Abstract

Various methods are available for simulating the movement patterns of musculoskeletal systems and determining individual muscle forces, but the results obtained from these methods have not been rigorously validated against experiment. The aim of this study was to compare model predictions of muscle force derived for a cat hindlimb during locomotion against direct measurements of muscle force obtained in vivo. The cat hindlimb was represented as a 5-segment, 13-degrees-of-freedom (DOF), articulated linkage actuated by 25 Hill-type muscle-tendon units (MTUs). Individual muscle forces were determined by combining gait data with two widely used computational methods—static optimization and computed muscle control (CMC)—available in opensim, an open-source musculoskeletal modeling and simulation environment. The forces developed by the soleus, medial gastrocnemius (MG), and tibialis anterior muscles during free locomotion were measured using buckle transducers attached to the tendons. Muscle electromyographic activity and MTU length changes were also measured and compared against the corresponding data predicted by the model. Model-predicted muscle forces, activation levels, and MTU length changes were consistent with the corresponding quantities obtained from experiment. The calculated values of muscle force obtained from static optimization agreed more closely with experiment than those derived from CMC.

References

References
1.
Anderson
,
F. C.
, and
Pandy
,
M. G.
,
2001
, “
Dynamic Optimization of Human Walking
,”
ASME J. Biomech. Eng.
,
123
(
5
), pp.
381
390
.10.1115/1.1392310
2.
Donelan
,
J. M.
,
Kram
,
R.
, and
Arthur
,
D. K.
,
2001
, “
Mechanical and Metabolic Determinants of the Preferred Step Width in Human Walking
,”
Proc. R. Soc. London B
,
268
(
1480
), pp.
1985
1992
.10.1098/rspb.2001.1761
3.
Collins
,
S. H.
,
Wiggin
,
M. B.
, and
Sawicki
,
G. S.
,
2015
, “
Reducing the Energy Cost of Human Walking Using an Unpowered Exoskeleton
,”
Nature
,
522
(
7555
), pp.
212
215
.10.1038/nature14288
4.
Shorter
,
K. A.
,
Wu
,
A.
, and
Kuo
,
A. D.
,
2017
, “
The High Cost of Swing Leg Circumduction During Human Walking
,”
Gait Posture
,
54
, pp.
265
270
.10.1016/j.gaitpost.2017.03.021
5.
Crowninshield
,
R. D.
, and
Brand
,
R. A.
,
1981
, “
The Prediction of Forces in Joint Structures: Distribution of Intersegmental Resultants
,”
Exercise Sport Sci. Rev.
,
9
(
1
), pp.
159
181
.https://journals.lww.com/acsm-essr/Citation/1981/01000/The_Prediction_of_Forces_in_Joint_Structures_.4.aspx
6.
Herzog
,
W.
,
1996
, “
Force-Sharing Among Synergistic Muscles: Theoretical Considerations and Experimental Approaches
,”
Exercise Sport Sci. Rev.
,
24
(
1
), pp.
173
202
.https://journals.lww.com/acsm-essr/Citation/1996/00240/Force_Sharing_Among_Synergistic_Muscles_.8.aspx
7.
Pandy
,
M. G.
,
2001
, “
Computer Modeling and Simulation of Human Movement
,”
Annu. Rev. Biomed. Eng.
,
3
(
1
), pp.
245
–2
73
.10.1146/annurev.bioeng.3.1.245
8.
Erdemir
,
A.
,
McLean
,
S.
,
Herzog
,
W.
, and
van den Bogert
,
A. J.
,
2007
, “
Model-Based Estimation of Muscle Forces Exerted During Movements
,”
Clin. Biomech.
,
22
(
2
), pp.
131
154
.10.1016/j.clinbiomech.2006.09.005
9.
Pandy
,
M. G.
, and
Andriacchi
,
T. P.
,
2010
, “
Muscle and Joint Function in Human Locomotion
,”
Annu. Rev. Biomed. Eng.
,
12
(
1
), pp.
401
433
.10.1146/annurev-bioeng-070909-105259
10.
Martin
,
J. A.
,
Brandon
,
S. C.
,
Keuler
,
E. M.
,
Hermus
,
J. R.
,
Ehlers
,
A. C.
,
Segalman
,
D. J.
,
Allen
,
M. S.
, and
Thelen
,
D. G.
,
2018
, “
Gauging Force by Tapping Tendons
,”
Nat. Commun.
,
9
(
1
), pp.
1
9
.10.1038/s41467-018-03797-6
11.
Ates
,
F.
,
Temelli
,
Y.
, and
Yucesoy
,
C. A.
,
2014
, “
Intraoperative Experiments Show Relevance of Inter-Antagonistic Mechanical Interaction for Spastic Muscle's Contribution to Joint Movement Disorder
,”
Clin. Biomech.
,
29
, pp.
943
949
.10.1016/j.clinbiomech.2014.06.010
12.
Ates
,
F.
,
Temelli
,
Y.
, and
Yucesoy
,
C. A.
,
2016
, “
The Mechanics of Activated Semitendinosus Are Not Representative of the Pathological Knee Joint Condition of Children With Cerebral Palsy
,”
J. Electromyography Kinesiology
,
28
, pp.
130
136
.10.1016/j.jelekin.2016.04.002
13.
Komi
,
P. V.
,
Salonen
,
M.
,
Järvinen
,
M.
, and
Kokko
,
O.
,
1987
, “
In Vivo Registration of Achilles Tendon Forces in Man—I: Methodological Development
,”
Int. J. Sports Med.
,
8
, pp.
3
8
.10.1055/s-2008-1025697
14.
Fukashiro
,
S.
,
Komi
,
P. V.
,
Järvinen
,
M.
, and
Miyashita
,
M.
,
1993
, “
Comparison Between the Directly Measured Achilles Tendon Force and the Tendon Force Calculated From the Ankle Joint Moment During Vertical Jumps
,”
Clin. Biomech.
,
8
(
1
), pp.
25
30
.10.1016/S0268-0033(05)80006-3
15.
Sartori
,
M.
,
Reggiani
,
M.
,
Farina
,
D.
, and
Lloyd
,
D. G.
,
2012
, “
EMG-Driven Forward-Dynamic Estimation of Muscle Force and Joint Moment About Multiple Degrees of Freedom in the Human Lower Extremity
,”
PLoS One
,
7
(
12
), p.
e52618
.10.1371/journal.pone.0052618
16.
Chao
,
E. Y. S.
,
2003
, “
Graphic-Based Musculoskeletal Model for Biomechanical Analyses and Animation
,”
Med. Eng. Phys.
,
25
(
3
), pp.
201
212
.10.1016/S1350-4533(02)00181-9
17.
Fisk
,
J. P.
, and
Wayne
,
J. S.
,
2009
, “
Development and Validation of a Computational Musculoskeletal Model of the Elbow and Forearm
,”
Ann. Biomed. Eng.
,
37
(
4
), pp.
803
812
.10.1007/s10439-009-9637-x
18.
Shelburne
,
K. B.
,
Torry
,
M.
, and
Pandy
,
M. G.
,
2005
, “
Muscle, Ligament, and Joint-Contact Forces at the Knee During Walking
,”
Med. Sci. Sports Exercise
,
37
(
11
), pp.
1948
1956
.10.1249/01.mss.0000180404.86078.ff
19.
Schache
,
A. G.
,
Dorn
,
T. W.
,
Blanch
,
P. D.
,
Brown
,
N. A.
, and
Pandy
,
M. G.
,
2012
, “
Mechanics of the Human Hamstring Muscles During Sprinting
,”
Med. Sci. Sports Exercise
,
44
(
4
), pp.
647
658
.10.1249/MSS.0b013e318236a3d2
20.
Jastifer
,
J.
,
Gustafson
,
P.
,
Patel
,
B.
, and
Uggen
,
C.
,
2012
, “
Pectoralis Major Transfer for Subscapularis Deficiency: A Computational Study
,”
Shoulder Elbow
,
4
(
1
), pp.
25
29
.10.1111/j.1758-5740.2011.00161.x
21.
Homayouni
,
T.
,
Underwood
,
K. N.
,
Beyer
,
K. C.
,
Martin
,
E. R.
,
Allan
,
C. H.
, and
Balasubramanian
,
R.
,
2015
, “
Modeling Implantable Passive Mechanisms for Modifying the Transmission of Forces and Movements Between Muscle and Tendons
,”
IEEE Trans. Biomed. Eng.
,
62
(
9
), pp.
2208
2214
.10.1109/TBME.2015.2419223
22.
Correa
,
T. A.
,
Schache
,
A. G.
,
Graham
,
H. K.
,
Baker
,
R.
,
Thomason
,
P.
, and
Pandy
,
M. G.
,
2012
, “
Potential of Lower-Limb Muscles to Accelerate the Body During Cerebral Palsy Gait
,”
Gait Posture
,
36
(
2
), pp.
194
200
.10.1016/j.gaitpost.2012.02.014
23.
Steele
,
K. M.
,
DeMers
,
M. S.
,
Schwartz
,
M. H.
, and
Delp
,
S. L.
,
2012
, “
Compressive Tibiofemoral Force During Crouch Gait
,”
Gait Posture
,
35
(
4
), pp.
556
560
.10.1016/j.gaitpost.2011.11.023
24.
Rankin
,
J. W.
,
Rubenson
,
J.
, and
Hutchinson
,
J. R.
,
2016
, “
Inferring Muscle Functional Roles of the Ostrich Pelvic Limb During Walking and Running Using Computer Optimization
,”
J. R. Soc. Interface
,
13
(
118
), p.
20160035
.10.1098/rsif.2016.0035
25.
Anderson
,
F. C.
, and
Pandy
,
M. G.
,
2003
, “
Individual Muscle Contributions to Support in Normal Walking
,”
Gait Posture
,
17
(
2
), pp.
159
169
.10.1016/S0966-6362(02)00073-5
26.
Liu
,
M.
,
Anderson
,
F. C.
,
Pandy
,
M. G.
, and
Delp
,
S. L.
,
2006
, “
Muscles That Support the Body Also Modulate Forward Progression During Walking
,”
J. Biomech.
,
39
(
14
), pp.
2623
2630
.10.1016/j.jbiomech.2005.08.017
27.
Pandy
,
M. G.
,
Lin
,
Y. C.
, and
Kim
,
H. J.
,
2010
, “
Muscle Coordination of Mediolateral Balance in Normal Walking
,”
J. Biomech.
,
43
(
11
), pp.
2055
2064
.10.1016/j.jbiomech.2010.04.010
28.
Harrison
,
S. M.
,
Whitton
,
R. C.
,
King
,
M.
,
Haussler
,
K. K.
,
Kawcak
,
C. E.
,
Stover
,
S. M.
, and
Pandy
,
M. G.
,
2012
, “
Forelimb Muscle Activity During Equine Locomotion
,”
J. Exp. Biol.
,
215
(
17
), pp.
2980
2991
.10.1242/jeb.065441
29.
McConnell
,
J.
,
Donnelly
,
C.
,
Hamner
,
S.
,
Dunne
,
J.
, and
Besier
,
T.
,
2012
, “
Passive and Dynamic Shoulder Rotation Range in Uninjured and Previously Injured Overhead Throwing Athletes and the Effect of Shoulder Taping
,”
Am. J. Phys. Med. Rehabil.
,
4
, pp.
111
116
.10.1016/j.pmrj.2011.11.010
30.
Gerus
,
P.
,
Sartori
,
M.
,
Besier
,
T. F.
,
Fregly
,
B. J.
,
Delp
,
S. L.
,
Banks
,
S. A.
,
Pandy
,
M. G.
,
D'Lima
,
D. D.
, and
Lloyd
,
D. G.
,
2013
, “
Subject-Specific Knee Joint Geometry Improves Predictions of Medial Tibiofemoral Contact Forces
,”
J. Biomech.
,
46
(
16
), pp.
2778
2786
.10.1016/j.jbiomech.2013.09.005
31.
Lin
,
Y. C.
,
Dorn
,
T. W.
,
Schache
,
A. G.
, and
Pandy
,
M. G.
,
2012
, “
Comparison of Different Methods for Estimating Muscle Forces in Human Movement
,”
Proc. Inst. Mech. Eng., Part H.
,
226
(
2
), pp.
103
112
.10.1177/0954411911429401
32.
Bruno
,
A. G.
,
Bouxsein
,
M. L.
, and
Anderson
,
D. E.
,
2015
, “
Development and Validation of a Musculoskeletal Model of the Fully Articulated Thoracolumbar Spine and Rib Cage
,”
ASME J. Biomech. Eng.
,
137
(
8
), p.
081003
.10.1115/1.4030408
33.
Simonsen
,
E. B.
, and
Komi
,
P. V.
,
2003
, “
Biomechanics of Locomotion
,”
Textbook of Sports Medicine Basic Science and Clinical Aspects of Sports Injury and Physical Activity
,
M.
Kjær
,
M.
Krogsgaard
,
P.
Magnusson
,
L.
Engebretsen
,
H.
Ross
,
T.
Takala
, and
S. L. Y.
Woo
, eds.,
Blackwell Science
,
Hong Kong
, China, pp.
107
133
.
34.
Delp
,
S. L.
,
Anderson
,
F. C.
,
Arnold
,
A. S.
,
Loan
,
P.
,
Habib
,
A.
,
John
,
C. T.
,
Guendelman
,
E.
, and
Thelen
,
D. G.
,
2007
, “
OpenSim: Open-Source Software to Create and Analyze Dynamic Simulations of Movement
,”
IEEE Trans. Biomed. Eng.
,
54
(
11
), pp.
1940
1950
.10.1109/TBME.2007.901024
35.
Schappacher-Tilp
,
G.
,
Binding
,
P.
,
Braverman
,
E.
, and
Herzog
,
W.
,
2009
, “
Velocity-Dependent Cost Function for the Prediction of Force Sharing Among Synergistic Muscles in a One Degree of Freedom Model
,”
J. Biomech.
,
42
(
5
), pp.
657
660
.10.1016/j.jbiomech.2008.12.013
36.
Herzog
,
W.
, and
Leonard
,
T. R.
,
1991
, “
Validation of Optimization Models That Estimate the Forces Exerted by Synergistic Muscles
,”
J. Biomech.
,
24
(
Suppl. 1
), pp.
31
39
.10.1016/0021-9290(91)90375-W
37.
Koppes
,
R. A.
,
Herzog
,
W.
, and
Corr
,
D. T.
,
2013
, “
Force Enhancement in Lengthening Contractions of Cat Soleus Muscle In Situ: Transient and Steady-State Aspects
,”
Physiol. Rep.
,
1
(
2
), pp.
1
10
.10.1002/phy2.17
38.
Thelen
,
D. G.
, and
Anderson
,
F. C.
,
2006
, “
Using Computed Muscle Control to Generate Forward Dynamic Simulations of Human Walking From Experimental Data
,”
J. Biomech.
,
39
(
6
), pp.
1107
1115
.10.1016/j.jbiomech.2005.02.010
39.
Kaya
,
M.
,
Leonard
,
T.
, and
Herzog
,
W.
,
2003
, “
Coordination of Medial Gastrocnemius and Soleus Forces During Cat Locomotion
,”
J. Exp. Biol.
,
206
(
20
), pp.
3645
3655
.10.1242/jeb.00544
40.
Herzog
,
W.
,
Leonard
,
T. R.
, and
Guimaraes
,
A. C. S.
,
1993
, “
Forces in Gastrocnemius, Soleus, and Plantaris Tendons of the Freely Moving Cat
,”
J. Biomech.
,
26
(
8
), pp.
945
953
.10.1016/0021-9290(93)90056-K
41.
Kaya
,
M.
,
2003
, “
Coordination of Cat Hindlimb Muscles During Voluntary Movements
,” Ph.D. thesis, University of Calgary, Calgary, AB, Canada.
42.
Kaya
,
M.
,
Jinha
,
A.
,
Leonard
,
T. R.
, and
Herzog
,
W.
,
2005
, “
Multi-Functionality of the Cat Medial Gastrocnemius During Locomotion
,”
J. Biomech.
,
38
(
6
), pp.
1291
1301
.10.1016/j.jbiomech.2004.06.009
43.
Walmsley
,
B.
,
Hodgson
,
J. A.
, and
Burke
,
R. E.
,
1978
, “
Forces Produced by Medial Gastrocnemius and Soleus Muscles During Locomotion in Freely Moving Cats
,”
J. Neurophysiol.
,
41
(
5
), pp.
1203
1216
.10.1152/jn.1978.41.5.1203
44.
Merletti
,
R.
,
1999
, “
Standards for Reporting EMG Data
,”
J. Electromyography Kinesiology
,
9
, pp.
3
4
.https://isek.org/wp-content/uploads/2015/05/Standards-for-Reporting-EMG-Data.pdf
45.
An
,
K. N.
,
Takahashi
,
K.
,
Harrigan
,
T. P.
, and
Chao
,
E. Y.
,
1984
, “
Determination of Muscle Orientations and Moment Arms
,”
ASME J. Biomech. Eng.
,
106
(
3
), pp.
280
282
.10.1115/1.3138494
46.
Boyd
,
S. K.
,
Muller
,
R.
,
Leonard
,
T.
, and
Herzog
,
W.
,
2005
, “
Long-Term Periarticular Bone Adaptation in a Feline Knee Injury Model for Post-Traumatic Experimental Osteoarthritis
,”
Osteoarthritis Cartilage
,
13
(
3
), pp.
235
242
.10.1016/j.joca.2004.11.004
47.
Burkholder
,
T. J.
, and
Nichols
,
T. R.
,
2004
, “
Three-Dimensional Model of the Feline Hindlimb
,”
J. Morphol.
,
261
(
1
), pp.
118
129
.10.1002/jmor.10233
48.
O'Neill
,
M. C.
,
Lee
,
L. F.
,
Larson
,
S. G.
,
Demes
,
B.
,
Stern
,
J. T.
, Jr.
, and
Umberger
,
B. R.
,
2013
, “
A Three-Dimensional Musculoskeletal Model of the Chimpanzee (Pan Troglodytes) Pelvis and Hind Limb
,”
J. Exp. Biol.
,
216
, pp.
3709
3723
.10.1242/jeb.079665
49.
Thelen
,
D. G.
,
2003
, “
Adjustment of Muscle Mechanics Model Parameters to Simulate Dynamic Contractions in Older Adults
,”
ASME J. Biomech. Eng.
,
125
(
1
), pp.
70
77
.10.1115/1.1531112
50.
Young
,
R. P.
,
Scott
,
S. H.
, and
Loeb
,
G. E.
,
1993
, “
The Distal Hindlimb Musculature of the Cat: Multiaxis Moment Arms at the Ankle Joint
,”
Exp. Brain Res.
,
96
(
1
), pp.
141
151
.10.1007/BF00230447
51.
MacFadden
,
L. N.
, and
Brown
,
N. A. T.
,
2007
, “
Biarticular Hip Extensor and Knee Flexor Muscle Moment Arms of the Feline Hindlimb
,”
J. Biomech.
,
40
(
15
), pp.
3448
3457
.10.1016/j.jbiomech.2007.05.021
52.
MacFadden
,
L. N.
, and
Brown
,
N. A. T.
,
2010
, “
The Influence of Modeling Separate Neuromuscular Compartments on the Force and Moment Generating Capacities of Muscles of the Feline Hindlimb
,”
ASME J. Biomech. Eng.
,
132
(
8
), p.
081003
.10.1115/1.4001680
53.
Sacks
,
R. D.
, and
Roy
,
R. R.
,
1982
, “
Architecture of the Hind Limb Muscles of Cats: Functional Significance
,”
J. Morphol.
,
173
(
2
), pp.
185
195
.10.1002/jmor.1051730206
54.
Zajac
,
F. E.
,
1989
, “
Muscle and Tendon: Properties, Models, Scaling, and Application to Biomechanics and Motor Control
,”
Crit. Rev. Biomed. Eng.
,
17
(
4
), pp.
359
411
. https://europepmc.org/article/med/2676342
55.
Anderson
,
F. C.
, and
Pandy
,
M. G.
,
2001
, “
Static and Dynamic Optimization Solutions for Gait Are Practically Equivalent
,”
J. Biomech.
,
34
(
2
), pp.
153
161
.10.1016/S0021-9290(00)00155-X
56.
Luh
,
J. J.
,
Chang
,
G. C.
,
Cheng
,
C. K.
,
Lai
,
J. S.
, and
Kuo
,
T. S.
,
1999
, “
Isokinetic Elbow Joint Torques Estimation From Surface EMG and Joint Kinematic Data: Using an Artificial Neural Network Model
,”
J. Electromyography Kinesiology
,
9
(
3
), pp.
173
183
.10.1016/S1050-6411(98)00030-3
57.
Ackland
,
D. C.
,
Lin
,
Y. C.
, and
Pandy
,
M. G.
,
2012
, “
Sensitivity of Model Predictions of Muscle Function to Changes in Moment Arms and Muscle-Tendon Parameters: A Monte Carlo Analysis
,”
J. Biomech.
,
45
(
8
), pp.
1463
1471
.10.1016/j.jbiomech.2012.02.023
58.
Valero-Cuevas
,
F. J.
,
Johanson
,
M. E.
, and
Towles
,
J. D.
,
2003
, “
Towards a Realistic Biomechanical Model of the Thumb: The Choice of Kinematic Description Maybe More Critical Than the Solution Method or the Variability/Uncertainty of Musculoskeletal Parameters
,”
J. Biomech.
,
36
(
7
), pp.
1019
1030
.10.1016/S0021-9290(03)00061-7
59.
Hicks
,
J. L.
,
Uchida
,
T. K.
,
Seth
,
A.
,
Rajagopal
,
A.
, and
Delp
,
S. L.
,
2015
, “
Is My Model Good Enough? Best Practices for Verification and Validation of Musculoskeletal Models and Simulations of Movement
,”
ASME J. Biomech. Eng.
,
137
(
2
), pp.
1
24
. 10.1115/1.4029304
60.
Bernstein
,
N. A.
,
1967
,
The Co-Ordination and Regulation of Movements
,
Pergamon Press
,
Oxford, New York
.
61.
Crowninshield
,
R. D.
, and
Brand
,
R. A.
,
1981
, “
A Physiologically Based Criterion of Muscle Force Prediction in Locomotion
,”
J. Biomech.
,
14
(
11
), pp.
793
801
.10.1016/0021-9290(81)90035-X
62.
Wesseling
,
M.
,
Derikx
,
L. C.
,
de Groote
,
F.
,
Bartels
,
W.
,
Meyer
,
C.
,
Verdonschot
,
N.
, and
Jonkers
,
I.
,
2015
, “
Muscle Optimization Techniques Impact the Magnitude of Calculated Hip Joint Contact Forces
,”
J. Orthop. Res.
,
33
(
3
), pp.
430
438
.10.1002/jor.22769
63.
Lai
,
A. K.
,
Arnold
,
A. S.
, and
Wakeling
,
J. M.
,
2017
, “
Why Are Antagonist Muscles Co-Activated in My Simulation? A Musculoskeletal Model for Analysing Human Locomotor Tasks
,”
Ann. Biomed. Eng.
,
45
(
12
), pp.
2762
2774
.10.1007/s10439-017-1920-7
64.
Redl
,
C.
,
Gfoehler
,
M.
, and
Pandy
,
M. G.
,
2007
, “
Sensitivity of Muscle Force Estimates to Variations in Muscle-Tendon Properties
,”
Hum. Mov. Sci.
,
26
(
2
), pp.
306
319
.10.1016/j.humov.2007.01.008
You do not currently have access to this content.