Unsteady locomotion: integrating muscle function with whole body dynamics and neuromuscular control.
By integrating studies of muscle function with analysis of whole body and limb dynamics, broader appreciation of neuromuscular function can be achieved. Ultimately, such studies need to address non-steady locomotor behaviors relevant to animals in their natural environments. When animals move slowly they likely rely on voluntary coordination of movement involving higher brain centers. However, when moving fast, their movements depend more strongly on responses controlled at more local levels. Our focus here is on control of fast-running locomotion. A key observation emerging from studies of steady level locomotion is that simple spring-mass dynamics, which help to economize energy expenditure, also apply to stabilization of unsteady running. Spring-mass dynamics apply to conditions that involve lateral impulsive perturbations, sudden changes in terrain height, and sudden changes in substrate stiffness or damping. Experimental investigation of unsteady locomotion is challenging, however, due to the variability inherent in such behaviors. Another emerging principle is that initial conditions associated with postural changes following a perturbation define different context-dependent stabilization responses. Distinct stabilization modes following a perturbation likely result from proximo-distal differences in limb muscle architecture, function and control strategy. Proximal muscles may be less sensitive to sudden perturbations and appear to operate, in such circumstances, under feed-forward control. In contrast, multiarticular distal muscles operate, via their tendons, to distribute energy among limb joints in a manner that also depends on the initial conditions of limb contact with the ground. Intrinsic properties of these distal muscle-tendon elements, in combination with limb and body dynamics, appear to provide rapid initial stabilizing mechanisms that are often consistent with spring-mass dynamics. These intrinsic mechanisms likely help to simplify the neural control task, in addition to compensating for delays inherent to subsequent force- and length-dependent neural feedback. Future work will benefit from integrative biomechanical approaches that employ a combination of modeling and experimental techniques to understand how the elegant interplay of intrinsic muscle properties, body dynamics and neural control allows animals to achieve stability and agility over a variety of conditions.
Biewener
Andrew A
AA
Concord Field Station, Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 01238, USA. abiewener@oeb.harvard.edu
Daley
Monica A
MA
D000818:Animals; D001696:Biomechanical Phenomena; D003198:Computer Simulation; D046094:Galliformes / Q000033:anatomy & histology / Q000502:physiology*; D006801:Humans; D007596:Joints; D008954:Models, Biological; D018482:Muscle, Skeletal / Q000502:physiology*; D004856:Postural Balance; D012420:Running / Q000502:physiology*; D009435:Synaptic Transmission
Science. 1997 Feb 21;275(5303):1113-5
9027309
J Biomech. 2007;40(1):157-64
16364330
J Exp Biol. 2003 Aug;206(Pt 15):2547-55
12819262
J Exp Biol. 1998 Dec;201(Pt 23):3185-95
9808832
Proc Biol Sci. 2003 Oct 22;270(1529):2173-83
14561282
J Exp Biol. 2006 Nov;209(Pt 21):4379-88
17050853
Am J Physiol. 1977 Nov;233(5):R243-61
411381
J Exp Biol. 2004 Jan;207(Pt 2):211-23
14668306
J Exp Biol. 1993 Dec;185:71-86
8294853
Science. 1989 Jul 7;245(4913):45-8
2740914
Science. 1973 Jul 13;181(4095):182-4
4268130
J Exp Biol. 2003 Sep;206(Pt 17):2941-58
12878663
J Neurophysiol. 2005 Sep;94(3):1733-50
15888535
J Exp Biol. 1999 Dec;202(Pt 23):3325-32
10562515
Comp Biochem Physiol A Mol Integr Physiol. 2002 Dec;133(4):1001-11
12485689
J Exp Biol. 1999 Dec;202(Pt 23):3369-75
10562519
J Neurophysiol. 1999 Feb;81(2):758-70
10036275
Science. 1994 Jul 29;265(5172):651-3
8036513
J Exp Biol. 2005 May;208(Pt 10):1963-70
15879076
J Appl Physiol (1985). 2002 Nov;93(5):1731-43
12381761
J Neurophysiol. 1979 Sep;42(5):1212-22
490196
J Exp Biol. 2006 Jan;209(Pt 1):171-87
16354788
Exerc Sport Sci Rev. 2000 Jul;28(3):99-107
10916700
J Appl Physiol (1985). 2004 Dec;97(6):2266-74
15258124
J Exp Biol. 1998 Jun;201(Pt 11):1681-94
9576879
J Exp Biol. 2006 Apr;209(Pt 8):1502-15
16574808
J Exp Biol. 2002 Sep;205(Pt 18):2803-23
12177146
J Appl Physiol (1985). 2004 Oct;97(4):1313-22
15169748
Proc Biol Sci. 2001 Feb 7;268(1464):229-33
11217891
Integr Comp Biol. 2002 Feb;42(1):149-57
21708704
J Exp Biol. 2007 Feb;210(Pt 3):484-94
17234618
Nature. 1992 Jun 4;357(6377):360-1
1594039
J Biomech. 1996 Apr;29(4):513-23
8964781
Prog Neurobiol. 1999 Jun;58(2):185-205
10338359
J Exp Biol. 1998 Dec;201(Pt 23):3197-210
9808833
J Biomech. 1990;23 Suppl 1:65-78
2081746
J Exp Biol. 2007 Apr;210(Pt 7):1255-65
17371924
Curr Opin Neurobiol. 1995 Dec;5(6):786-91
8805415
Neuroscience. 2007 Jan 5;144(1):302-13
17055177
J Biomech. 1996 Apr;29(4):391-403
8964769
J Exp Biol. 2004 Jun;207(Pt 13):2277-88
15159432
J Biomech. 1989;22(11-12):1217-27
2625422
J Exp Biol. 2007 Feb;210(Pt 3):383-94
17234607
J Exp Biol. 1995;198(Pt 9):1829-41
9319738
Proc Biol Sci. 2003 Aug 22;270(1525):1741-6
12965003
Biol Cybern. 2000 Dec;83(6):501-15
11130583
J Exp Biol. 1982 Apr;97:57-66
7086351
Exp Brain Res. 1995;106(3):499-504
8983995
J Exp Biol. 2005 Mar;208(Pt 6):1191-200
15767317
J Biomech. 1993 Aug;26(8):945-53
8349719
J Biomech. 1999 Aug;32(8):787-94
10433420
J Biomech. 1986;19(11):899-906
3793738
Proc Natl Acad Sci U S A. 2006 Oct 17;103(42):15681-6
17032779
J Biomech. 1988;21(9):721-32
3182876
Acta Anat (Basel). 1994;151(1):1-13
7879588
Comp Biochem Physiol A Mol Integr Physiol. 2002 Dec;133(4):1087-99
12485693
Proc Biol Sci. 2006 Nov 22;273(1603):2861-7
17015312
J Physiol. 1987 Nov;392:513-22
3446790
Nature. 1990 Jul 19;346(6281):265-7
2374590