Analysis of High-Dimensional Coordination in Human Movement Using Variance Spectrum Scaling and Intrinsic Dimensionality
Abstract
:1. Introduction
From Dimensionality Reduction to Manifold Smoothness
2. Materials and Methods
2.1. Finite Size Kuramoto System Around the Critical Region of Coupling Strength
Analysis
2.2. Human Gait Recorded with High-Density Motion Tracking
2.2.1. Study Population
2.2.2. Protocol and Equipment
2.2.3. Analysis
3. Results
3.1. Variance Scaling in the Kuramoto System
3.2. Variance Scaling in Human Gait
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
- Bernstein, N.A. The Coordination and Regulation of Movements; Pergamon Press: Oxford, UK, 1967. [Google Scholar]
- Latash, M.L.; Turvey, M.T. (Eds.) Dexterity and Its Development; Psychology Press: New York, NY, USA, 1996; ISBN 978-1-4106-0335-7. [Google Scholar]
- Profeta, V.L.S.; Turvey, M.T. Bernstein’s levels of movement construction: A contemporary perspective. Hum. Mov. Sci. 2018, 57, 111–133. [Google Scholar] [CrossRef] [PubMed]
- Kelso, J.A.S.; Tuller, B. Toward a theory of apractic syndromes. Brain Lang. 1981, 12, 224–245. [Google Scholar] [CrossRef]
- Latash, M.L. The bliss (not the problem) of motor abundance (not redundancy). Exp. Brain Res. 2012, 217, 1–5. [Google Scholar] [CrossRef] [PubMed]
- Latash, M.L. One more time about motor (and non-motor) synergies. Exp. Brain Res. 2021, 239, 2951–2967. [Google Scholar] [CrossRef]
- Vereijken, B.; Emmerik, R.V.; Whiting, H.T.A.; Newell, K.M. Free(z)ing Degrees of Freedom in Skill Acquisition. J. Mot. Behav. 1992, 24, 133–142. [Google Scholar] [CrossRef]
- Verhoeven, F.M.; Newell, K.M. Coordination and control of posture and ball release in basketball free-throw shooting. Hum. Mov. Sci. 2016, 49, 216–224. [Google Scholar] [CrossRef]
- Guimarães, A.N.; Ugrinowitsch, H.; Dascal, J.B.; Porto, A.B.; Okazaki, V.H.A. Freezing Degrees of Freedom During Motor Learning: A Systematic Review. Mot. Control 2020, 24, 457–471. [Google Scholar] [CrossRef]
- Minino, R.; Liparoti, M.; Romano, A.; Mazzeo, F.; Sorrentino, P.; Tafuri, D.; Troisi Lopez, E. The influence of auditory stimulation on whole body variability in healthy older adults during gait. J. Biomech. 2024, 172, 112222. [Google Scholar] [CrossRef]
- Toiviainen, P.; Hartmann, M. Analyzing multidimensional movement interaction with generalized cross-wavelet transform. Hum. Mov. Sci. 2022, 81, 102894. [Google Scholar] [CrossRef]
- van Diest, M.; Stegenga, J.; Wörtche, H.J.; Roerdink, J.B.T.M.; Verkerke, G.J.; Lamoth, C.J.C. Quantifying Postural Control during Exergaming Using Multivariate Whole-Body Movement Data: A Self-Organizing Maps Approach. PLoS ONE 2015, 10, e0134350. [Google Scholar] [CrossRef]
- Liu, K.; Wang, H.; Xiao, J. The Multivariate Largest Lyapunov Exponent as an Age-Related Metric of Quiet Standing Balance. Comput. Math. Methods Med. 2015, 2015, 309756. [Google Scholar] [CrossRef] [PubMed]
- Romano, M.C.; Thiel, M.; Kurths, J.; Bloh, W.V. Multivariate recurrence plots. Phys. Lett. Sect. A Gen. At. Solid State Phys. 2004, 330, 214–223. [Google Scholar] [CrossRef]
- Frank, T.D.; Richardson, M.J. On a test statistic for the Kuramoto order parameter of synchronization: An illustration for group synchronization during rocking chairs. Phys. D Nonlinear Phenom. 2010, 239, 2084–2092. [Google Scholar] [CrossRef]
- Alderisio, F.; Fiore, G.; Salesse, R.N.; Bardy, B.G.; Bernardo, M.D. Interaction patterns and individual dynamics shape the way we move in synchrony. Sci. Rep. 2017, 7, 6846. [Google Scholar] [CrossRef] [PubMed]
- Zhang, M.; Kalies, W.D.; Kelso, J.A.S.; Tognoli, E. Topological portraits of multiscale coordination dynamics. J. Neurosci. Methods 2020, 339, 108672. [Google Scholar] [CrossRef] [PubMed]
- Daffertshofer, A.; Lamoth, C.J.C.; Meijer, O.G.; Beek, P.J. PCA in studying coordination and variability: A tutorial. Clin. Biomech. 2004, 19, 415–428. [Google Scholar] [CrossRef]
- Gloumakov, Y.; Spiers, A.J.; Dollar, A.M. Dimensionality Reduction and Motion Clustering During Activities of Daily Living: Three-, Four-, and Seven-Degree-of-Freedom Arm Movements. IEEE Trans. Neural Syst. Rehabil. Eng. 2020, 28, 2826–2836. [Google Scholar] [CrossRef]
- Stringer, C.; Pachitariu, M.; Steinmetz, N.; Carandini, M.; Harris, K.D. High-dimensional geometry of population responses in visual cortex. Nature 2019, 571, 361–365. [Google Scholar] [CrossRef]
- Piergiovanni, S.; Terrier, P. Validity of Linear and Nonlinear Measures of Gait Variability to Characterize Aging Gait with a Single Lower Back Accelerometer. Sensors 2024, 24, 7427. [Google Scholar] [CrossRef]
- de Veronez, S.O.; do Espirito-Santo, C.C.; de Dantas, A.F.O.A.; Pereira, N.D.; Ilha, J. The use of nonlinear analysis in understanding postural control: A scoping review. Hum. Mov. Sci. 2024, 96, 103246. [Google Scholar] [CrossRef]
- Marjaninejad, A.; Valero-Cuevas, F.J. Should Anthropomorphic Systems be “Redundant”? In Biomechanics of Anthropomorphic Systems; Venture, G., Laumond, J.-P., Watier, B., Eds.; Springer International Publishing: Cham, Switzerland, 2019; pp. 7–34. ISBN 978-3-319-93870-7. [Google Scholar]
- Van Der Maaten, L.; Postma, E.O.; van den Herik, H.J. Dimensionality reduction: A comparative review. J. Mach. Learn. Res. 2009, 10, 13. [Google Scholar]
- Fuchs, A.; Scott Kelso, J.A. Coordination Dynamics and Synergetics: From Finger Movements to Brain Patterns and Ballet Dancing. In Complexity and Synergetics; Müller, S.C., Plath, P.J., Radons, G., Fuchs, A., Eds.; Springer International Publishing: Cham, Switzerland, 2018; pp. 301–316. ISBN 978-3-319-64334-2. [Google Scholar]
- Cunningham, J.P.; Yu, B.M. Dimensionality reduction for large-scale neural recordings. Nat. Neurosci. 2014, 17, 1500–1509. [Google Scholar] [CrossRef] [PubMed]
- Kelso, J.A.S.; Bressler, S.L.; Buchanan, S.; DeGuzman, G.C.; Ding, M.; Fuchs, A.; Holroyd, T. A phase transition in human brain and behavior. Phys. Lett. A 1992, 169, 134–144. [Google Scholar] [CrossRef]
- Fuchs, A.; Mayville, J.M.; Cheyne, D.; Weinberg, H.; Deecke, L.; Kelso, J.A.S. Spatiotemporal Analysis of Neuromagnetic Events Underlying the Emergence of Coordinative Instabilities. NeuroImage 2000, 12, 71–84. [Google Scholar] [CrossRef] [PubMed]
- Kelso, J.a.S.; Fuchs, A.; Lancaster, R.; Holroyd, T.; Cheyne, D.; Weinberg, H. Dynamic cortical activity in the human brain reveals motor equivalence. Nature 1998, 392, 814–818. [Google Scholar] [CrossRef]
- Fuchs, A.; Jirsa, V.K.; Kelso, J.S. Theory of the relation between human brain activity (MEG) and hand movements. Neuroimage 2000, 11, 359–369. [Google Scholar] [CrossRef]
- Frank, T.D.; Daffertshofer, A.; Peper, C.E.; Beek, P.J.; Haken, H. Towards a comprehensive theory of brain activity: Coupled oscillator systems under external forces. Phys. D Nonlinear Phenom. 2000, 144, 62–86. [Google Scholar] [CrossRef]
- Juhász, R.; Kelling, J.; Ódor, G. Critical dynamics of the Kuramoto model on sparse random networks. J. Stat. Mech. 2019, 2019, 053403. [Google Scholar] [CrossRef]
- Ódor, G.; Kelling, J. Critical synchronization dynamics of the Kuramoto model on connectome and small world graphs. Sci. Rep. 2019, 9, 19621. [Google Scholar] [CrossRef]
- Popovych, O.V.; Maistrenko, Y.L.; Tass, P.A. Phase chaos in coupled oscillators. Phys. Rev. E 2005, 71, 3–6. [Google Scholar] [CrossRef]
- Maistrenko, Y.L.; Popovych, O.V.; Tass, P.A. Desynchronization and chaos in the Kuramoto model. In Dynamics of Coupled Map Lattices and of Related Spatially Extended Systems; Lecture Notes in Physics; Springer: Berlin/Heidelberg, Germany, 2005; Volume 671, ISBN 3-540-24289-9. [Google Scholar]
- Breakspear, M.; Heitmann, S.; Daffertshofer, A. Generative models of cortical oscillations: Neurobiological implications of the Kuramoto model. Front. Hum. Neurosci. 2010, 4, 190. [Google Scholar] [CrossRef] [PubMed]
- Dotov, D.; Delasanta, L.; Cameron, D.J.; Large, E.W.; Trainor, L. Collective dynamics support group drumming, reduce variability, and stabilize tempo drift. eLife 2022, 11, e74816. [Google Scholar] [CrossRef]
- Acebrón, J.A.; Bonilla, L.L.; Vicente, C.J.P.; Ritort, F.; Spigler, R. The Kuramoto model: A simple paradigm for synchronization phenomena. Rev. Mod. Phys. 2005, 77, 137–185. [Google Scholar] [CrossRef]
- Bertaux, A.; Gueugnon, M.; Moissenet, F.; Orliac, B.; Martz, P.; Maillefert, J.-F.; Ornetti, P.; Laroche, D. Gait analysis dataset of healthy volunteers and patients before and 6 months after total hip arthroplasty. Sci. Data 2022, 9, 399. [Google Scholar] [CrossRef] [PubMed]
- Grassberger, P.; Procaccia, I. Measuring the strangeness of strange attractors. Phys. D Nonlinear Phenom. 1983, 9, 189–208. [Google Scholar] [CrossRef]
- Levina, E.; Bickel, P.J. Maximum Likelihood estimation of intrinsic dimension. In Proceedings of the 18th International Conference on Neural Information Processing Systems, Vancouver, BC, Canada, 1 December 2004; MIT Press: Cambridge, MA, USA, 2004; pp. 777–784. [Google Scholar]
- Kelso, J.A.S. Unifying large- and small-scale theories of coordination. Entropy 2021, 23, 537. [Google Scholar] [CrossRef] [PubMed]
- Harrison, S.J.; Kinsella-Shaw, J.M.; Dotov, D. Effects of footedness and stance asymmetry confirm an inter-leg metastable coordination dynamics of standing posture. J. Mot. Behav. 2021, 53, 135–156. [Google Scholar] [CrossRef]
- Nah, M.C.; Krotov, A.; Russo, M.; Sternad, D.; Hogan, N. Learning to manipulate a whip with simple primitive actions—A simulation study. iScience 2023, 26, 107395. [Google Scholar] [CrossRef]
- Bruno, A.M.; Frost, W.N.; Humphries, M.D. A spiral attractor network drives rhythmic locomotion. eLife 2017, 6, e27342. [Google Scholar] [CrossRef]
- Altan, E.; Solla, S.A.; Miller, L.E.; Perreault, E.J. Estimating the dimensionality of the manifold underlying multi-electrode neural recordings. PLoS Comput. Biol. 2021, 17, e1008591. [Google Scholar] [CrossRef]
- Fortunato, C.; Bennasar-Vázquez, J.; Park, J.; Chang, J.C.; Miller, L.E.; Dudman, J.T.; Perich, M.G.; Gallego, J.A. Nonlinear manifolds underlie neural population activity during behaviour. bioRxiv 2023. [Google Scholar] [CrossRef]
- Shenoy, K.V.; Sahani, M.; Churchland, M.M. Cortical Control of Arm Movements: A Dynamical Systems Perspective. Annu. Rev. Neurosci. 2013, 36, 337–359. [Google Scholar] [CrossRef]
- Ting, L.H. Dimensional reduction in sensorimotor systems: A framework for understanding muscle coordination of posture. In Progress in Brain Research; Cisek, P., Drew, T., Kalaska, J.F., Eds.; Elsevier: Amsterdam, The Netherlands, 2007; Volume 165, pp. 299–321. [Google Scholar]
- Churchland, A.K.; Abbott, L.F. Conceptual and technical advances define a key moment for theoretical neuroscience. Nat. Neurosci. 2016, 19, 348–349. [Google Scholar] [CrossRef] [PubMed]
- Churchland, M.M.; Cunningham, J.P.; Kaufman, M.T.; Foster, J.D.; Nuyujukian, P.; Ryu, S.I.; Shenoy, K.V. Neural population dynamics during reaching. Nature 2012, 487, 51–56. [Google Scholar] [CrossRef] [PubMed]
- Vyas, S.; Golub, M.D.; Sussillo, D.; Shenoy, K.V. Computation Through Neural Population Dynamics. Annu. Rev. Neurosci. 2020, 43, 249–275. [Google Scholar] [CrossRef]
- Yan, Y.; Goodman, J.M.; Moore, D.D.; Solla, S.A.; Bensmaia, S.J. Unexpected complexity of everyday manual behaviors. Nat. Commun. 2020, 11, 3564. [Google Scholar] [CrossRef]
- Abarbanel, H.D.I. Analysis of Observed Chaotic Data; Springer: Berlin/Heidelberg, Germany, 1996. [Google Scholar]
- Full, R.J.; Koditschek, D.E. Templates and anchors: Neuromechanical hypotheses of legged locomotion on land. J. Exp. Biol. 1999, 202, 3325–3332. [Google Scholar] [CrossRef]
- Holt, K.G.; Jeng, S.F.; Ratcliffe, R.; Hamill, J. Energetic Cost and Stability during Human Walking at the Preferred Stride Frequency. J. Mot. Behav. 1995, 27, 164–178. [Google Scholar] [CrossRef]
- Kuo, A.D. The six determinants of gait and the inverted pendulum analogy: A dynamic walking perspective. Hum. Mov. Sci. 2007, 26, 617–656. [Google Scholar] [CrossRef]
- Kugler, P.N.; Turvey, M.T. Information, Natural Law, and the Self-Assembly of Rhythmic Movement; Lawrence Erlbaum Associates, Inc.: Mahwah, NJ, USA, 1987. [Google Scholar]
- Kelso, J.A.S. Dynamic Patterns: The Self-Organization of Brain and Behavior; MIT Press: Cambridge, MA, USA, 1995; ISBN 978-0-262-61131-2. [Google Scholar]
- Kelso, J.A.S. Multistability and metastability: Understanding dynamic coordination in the brain. Philos. Trans. R. Soc. London. Ser. B Biol. Sci. 2012, 367, 906–918. [Google Scholar] [CrossRef]
- Park, J.; Wu, Y.-H.; Lewis, M.M.; Huang, X.; Latash, M.L. Changes in multifinger interaction and coordination in Parkinson’s disease. J. Neurophysiol. 2012, 108, 915–924. [Google Scholar] [CrossRef] [PubMed]
- Latash, M.L.; Scholz, J.P.; Schöner, G. Motor control strategies revealed in the structure of motor variability. Exerc. Sport Sci. Rev. 2002, 30, 26–31. [Google Scholar] [CrossRef] [PubMed]
- Stergiou, N.; Harbourne, R.T.; Cavanaugh, J.T. Optimal Movement Variability: A New Theoretical Perspective for Neurologic Physical Therapy. J. Neurol. Phys. Ther. 2006, 30, 120–129. [Google Scholar] [CrossRef]
- Dotov, D.G.; Bayard, S.; Cochen de Cock, V.; Geny, C.; Driss, V.; Garrigue, G.; Bardy, B.; Dalla Bella, S. Biologically-variable rhythmic auditory cues are superior to isochronous cues in fostering natural gait variability in Parkinson’s disease. Gait Posture 2017, 51, 64–69. [Google Scholar] [CrossRef] [PubMed]
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Dotov, D.; Gu, J.; Hotor, P.; Spyra, J. Analysis of High-Dimensional Coordination in Human Movement Using Variance Spectrum Scaling and Intrinsic Dimensionality. Entropy 2025, 27, 447. https://doi.org/10.3390/e27040447
Dotov D, Gu J, Hotor P, Spyra J. Analysis of High-Dimensional Coordination in Human Movement Using Variance Spectrum Scaling and Intrinsic Dimensionality. Entropy. 2025; 27(4):447. https://doi.org/10.3390/e27040447
Chicago/Turabian StyleDotov, Dobromir, Jingxian Gu, Philip Hotor, and Joanna Spyra. 2025. "Analysis of High-Dimensional Coordination in Human Movement Using Variance Spectrum Scaling and Intrinsic Dimensionality" Entropy 27, no. 4: 447. https://doi.org/10.3390/e27040447
APA StyleDotov, D., Gu, J., Hotor, P., & Spyra, J. (2025). Analysis of High-Dimensional Coordination in Human Movement Using Variance Spectrum Scaling and Intrinsic Dimensionality. Entropy, 27(4), 447. https://doi.org/10.3390/e27040447