Abstract
Hill-type models are frequently used in biomechanical simulations. They are attractive for their low computational cost and close relation to commonly measured musculotendon parameters. Still, more attention is needed to improve the activation dynamics of the model specifically because of the nonlinearity observed in the electromyography (EMG)–force relation. Moreover, one of the important and practical questions regarding the assessment of the model's performance is how adequately can the model simulate any fundamental type of human movement without modifying model parameters for different tasks? This paper tries to answer this question by proposing a simple physiologically based activation dynamics model. The model describes the kinetics of the calcium dynamics while activating and deactivating the muscle contraction process. Hence, it allowed simulating the recently discovered role of store-operated calcium entry (SOCE) channels as immediate counterflux to calcium loss across the tubular system during excitation–contraction coupling. By comparing the ability to fit experimental data without readjusting the parameters, the proposed model has proven to have more steady performance than phenomenologically based models through different submaximal isometric contraction levels. This model indicates that more physiological insights are key for improving Hill-type model performance.
Issue Section:
Research Papers
References
1.
Ma
,
Y.
,
Xie
,
S.
, and
Zhang
,
Y.
, 2016
, “
A Patient-Specific EMG-Driven Neuromuscular Model for the Potential Use of Human-Inspired Gait Rehabilitation Robots
,” Comput. Biol. Med.
,
70
, pp. 88
–98
.10.1016/j.compbiomed.2016.01.0012.
Langholz
,
J. B.
,
Westman
,
G.
, and
Karlsteen
,
M.
, 2016
, “
Musculoskeletal Modelling in Sports-Evaluation of Different Software Tools With Focus on Swimming
,” Procedia Eng.
,
147
, pp. 281
–287
.10.1016/j.proeng.2016.06.2783.
Asmussen
,
M.
,
Cigoja
,
S.
,
Firminger
,
C.
,
Fletcher
,
J.
,
Edwards
,
B.
, and
Nigg
,
B.
, 2019
, “
Using Musculoskeletal Modelling to Understand the Energetic Cost of Running With Different Footwear
,” J. Sci. Med. Sport
,
22
, p. S73
.10.1016/j.jsams.2019.08.2874.
Shao
,
Q.
,
Bassett
,
D. N.
,
Manal
,
K.
, and
Buchanan
,
T. S.
, 2009
, “
An EMG-Driven Model to Estimate Muscle Forces and Joint Moments in Stroke Patients
,” Comput. Biol. Med.
,
39
(12
), pp. 1083
–1088
.10.1016/j.compbiomed.2009.09.0025.
Chu
,
W. T. V.
, and
Sanger
,
T. D.
, 2009
, “
Force Variability During Isometric Biceps Contraction in Children With Secondary Dystonia Due to Cerebral Palsy
,” Mov. Disord.
,
24
(9
), pp. 1299
–1305
.10.1002/mds.225736.
Ma
,
Y.
,
Xie
,
S.
, and
Sun
,
C.
, 2016
, “
Evaluation of the Patient-Specific Electromyography (EMG)-Driven Neuromuscular Model for Cerebral Palsy Patients
,” IEEE/ASME International Conference on Advanced Intelligent Mechatronics (AIM)
, Banff, AB, Canada, July 12–15, pp. 270
–275
.10.1109/AIM.2016.75767787.
Wiedemann
,
L. G.
,
Jayaneththi
,
V. R.
,
Kimpton
,
J.
,
Chan
,
A.
,
Müller
,
M. A.
,
Hogan
,
A.
,
Lim
,
E.
,
Wilson
,
N. C.
, and
McDaid
,
A. J.
, 2018
, “
Neuromuscular Characterisation in Cerebral Palsy Using Hybrid Hill-Type Models on Isometric Contractions
,” Comput. Biol. Med.
,
103
, pp. 269
–276
.10.1016/j.compbiomed.2018.10.0278.
Pi
,
M.
,
Yuan
,
Y.
, and
Li
,
Z.
, 2019
, “
Control of the Robotic Leg Prostheses Based on a Neuromuscular Model
,” 2019 Fourth IEEE International Conference on Advanced Robotics and Mechatronics (ICARM)
, Toyonaka, Japan, July 3–5, pp. 141
–145
.10.1109/ICARM.2019.88340439.
Mghames
,
S.
,
Santina
,
C. D.
,
Garabini
,
M.
, and
Bicchi
,
A.
, 2019
, “
A Neuromuscular-Model Based Control Strategy to Minimize Muscle Effort in Assistive Exoskeletons
,” IEEE International Conference on Rehabilitation Robotics
, Toronto, ON, Canada, June 24–28, pp. 963
–970
.10.1109/ICORR.2019.877945610.
Ding
,
Z.
,
Azmi
,
N. L.
, and
Bull
,
A. M. J.
, 2019
, “
Validation and Use of a Musculoskeletal Gait Model to Study the Role of Functional Electrical Stimulation
,” IEEE Trans. Biomed. Eng.
,
66
(3
), pp. 892
–897
.10.1109/TBME.2018.286561411.
Del Santo
,
F.
,
Gelli
,
F.
,
Ginanneschi
,
F.
,
Popa
,
T.
, and
Rossi
,
A.
, 2007
, “
Relation Between Isometric Muscle Force and Surface EMG in Intrinsic Hand Muscles as Function of the Arm Geometry
,” Brain Res.
,
1163
(1
), pp. 79
–85
.10.1016/j.brainres.2007.06.01212.
Stegeman
,
D. F.
,
Blok
,
J. H.
,
Hermens
,
H. J.
, and
Roeleveld
,
K.
, 2000
, “
Surface EMG Models: Properties and Applications
,” J. Electromyogr. Kinesiol.
,
10
(5
), pp. 313
–326
.10.1016/S1050-6411(00)00023-713.
Gabriel
,
D. A.
,
Kamen
,
G.
, and
Frost
,
G.
, 2006
, “
Neural Adaptations to Resistive Exercise: Mechanisms and Recommendations for Training Practices
,” Sports Med.
,
36
(2
), pp. 133
–149
.10.2165/00007256-200636020-0000414.
Vigotsky
,
A. D.
,
Halperin
,
I.
,
Lehman
,
G. J.
,
Trajano
,
G. S.
, and
Vieira
,
T. M.
, 2018
, “
Interpreting Signal Amplitudes in Surface Electromyography Studies in Sport and Rehabilitation Sciences
,” Front. Physiol.
,
8
, p. 985
.10.3389/fphys.2017.0098515.
Lu
,
T. W.
, and
Chang
,
C. F.
, 2012
, “
Biomechanics of Human Movement and Its Clinical Applications
,” Kaohsiung J. Med. Sci.
,
28
(2
), pp. S13
–S25
.10.1016/j.kjms.2011.08.00416.
Buchanan
,
T. S.
,
Lloyd
,
D. G.
,
Manal
,
K.
, and
Gonzalez
,
R. V.
, 2002
, “
A Real-Time EMG-Driven Virtual Arm
,” Comput. Biol. Med.
,
32
(1
), pp. 25
–36
.10.1016/S0010-4825(01)00024-517.
Buchanan
,
T. S.
,
Lloyd
,
D. G.
,
Manal
,
K.
, and
Besier
,
T. F.
, 2004
, “
Neuromusculoskeletal Modeling: Estimation of Muscle Forces and Joint Moments and Movements From Measurements of Neural Command
,” J. Appl. Biomech.
,
20
(4
), pp. 367
–395
.10.1123/jab.20.4.36718.
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://pubmed.ncbi.nlm.nih.gov/2676342/19.
Desplenter
,
T.
, and
Trejos
,
A. L.
, 2018
, “
Evaluating Muscle Activation Models for Elbow Motion Estimation
,” Sensors (Switzerland)
,
18
(4
), p. 1004
.10.3390/s1804100420.
Fukuda
,
T. Y.
,
Echeimberg
,
J. O.
,
Pompeu
,
J. E.
,
Lucareli
,
P. R. G.
,
Garbelotti
,
S.
,
Gimenes
,
R. O.
, and
Apolinário
,
A.
, 2010
, “
Root Mean Square Value of the Electromyographic Signal in the Isometric Torque of the Quadriceps, Hamstrings and Brachial Biceps Muscles in Female Subjects
,” J. Appl. Res.
,
10
(1
), pp. 32
–39
.https://www.researchgate.net/publication/221963814_Root_Mean_Square_Value_of_the_Electromyographic_Signal_in_the_Isometric_Torque_of_the_Quadriceps_Hamstrings_and_Brachial_Biceps_Muscles_in_Female21.
Sbriccoli
,
P.
,
Bazzucchi
,
I.
,
Rosponi
,
A.
,
Bernardi
,
M.
,
De Vito
,
G.
, and
Felici
,
F.
, 2003
, “
Amplitude and Spectral Characteristics of Biceps Brachii SEMG Depend Upon Speed of Isometric Force Generation
,” J. Electromyogr. Kinesiol.
,
13
(2
), pp. 139
–147
.10.1016/S1050-6411(02)00098-622.
Bilodeau
,
M.
,
Schindler-Ivens
,
S.
,
Williams
,
D. M.
,
Chandran
,
R.
, and
Sharma
,
S. S.
, 2003
, “
EMG Frequency Content Changes With Increasing Force and During Fatigue in the Quadriceps Femoris Muscle of Men and Women
,” J. Electromyogr. Kinesiol.
,
13
(1
), pp. 83
–92
.10.1016/S1050-6411(02)00050-023.
McGill
,
K. C.
, 2004
, “
Surface Electromyogram Signal Modelling
,” Med. Biol. Eng. Comput.
,
42
(4
), pp. 446
–454
.10.1007/BF0235098524.
Woods
,
J. J.
, and
Bigland-Ritchie
,
B.
, 1983
, “
Linear and Non-Linear Surface EMG/Force Relationships in Human Muscles. An Anatomical/Functional Argument for the Existence of Both
,” Am. J. Phys. Med.
,
62
(6
), pp. 287
–299
.https://pubmed.ncbi.nlm.nih.gov/6650674/25.
Jahanmiri-Nezhad
,
F.
,
Hu
,
X.
,
Suresh
,
N. L.
,
Rymer
,
W. Z.
, and
Zhou
,
P.
, 2014
, “
EMG-Force Relation in the First Dorsal Interosseous Muscle of Patients With Amyotrophic Lateral Sclerosis
,” NeuroRehabilitation
,
35
(2
), pp. 307
–314
.10.3233/NRE-14112526.
Watanabe
,
K.
, and
Akima
,
H.
, 2009
, “
Normalized EMG to Normalized Torque Relationship of Vastus Intermedius Muscle During Isometric Knee Extension
,” Eur. J. Appl. Physiol.
,
106
(5
), pp. 665
–673
.10.1007/s00421-009-1064-z27.
Perreault
,
E. J.
,
Heckman
,
C. J.
, and
Sandercock
,
T. G.
, 2003
, “
Hill Muscle Model Errors During Movement Are Greatest Within the Physiologically Relevant Range of Motor Unit Firing Rates
,” J. Biomech.
,
36
(2
), pp. 211
–218
.10.1016/S0021-9290(02)00332-928.
Cooke
,
R.
, 2004
, “
Milestone in Physiology. The Sliding Filament Model: 1972-2004
,” J. Gen. Physiol.
,
123
(6
), pp. 643
–656
.10.1085/jgp.20040908929.
Calderón
,
J. C.
,
Bolaños
,
P.
, and
Caputo
,
C.
, 2014
, “
The Excitation-Contraction Coupling Mechanism in Skeletal Muscle
,” Biophys. Rev.
,
6
(1
), pp. 133
–160
.10.1007/s12551-013-0135-x30.
Berchtold
,
M. W.
,
Brinkmeier
,
H.
, and
Müntener
,
M.
, 2000
, “
Calcium Ion in Skeletal Muscle: Its Crucial Role for Muscle Function, Plasticity, and Disease
,” Physiol. Rev.
,
80
(3
), pp. 1215
–1265
.10.1152/physrev.2000.80.3.121531.
Greig
,
C. A.
, and
Jones
,
D. A.
, 2016
, “
Muscle Physiology and Contraction
,” Surgery (U. K.)
,
34
(3
), pp. 107
–114
.10.1016/j.mpsur.2016.01.00432.
McMillen
,
T.
,
Williams
,
T.
, and
Holmes
,
P.
, 2008
, “
Nonlinear Muscles, Passive Viscoelasticity and Body Taper Conspire to Create Neuromechanical Phase Lags in Anguilliform Swimmers
,” PLoS Comput. Biol.
,
4
(8
), p. e1000157
.10.1371/journal.pcbi.100015733.
Williams
,
T. L.
, 2010
, “
A New Model for Force Generation by Skeletal Muscle, Incorporating Work-Dependent Deactivation
,” J. Exp. Biol.
,
213
(4
), pp. 643
–650
.10.1242/jeb.03759834.
Koenig
,
X.
,
Choi
,
R. H.
,
Schicker
,
K.
,
Singh
,
D. P.
,
Hilber
,
K.
, and
Launikonis
,
B. S.
, 2019
, “
Mechanistic Insights Into Store-Operated Ca2+ Entry During Excitation-Contraction Coupling in Skeletal Muscle
,” Biochim. Biophys. Acta - Mol. Cell Res.
,
1866
(7
), pp. 1239
–1248
.10.1016/j.bbamcr.2019.02.01435.
Michelucci
,
A.
,
García-Castañeda
,
M.
,
Boncompagni
,
S.
, and
Dirksen
,
R. T.
, 2018
, “
Role of STIM1/ORAI1-Mediated Store-Operated Ca2+ Entry in Skeletal Muscle Physiology and Disease
,” Cell Calcium
,
76
, pp. 101
–115
.10.1016/j.ceca.2018.10.00436.
Koenig
,
X.
,
Choi
,
R. H.
, and
Launikonis
,
B. S.
, 2018
, “
Store-Operated Ca2+ Entry Is Activated by Every Action Potential in Skeletal Muscle
,” Commun. Biol.
,
1
(1
), p. 31
.10.1038/s42003-018-0033-737.
Sztretye
,
M.
,
Geyer
,
N.
,
Vincze
,
J.
,
Al-Gaadi
,
D.
,
Oláh
,
T.
,
Szentesi
,
P.
,
Kis
,
G.
,
Antal
,
M.
,
Balatoni
,
I.
,
Csernoch
,
L.
, and
Dienes
,
B.
, 2017
, “
SOCE Is Important for Maintaining Sarcoplasmic Calcium Content and Release in Skeletal Muscle Fibers
,” Biophys. J.
,
113
(11
), pp. 2496
–2507
.10.1016/j.bpj.2017.09.02338.
Edwards
,
J. N.
,
Murphy
,
R. M.
,
Cully
,
T. R.
,
von Wegner
,
F.
,
Friedrich
,
O.
, and
Launikonis
,
B. S.
, 2010
, “
Ultra-Rapid Activation and Deactivation of Store-Operated Ca2+ Entry in Skeletal Muscle
,” Cell Calcium
,
47
(5
), pp. 458
–467
.10.1016/j.ceca.2010.04.00139.
Launikonis
,
B. S.
, and
Ríos
,
E.
, 2007
, “
Store-Operated Ca2+ Entry During Intracellular Ca2+ Release in Mammalian Skeletal Muscle
,” J. Physiol.
,
583
(1
), pp. 81
–97
.10.1113/jphysiol.2007.13504640.
Pan
,
Z.
,
Yang
,
D.
,
Nagaraj
,
R. Y.
,
Nosek
,
T. A.
,
Nishi
,
M.
,
Takeshima
,
H.
,
Cheng
,
H.
, and
Ma
,
J.
, 2002
, “
Dysfunction of Store-Operated Calcium Channel in Muscle Cells Lacking Mg29
,” Nat. Cell Biol.
,
4
(5
), pp. 379
–383
.10.1038/ncb78841.
Edman
,
K. A. P.
, 1996
, “
Fatigue vs. Shortening-Induced Deactivation in Striated Muscle
,” Acta Physiol. Scand.
,
156
(3
), pp. 183
–192
.10.1046/j.1365-201X.1996.t01-1-198000.x42.
Piazza
,
S. J.
, and
Delp
,
S. L.
, 1996
, “
The Influence of Muscles on Knee Flexion During the Swing Phase of Gait
,” J. Biomech.
,
29
(6
), pp. 723
–733
.10.1016/0021-9290(95)00144-143.
Manal
,
K.
, and
Buchanan
,
T. S.
, 2003
, “
A One-Parameter Neural Activation to Muscle Activation Model: Estimating Isometric Joint Moments From Electromyograms
,” J. Biomech.
,
36
(8
), pp. 1197
–1202
.10.1016/S0021-9290(03)00152-044.
Menegaldo
,
L. L.
,
de Oliveira
,
L. F.
, and
Minato
,
K. K.
, 2014
, “
EMGD-FE: An Open Source Graphical User Interface for Estimating Isometric Muscle Forces in the Lower Limb Using an EMG-Driven Model
,” Biomed. Eng. Online
,
13
(1
), p. 37
.10.1186/1475-925X-13-3745.
Heine
,
C. B.
, and
Menegaldo
,
L. L.
, 2018
, “
Numerical Validation of a Subject-Specific Parameter Identification Approach of a Quadriceps Femoris EMG-Driven Model
,” Med. Eng. Phys.
,
53
, pp. 66
–74
.10.1016/j.medengphy.2018.01.00646.
Menegaldo
,
L. L.
, and
Oliveira
,
L. F.
, 2011
, “
An EMG-Driven Model to Evaluate Quadriceps Strengthening After an Isokinetic Training
,” Procedia IUTAM
,
2
, pp. 131
–141
.10.1016/j.piutam.2011.04.01447.
de Oliveira
,
V. B.
,
de Oliveira
,
L. F.
, and
Menegaldo
,
L. L.
, 2018
, “
Estimation of Vastus Intermedius Electromyography: Comparison of Three Methods and Their Impact on the Knee Isometric Extension Moment Predicted by an EMG-Driven Model
,” Isokinet. Exercise Sci.
,
26
(4
), pp. 299
–306
.10.3233/IES-18216748.
Menegaldo
,
L. L.
, and
Oliveira
,
L. F. D.
, 2009
, “
Effect of Muscle Model Parameter Scaling for Isometric Plantar Flexion Torque Prediction
,” J. Biomech.
,
42
(15
), pp. 2597
–2601
.10.1016/j.jbiomech.2009.06.04349.
Winters
,
J. M.
, and
Stark
,
L.
, 1987
, “
Muscle Models: What Is Gained and What Is Lost by Varying Model Complexity
,” Biol. Cybern.
,
55
(6
), pp. 403
–420
.10.1007/BF0031837550.
Knoek van Soest
,
A. J.
,
Casius
,
L. J. R.
, and
Lemaire
,
K. K.
, 2019
, “
Huxley-Type Cross-Bridge Models in Largeish-Scale Musculoskeletal Models; an Evaluation of Computational Cost
,” J. Biomech.
,
83
, pp. 43
–48
.10.1016/j.jbiomech.2018.11.02151.
MacEri
,
F.
,
Marino
,
M.
, and
Vairo
,
G.
, 2012
, “
An Insight on Multiscale Tendon Modeling in Muscle-Tendon Integrated Behavior
,” Biomech. Model. Mechanobiol.
,
11
(3–4
), pp. 505
–517
.10.1007/s10237-011-0329-852.
Karathanasopoulos
,
N.
, and
Ganghoffer
,
J. F.
, 2019
, “
Exploiting Viscoelastic Experimental Observations and Numerical Simulations to Infer Biomimetic Artificial Tendon Fiber Designs
,” Front. Bioeng. Biotechnol.
,
7
, p. 85
.10.3389/fbioe.2019.0008553.
Karathanasopoulos
,
N.
, and
Ganghoffer
,
J. F.
, 2019
, “
Investigating the Effect of Aging on the Viscosity of Tendon Fascicles and Fibers
,” Front. Bioeng. Biotechnol.
,
7
, p. 107
.10.3389/fbioe.2019.0010754.
Williams
,
T. L.
,
Bowtell
,
G.
, and
Curtin
,
N. A.
, 1998
, “
Predicting Force Generation by Lamprey Muscle During Applied Sinusoidal Movement Using a Simple Dynamic Model
,” J. Exp. Biol.
,
201
(6
), pp. 869
–875
.10.1242/jeb.201.6.869Copyright © 2022 by ASME
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