10.1002/cne.902350208
51. English, A. W. M. & Weeks, O. I. 1987 An anatomical and functional analysis of cat biceps femoris and semitendinosus muscles. J. Morphol. 191, 161-175. doi:10.1002/jmor.1051910207
52. Turkawski, S. J. J., van Eijden, T. M. G. J. & Weijs, W. A. 1998 Force vectors of single motor units in a multipennate muscle. J. Dent. Res. 77, 1823-1831. doi:10.1177/00220345980770101001
53. Higham, T. E. & Biewener, A. A. 2009 Fatigue alters in vivo function within and between limb muscles during locomotion. Proc. R. Soc. B 276, 1193-1197. doi:10.1098/rspb.2008.1734
54. Azizi, E. & Roberts, T. J. 2009 Biaxial strain and variable stiffness in aponeuroses. J. Physiol. 587, 4309-4318. doi:10.1113/jphysiol.2009.173690
55. Murray, W. M., Buchanan, T. S. & Delp, S. L. 2000 The isometric functional capacity of muscles that cross the elbow. J. Biomech. 33, 943-952. doi:10.1016/S0021-92900000051-8
56. Rehorn, M. R. & Blemker, S. S. 2010 The effects of aponeurosis geometry on strain injury susceptibility explored with a 3D muscle model. J. Biomech. 43, 2574-2581. doi:10.1016/j.jbiomech.2010.05.011
57. Gillis, G. B., Flynn, J. P., McGuigan, P. & Biewener, A. A. 2005 Patterns of strain and activation in the thigh muscles of goats across gaits during level locomotion. J. Exp. Biol. 208, 4599-4611. doi:10.1242/jeb.01940
58. Higham, T. E. & Nelson, F. E. 2008 The integration of lateral gastrocnemius muscle function and kinematics in running turkeys. Zoology 111, 483-493. doi:10.1016/j.zool.2008.01.001
59. Higham, T. E. & Jayne, B. C. 2004 In vivo muscle activity in the hindlimb of the arboreal lizard, Chamaeleo calyptratus: general patterns and effects of incline. J. Exp. Biol. 207, 249-261. doi:10.1242/jeb.00745
60. Flammang, B. E. & Lauder, G. V. 2009 Caudal fin shape modulation and control during acceleration, braking and backing maneuvers in bluegill sunfish, Lepomis macrochirus. J. Exp. Biol. 212, 277-286. doi:10.1242/jeb. 021360
61. Reilly, S. M. 1995 Quantitative electromyography and muscle function of the hind limb during quadrupedal running in the lizard Sceloporus clarki. Zoology 98, 263-277.
62. Rivera, A. R. V. & Blob, R. W. 2010 Forelimb kinematics and motor patterns of the slider turtle Trachemys scripta during swimming and walking: shared and novel strategies for meeting locomotor demands of water and land. J. Exp. Biol. 213, 3515-3526. doi:10.1242/jeb.047167
63. Zajac, F. E., Neptune, R. R. & Kautz, S. A. 2002 Biomechanics and muscle coordination of human walking. I. Introduction to concepts, power transfer, dynamics and simulations. Gait Posture 16, 215-232. doi:10.1016/S0966-63620200068-1
64. Maas, H., Baan, G. C. & 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, 927-940. doi:10.1016/S0021-92900100055-0
65. Marsh, R. L., Ellerby, D. J., Carr, J. A., Henry, H. T. & Buchanan, C. I. 2004 Partitioning the energetics of walking and running: swinging the limbs is expensive. Science 303, 80-83. doi:10.1126/science.1090704
66. Marsh, R. L., Ellerby, D. J., Henry, H. T. & Rubenson, J. 2006 The energetic costs of trunk and distal-limb loading during walking and running in guinea fowl Numida meleagris. I. Organismal metabolism and biomechanics. J. Exp. Biol. 209, 2050-2063. doi:10.1242/jeb.02226
67. Gatesy, S. M. 1999 Guineafowl hind limb function. I. Cineradiographic analysis and speed effects. J. Morphol. 240, 115-125. doi:10.1002/SICI1097-4687199905 240:2,115::AID-JMOR3.3.0.CO;2-Y
68. Gatesy, S. M. & Biewener, A. A. 1991 Bipedal locomotion: effects of speed, size and limb posture in birds and humans. J. Zool. Lond. 224, 127-147. doi:10. 1111/j.1469-7998.1991.tb04794.x
69. Roberts, T. J. & Gabaldon, A. M. 2008 Interpreting muscle function from EMG: lessons learned from direct measurements of muscle force. Integr. Comp. Biol. 48, 312-320. doi:10.1093/icb/icn056
70. Biewener, A. A. & Corning, W. R. 2001 Dynamics of mallard Anas platyrhynchos gastrocnemius function during swimming versus terrestrial locomotion. J. Exp. Biol. 204, 1745-1756.
71. Zar, J. H. 1996 Biostatistical analysis, 3rd edn. Upper Saddle River, NJ: Prentice Hall.
72. Daley, M. A., Felix, G. & Biewener, A. A. 2007 Running stability is enhanced by a proximo-distal gradient in joint neuromechanical control. J. Exp. Biol. 210, 383-394. doi:10.1242/jeb.02668
73. Roberts, T. J. & Scales, J. A. 2004 Adjusting muscle function to demand: joint work during acceleration in wild turkeys. J. Exp. Biol. 207, 4165-4174. doi:10.1242/jeb.01253