Musculoskeletal models of a human and bonobo finger: parameter identification and comparison to in vitro experiments

Introduction Knowledge of internal finger loading during human and non-human primate activities such as tool use or knuckle-walking has become increasingly important to reconstruct the behaviour of fossil hominins based on bone morphology. Musculoskeletal models have proven useful for predicting these internal loads during human activities, but load predictions for non-human primate activities are missing due to a lack of suitable finger models. The main goal of this study was to implement both a human and a representative non-human primate finger model to facilitate comparative studies on metacarpal bone loading. To ensure that the model predictions are sufficiently accurate, the specific goals were: (1) to identify species-specific model parameters based on in vitro measured fingertip forces resulting from single tendon loading and (2) to evaluate the model accuracy of predicted fingertip forces and net metacarpal bone loading in a different loading scenario. Materials & Methods Three human and one bonobo (Pan paniscus) fingers were tested in vitro using a previously developed experimental setup. The cadaveric fingers were positioned in four static postures and load was applied by attaching weights to the tendons of the finger muscles. For parameter identification, fingertip forces were measured by loading each tendon individually in each posture. For the evaluation of model accuracy, the extrinsic flexor muscles were loaded simultaneously and both the fingertip force and net metacarpal bone force were measured. The finger models were implemented using custom Python scripts. Initial parameters were taken from literature for the human model and own dissection data for the bonobo model. Optimized model parameters were identified by minimizing the error between predicted and experimentally measured fingertip forces. Fingertip forces and net metacarpal bone loading in the combined loading scenario were predicted using the optimized models and the remaining error with respect to the experimental data was evaluated. Results The parameter identification procedure led to minor model adjustments but considerably reduced the error in the predicted fingertip forces (root mean square error reduced from 0.53/0.69 N to 0.11/0.20 N for the human/bonobo model). Both models remained physiologically plausible after the parameter identification. In the combined loading scenario, fingertip and net metacarpal forces were predicted with average directional errors below 6° and magnitude errors below 12%. Conclusions This study presents the first attempt to implement both a human and non-human primate finger model for comparative palaeoanthropological studies. The good agreement between predicted and experimental forces involving the action of extrinsic flexors—which are most relevant for forceful grasping—shows that the models are likely sufficiently accurate for comparisons of internal loads occurring during human and non-human primate manual activities.

[1]  Michael A Sherman,et al.  WHAT IS A MOMENT ARM? CALCULATING MUSCLE EFFECTIVENESS IN BIOMECHANICAL MODELS USING GENERALIZED COORDINATES. , 2013, Proceedings of the ... ASME Design Engineering Technical Conferences. ASME Design Engineering Technical Conferences.

[2]  J T Dennerlein,et al.  Tensions of the flexor digitorum superficialis are higher than a current model predicts. , 1998, Journal of biomechanics.

[3]  Derek G. Kamper,et al.  Modeling of Multiarticular Muscles: Importance of Inclusion of Tendon–Pulley Interactions in the Finger , 2009, IEEE Transactions on Biomedical Engineering.

[4]  H. Scherberger,et al.  Musculoskeletal Representation of a Large Repertoire of Hand Grasping Actions in Primates , 2015, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[5]  Scott L. Delp,et al.  A Model of the Upper Extremity for Simulating Musculoskeletal Surgery and Analyzing Neuromuscular Control , 2005, Annals of Biomedical Engineering.

[6]  Joseph D. Towles,et al.  Towards a realistic biomechanical model of the thumb: the choice of kinematic description may be more critical than the solution method or the variability/uncertainty of musculoskeletal parameters. , 2003, Journal of biomechanics.

[7]  D. Pahr,et al.  The effect of the extensor mechanism on maximum isometric fingertip forces: A numerical study on the index finger. , 2016, Journal of biomechanics.

[8]  Thomas Feix,et al.  Estimating thumb–index finger precision grip and manipulation potential in extant and fossil primates , 2015, Journal of The Royal Society Interface.

[9]  Ajay Seth,et al.  Is my model good enough? Best practices for verification and validation of musculoskeletal models and simulations of movement. , 2015, Journal of biomechanical engineering.

[10]  K. Kursa,et al.  In vivo forces generated by finger flexor muscles do not depend on the rate of fingertip loading during an isometric task. , 2005, Journal of biomechanics.

[11]  Kevin D. Hunt,et al.  Positional behavior in the Hominoidea , 1991, International Journal of Primatology.

[12]  Joseph D. Towles,et al.  Quantification of fingertip force reduction in the forefinger following simulated paralysis of extensor and intrinsic muscles. , 2000, Journal of biomechanics.

[13]  D J Giurintano,et al.  A 3D biomechanical model of the hand for power grip. , 2003, Journal of biomechanical engineering.

[14]  A A Amis,et al.  Finger joint force predictions related to design of joint replacements. , 1982, Journal of biomedical engineering.

[15]  David Bendahan,et al.  Quantification of finger joint loadings using musculoskeletal modelling clarifies mechanical risk factors of hand osteoarthritis. , 2014, Medical engineering & physics.

[16]  D. Doran,et al.  Great Ape Societies: Comparative positional behavior of the African apes , 1996 .

[17]  Franck Quaine,et al.  Biomechanical model for the determination of the forces acting on the finger pulley system. , 2006, Journal of biomechanics.

[18]  Edmund Y. S. Chao,et al.  Biomechanics of the hand : a basic research study , 1989 .

[19]  Sergey Koren,et al.  The bonobo genome compared with the chimpanzee and human genomes , 2012, Nature.

[20]  Tsukasa Ogasawara,et al.  A tendon skeletal finger model for evaluation of pinching effort , 2009, 2009 IEEE/RSJ International Conference on Intelligent Robots and Systems.

[21]  K. An,et al.  Tendon excursion and moment arm of index finger muscles. , 1983, Journal of biomechanics.

[22]  Franck Quaine,et al.  Middle and ring fingers are more exposed to pulley rupture than index and little during sport-climbing: a biomechanical explanation. , 2008, Clinical biomechanics.

[23]  E. Vereecke,et al.  Insights into the musculature of the bonobo hand , 2018, Journal of anatomy.

[24]  Eric Jones,et al.  SciPy: Open Source Scientific Tools for Python , 2001 .

[25]  J. Wolff Das Gesetz der Transformation der Knochen , 1893 .

[26]  F. Amirouche,et al.  A clove-hitch suture method for small-caliber tendon ends. , 2012, The Journal of bone and joint surgery. American volume.

[27]  Daniel E Lieberman,et al.  Hand biomechanics during simulated stone tool use. , 2011, Journal of human evolution.

[28]  D. Pahr,et al.  Trabecular Bone Structure Correlates with Hand Posture and Use in Hominoids , 2013, PloS one.

[29]  C. Long,et al.  Intrinsic-extrinsic muscle control of the hand in power grip and precision handling. An electromyographic study. , 1970, The Journal of bone and joint surgery. American volume.

[30]  D. Pahr,et al.  A novel experimental design for the measurement of metacarpal bone loading and deformation and fingertip force , 2018, PeerJ.

[31]  E. Berton,et al.  Effect of object width on muscle and joint forces during thumb-index finger grasping. , 2011, Journal of applied biomechanics.

[32]  Eric Berton,et al.  Quantification of hand and forearm muscle forces during a maximal power grip task. , 2012, Medicine and science in sports and exercise.

[33]  Ayman Habib,et al.  OpenSim: Open-Source Software to Create and Analyze Dynamic Simulations of Movement , 2007, IEEE Transactions on Biomedical Engineering.

[34]  Richard A. Ketcham,et al.  Iconography : Does trabecular bone structure within the metacarpal heads of primates vary with hand posture? , 2017 .

[35]  H. Frost Bone “mass” and the “mechanostat”: A proposal , 1987, The Anatomical record.

[36]  R. L. Susman Comparative and functional morphology of hominoid fingers. , 1979, American journal of physical anthropology.

[37]  Sang Wook Lee,et al.  Estimation of the effective static moment arms of the tendons in the index finger extensor mechanism. , 2008, Journal of biomechanics.

[38]  P. Lemelin,et al.  Anatomy, Function, and Evolution of the Primate Hand Musculature , 2016 .

[39]  K N An,et al.  Normative model of human hand for biomechanical analysis. , 1979, Journal of biomechanics.

[40]  Peter J Keir,et al.  Modelling tendon excursions and moment arms of the finger flexors: anatomic fidelity versus function. , 2011, Journal of biomechanics.

[41]  Derek G. Kamper,et al.  Orthopaedic applications of a validated force-based biomechanical model of the index finger , 2014, 2014 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[42]  F. Zajac,et al.  Large index-fingertip forces are produced by subject-independent patterns of muscle excitation. , 1998, Journal of biomechanics.

[43]  M W Marzke,et al.  Chimpanzee thumb muscle cross sections, moment arms and potential torques, and comparisons with humans. , 1999, American journal of physical anthropology.

[44]  W P Cooney,et al.  Flexor tendon forces: in vivo measurements. , 1992, The Journal of hand surgery.

[45]  Christopher J. Dunmore,et al.  Inverse remodelling algorithm identifies habitual manual activities of primates based on metacarpal bone architecture , 2018, Biomechanics and modeling in mechanobiology.

[46]  E. Zancolli Structural and dynamic bases of hand surgery , 1979 .

[47]  Jack T. Dennerlein,et al.  Extrinsic and Intrinsic Index Finger Muscle Attachments in an OpenSim Upper-Extremity Model , 2014, Annals of Biomedical Engineering.

[48]  R Huiskes,et al.  If bone is the answer, then what is the question? , 2000, Journal of anatomy.