|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online July 23, 2003
Muscle force-length dynamics during level versus incline locomotion: a comparison of in vivo performance of two guinea fowl ankle extensors
Concord Field Station, Department of Organismic and Evolutionary Biology, Harvard University, Bedford, MA 01730, USA
* Author for correspondence (e-mail: mdaley{at}oeb.harvard.edu)
Accepted 19 May 2003
For a terrestrial animal to move in the complex natural environment, the limb muscles must modulate force and work performance to meet changing mechanical requirements; however, it is not clear whether this is accomplished via a collective shift in function by all limb muscles, or a division of labor among limb muscles. Do muscles differ in their ability to modulate force-length contractile function to meet the mechanical demands of different locomotor tasks? We explore this question by examining the in vivo force-length performance of the guinea fowl Numida meleagris lateral gastrocnemius (LG) and digital flexor-IV (DF-IV), during level and incline locomotion. During level locomotion, the LG and DF-IV exhibit differing muscle fascicle strain patterns: the LG shortens by 10-15% while developing force, whereas the DF-IV undergoes a stretch-shorten cycle with large strain amplitudes and small net strains of 1-8%. Furthermore, the DF-IV operates at higher muscle stresses (92-130 kPa, compared to 23-39 kPa for LG) and possesses a longer tendon, which allows the DF-IV tendon to recover greater elastic energy than the LG tendon. During incline locomotion, these muscles contribute only one-third of the energy expected for their mass, with the DF-IV exhibiting high stride-to-stride variability in work output. While the stretch-shorten cycle of the DF-IV muscle may allow more economic force production, it also leads to large changes in work output with small changes in the relative timing of force and strain. Thus, while the primary determinants of LG work are net strain and mean force, the primary determinant of DF-IV work is the phase relationship between force and strain. Our results suggest that, in addition to influencing a muscle's mechanical performance during steady level locomotion, morphology also affects its capacity and mechanism for altering work output for different locomotor tasks.
Key words: muscle, strain, phase, work, sonomicrometry, gastrocnemius, digital flexor, guinea fowl, Numida meleagris
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
Related articles in JEB:
This article has been cited by other articles:
|
|
 |
|
  M. P. McGuigan, E. Yoo, D. V. Lee, and A. A. Biewener Dynamics of goat distal hind limb muscle-tendon function in response to locomotor grade J. Exp. Biol., July 1, 2009; 212(13): 2092 - 2104. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. A. Daley, A. Voloshina, and A. A. Biewener The role of intrinsic muscle mechanics in the neuromuscular control of stable running in the guinea fowl J. Physiol., June 1, 2009; 587(11): 2693 - 2707. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Rubenson and R. L. Marsh Mechanical efficiency of limb swing during walking and running in guinea fowl (Numida meleagris) J Appl Physiol, May 1, 2009; 106(5): 1618 - 1630. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. E Higham and A. A Biewener Fatigue alters in vivo function within and between limb muscles during locomotion Proc R Soc B, March 22, 2009; 276(1659): 1193 - 1197. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. S. Sawicki and D. P. Ferris Mechanics and energetics of incline walking with robotic ankle exoskeletons J. Exp. Biol., January 1, 2009; 212(1): 32 - 41. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. J. Roberts and A. M. Gabaldon Interpreting muscle function from EMG: lessons learned from direct measurements of muscle force Integr. Comp. Biol., August 1, 2008; 48(2): 312 - 320. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. E. Higham and A. A. Biewener Integration within and between muscles during terrestrial locomotion: effects of incline and speed J. Exp. Biol., July 15, 2008; 211(14): 2303 - 2316. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. F. Hodson-Tole and J. M. Wakeling Motor unit recruitment patterns 2: the influence of myoelectric intensity and muscle fascicle strain rate J. Exp. Biol., June 15, 2008; 211(12): 1893 - 1902. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. M. Berg and A. A. Biewener Kinematics and power requirements of ascending and descending flight in the pigeon (Columba livia) J. Exp. Biol., April 1, 2008; 211(7): 1120 - 1130. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. E Higham, A. A Biewener, and J. M Wakeling Functional diversification within and between muscle synergists during locomotion Biol Lett, February 23, 2008; 4(1): 41 - 44. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. R. Carrier, S. M. Deban, and T. Fischbein Locomotor function of forelimb protractor and retractor muscles of dogs: evidence of strut-like behavior at the shoulder J. Exp. Biol., January 1, 2008; 211(1): 150 - 162. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. M. Gabaldon, F. E. Nelson, and T. J. Roberts Relative shortening velocity in locomotor muscles: turkey ankle extensors operate at low V/Vmax Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2008; 294(1): R200 - R210. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. DeVita, J. Helseth, and T. Hortobagyi Muscles do more positive than negative work in human locomotion J. Exp. Biol., October 1, 2007; 210(19): 3361 - 3373. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. T. Richards and A. A. Biewener Modulation of in vivo muscle power output during swimming in the African clawed frog (Xenopus laevis) J. Exp. Biol., September 15, 2007; 210(18): 3147 - 3159. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. A. Biewener and M. A. Daley Unsteady locomotion: integrating muscle function with whole body dynamics and neuromuscular control J. Exp. Biol., September 1, 2007; 210(17): 2949 - 2960. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. J. Roberts, B. K. Higginson, F. E. Nelson, and A. M. Gabaldon Muscle strain is modulated more with running slope than speed in wild turkey knee and hip extensors J. Exp. Biol., July 15, 2007; 210(14): 2510 - 2517. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Nishikawa, A. A. Biewener, P. Aerts, A. N. Ahn, H. J. Chiel, M. A. Daley, T. L. Daniel, R. J. Full, M. E. Hale, T. L. Hedrick, et al. Neuromechanics: an integrative approach for understanding motor control Integr. Comp. Biol., July 1, 2007; 47(1): 16 - 54. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. F. Hodson-Tole and J. M. Wakeling Variations in motor unit recruitment patterns occur within and between muscles in the running rat (Rattus norvegicus) J. Exp. Biol., July 1, 2007; 210(13): 2333 - 2345. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. P. McGowan, R. V. Baudinette, and A. A. Biewener Modulation of proximal muscle function during level versus incline hopping in tammar wallabies (Macropus eugenii) J. Exp. Biol., April 1, 2007; 210(7): 1255 - 1265. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. Daley, G. Felix, and A. A. Biewener Running stability is enhanced by a proximo-distal gradient in joint neuromechanical control J. Exp. Biol., February 1, 2007; 210(3): 383 - 394. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. A. Daley and A. A. Biewener Running over rough terrain reveals limb control for intrinsic stability PNAS, October 17, 2006; 103(42): 15681 - 15686. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. J. Dutto, D. F. Hoyt, H. M. Clayton, E. A. Cogger, and S. J. Wickler Joint work and power for both the forelimb and hindlimb during trotting in the horse J. Exp. Biol., October 15, 2006; 209(20): 3990 - 3999. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. R. Lammers, K. D. Earls, and A. R. Biknevicius Locomotor kinetics and kinematics on inclines and declines in the gray short-tailed opossum Monodelphis domestica J. Exp. Biol., October 15, 2006; 209(20): 4154 - 4166. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. P. McGowan, H. A. Duarte, J. B. Main, and A. A. Biewener Effects of load carrying on metabolic cost and hindlimb muscle dynamics in guinea fowl (Numida meleagris) J Appl Physiol, October 1, 2006; 101(4): 1060 - 1069. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Rubenson, H. T. Henry, P. M. Dimoulas, and R. L. Marsh The cost of running uphill: linking organismal and muscle energy use in guinea fowl (Numida meleagris) J. Exp. Biol., July 1, 2006; 209(13): 2395 - 2408. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. R. Carrier, S. M. Deban, and T. Fischbein Locomotor function of the pectoral girdle `muscular sling' in trotting dogs J. Exp. Biol., June 1, 2006; 209(11): 2224 - 2237. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Autumn, S. T. Hsieh, D. M. Dudek, J. Chen, C. Chitaphan, and R. J. Full Dynamics of geckos running vertically J. Exp. Biol., January 15, 2006; 209(2): 260 - 272. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. Daley, J. R. Usherwood, G. Felix, and A. A. Biewener Running over rough terrain: guinea fowl maintain dynamic stability despite a large unexpected change in substrate height J. Exp. Biol., January 1, 2006; 209(1): 171 - 187. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. B. Gillis, J. P. Flynn, P. McGuigan, and A. A. Biewener Patterns of strain and activation in the thigh muscles of goats across gaits during level locomotion J. Exp. Biol., December 15, 2005; 208(24): 4599 - 4611. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. A. Butterfield and W. Herzog Quantification of muscle fiber strain during in vivo repetitive stretch-shortening cycles J Appl Physiol, August 1, 2005; 99(2): 593 - 602. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. P. McGowan, R. V. Baudinette, J. R. Usherwood, and A. A. Biewener The mechanics of jumping versus steady hopping in yellow-footed rock wallabies J. Exp. Biol., July 15, 2005; 208(14): 2741 - 2751. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. J. Roberts and R. A. Belliveau Sources of mechanical power for uphill running in humans J. Exp. Biol., May 15, 2005; 208(10): 1963 - 1970. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. A. Biewener Biomechanical consequences of scaling J. Exp. Biol., May 1, 2005; 208(9): 1665 - 1676. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Pontzer A new model predicting locomotor cost from limb length via force production J. Exp. Biol., April 15, 2005; 208(8): 1513 - 1524. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. J Ellerby, H. T Henry, J. A Carr, C. I Buchanan, and R. L Marsh Blood flow in guinea fowl Numida meleagris as an indicator of energy expenditure by individual muscles during walking and running J. Physiol., April 15, 2005; 564(2): 631 - 648. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. J. Wickler, D. F. Hoyt, A. A. Biewener, E. A. Cogger, and K. L. De La Paz In vivo muscle function vs speed II. Muscle function trotting up an incline J. Exp. Biol., March 15, 2005; 208(6): 1191 - 1200. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Soman, T. L. Hedrick, and A. A. Biewener Regional patterns of pectoralis fascicle strain in the pigeon Columba livia during level flight J. Exp. Biol., February 15, 2005; 208(4): 771 - 786. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. P. McGowan, R. V. Baudinette, and A. A. Biewener Joint work and power associated with acceleration and deceleration in tammar wallabies (Macropus eugenii) J. Exp. Biol., January 1, 2005; 208(1): 41 - 53. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. J. Roberts and J. A. Scales Adjusting muscle function to demand: joint work during acceleration in wild turkeys J. Exp. Biol., November 1, 2004; 207(23): 4165 - 4174. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. M. Gabaldon, F. E. Nelson, and T. J. Roberts Mechanical function of two ankle extensors in wild turkeys: shifts from energy production to energy absorption during incline versus decline running J. Exp. Biol., June 1, 2004; 207(13): 2277 - 2288. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. A. Biewener, C. McGowan, G. M. Card, and R. V. Baudinette Dynamics of leg muscle function in tammar wallabies (M. eugenii) during level versus incline hopping J. Exp. Biol., January 15, 2004; 207(2): 211 - 223. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. E. Higham and B. C. Jayne In vivo muscle activity in the hindlimb of the arboreal lizard, Chamaeleo calyptratus: general patterns and the effects of incline J. Exp. Biol., January 15, 2004; 207(2): 249 - 261. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Phillips MOUNTING MUSCLE MODULATION J. Exp. Biol., September 1, 2003; 206(17): 2903 - 2903. [Full Text] [PDF]
|
|
