journal article Open Access Aug 31, 2020

Plasticity of muscle synergies through fractionation and merging during development and training of human runners

View at Publisher Save 10.1038/s41467-020-18210-4
Abstract
AbstractComplex motor commands for human locomotion are generated through the combination of motor modules representable as muscle synergies. Recent data have argued that muscle synergies are inborn or determined early in life, but development of the neuro-musculoskeletal system and acquisition of new skills may demand fine-tuning or reshaping of the early synergies. We seek to understand how locomotor synergies change during development and training by studying the synergies for running in preschoolers and diverse adults from sedentary subjects to elite marathoners, totaling 63 subjects assessed over 100 sessions. During development, synergies are fractionated into units with fewer muscles. As adults train to run, specific synergies coalesce to become merged synergies. Presences of specific synergy-merging patterns correlate with enhanced or reduced running efficiency. Fractionation and merging of muscle synergies may be a mechanism for modifying early motor modules (Nature) to accommodate the changing limb biomechanics and influences from sensorimotor training (Nurture).
Topics

No keywords indexed for this article. Browse by subject →

References
65
[1]
Bizzi, E., Hogan, N., Mussa-Ivaldi, F. A. & Giszter, S. Does the nervous system use equilibrium-point control to guide single and multiple joint movements? Behav. Brain. Sci. 15, 603–613 (1992). 10.1017/s0140525x00072538
[2]
Dewolf, A. H., Sylos-Labini, F., Cappellini, G., Lacquaniti, F. & Ivanenko, Y. Emergence of different gaits in infancy: relationship between developing neural circuits and changing biomechanics. Front. Bioengin. Biotech. 8, 473 (2020). 10.3389/fbioe.2020.00473
[3]
Cunningham, J. P. & Yu, B. M. Dimensionality reduction for large-scale neural recordings. Nat. Neurosci. 17, 1500–1509 (2014). 10.1038/nn.3776
[4]
Neural Manifolds for the Control of Movement

Juan A. Gallego, Matthew G. Perich, Lee E. Miller et al.

Neuron 2017 10.1016/j.neuron.2017.05.025
[5]
Cheung, V. C. K., d’Avella, A. & Bizzi, E. Adjustments of motor pattern for load compensation via modulated activations of muscle synergies during natural behaviors. J. Neurophysiol. 101, 1235–1257 (2009). 10.1152/jn.01387.2007
[6]
d’Avella, A. & Bizzi, E. Shared and specific muscle synergies in natural motor behaviors. Proc. Natl Acad. Sci. USA 102, 3076–3081 (2005). 10.1073/pnas.0500199102
[7]
Dominici, N. et al. Locomotor primitives in newborn babies and their development. Science 334, 997–999 (2011). 10.1126/science.1210617
[8]
Yang, Q., Logan, D. & Giszter, S. F. Motor primitives are determined in early development and are then robustly conserved into adulthood. Proc. Natl Acad. Sci. USA 116, 12025–12034 (2019). 10.1073/pnas.1821455116
[9]
Berger, D. J., Gentner, R., Edmunds, T., Pai, D. K. & d’Avella, A. Differences in adaptation rates after virtual surgeries provide direct evidence for modularity. J. Neurosci. 33, 12384–12394 (2013). 10.1523/jneurosci.0122-13.2013
[10]
Neural constraints on learning

Patrick T. Sadtler, Kristin M. Quick, Matthew D. Golub et al.

Nature 2014 10.1038/nature13665
[11]
Yokoyama, H., Ogawa, T., Kawashima, N., Shinya, M. & Nakazawa, K. Distinct sets of locomotor modules control the speed and modes of human locomotion. Sci. Rep. 6, 36275 (2016).
[12]
Kargo, W. J. & Nitz, D. A. Early skill learning is expressed through selection and tuning of cortically represented muscle synergies. J. Neurosci. 23, 11255–11269 (2003). 10.1523/jneurosci.23-35-11255.2003
[13]
Sawers, A., Allen, J. L. & Ting, L. H. Long-term training modifies the modular structure and organization of walking balance control. J. Neurophysiol. 114, 3359–3373 (2015). 10.1152/jn.00758.2015
[14]
Schepens, B., Willems, P. A. & Cavagna, G. A. The mechanics of running in children. J. Physiol. 509.3, 927–940 (1998). 10.1111/j.1469-7793.1998.927bm.x
[15]
Turner, A. M., Owings, M. & Schwane, J. A. Improvement in running economy after 6 weeks of plyometric training. J. Strength Cond. Res. 17, 60–67 (2003).
[16]
McDougall, C. Born to run: the hidden tribe, the ultra-runners, and the greatest race the world has never seen (Profile, London, 2009).
[17]
Hart, C. B. & Giszter, S. F. A neural basis for motor primitives in the spinal cord. J. Neurosci. 30, 1322–1336 (2010). 10.1523/jneurosci.5894-08.2010
[18]
Levine, A. J. et al. Identification of a cellular node for motor control pathways. Nat. Neurosci. 17, 586–593 (2014). 10.1038/nn.3675
[19]
Takei, T., Confais, J., Tomatsu, S., Oya, T. & Seki, K. Neural basis for hand muscle synergies in the primate spinal cord. Proc. Natl Acad. Sci. USA 114, 8643–8648 (2017). 10.1073/pnas.1704328114
[20]
Amundsen Huffmaster, S. L., Van Acker, G. M., Luchies, C. W. & Cheney, P. D. Muscle synergies obtained from comprehensive mapping of the cortical forelimb representation using stimulus triggered averaging of EMG activity. J. Neurosci. 38, 8759–8771 (2018). 10.1523/jneurosci.2519-17.2018
[21]
Neuromechanical Principles Underlying Movement Modularity and Their Implications for Rehabilitation

Lena H. Ting, Hillel J. Chiel, Randy D. Trumbower et al.

Neuron 2015 10.1016/j.neuron.2015.02.042
[22]
Bizzi, E. & Cheung, V. C. K. The neural origin of muscle synergies. Front. Comput. Neurosci. 7, 51 (2013). 10.3389/fncom.2013.00051
[23]
Cappellini, G., Ivanenko, Y. P., Poppele, R. E. & Lacquaniti, F. Motor patterns in human walking and running. J. Neurophysiol. 95, 3426–3437 (2006). 10.1152/jn.00081.2006
[24]
Santuz, A. et al. Modular control of human movement during running: an open access data set. Front. Physiol. 9, 1509 (2018). 10.3389/fphys.2018.01509
[25]
Santuz, A., Ekizos, A., Janshen, L., Baltzopoulos, V. & Arampatzis, A. The influence of footwear on the modular organization of running. Front. Physiol. 8, 958 (2017). 10.3389/fphys.2017.00958
[26]
Cheung, V. C. K. et al. Muscle synergy patterns as physiological markers of motor cortical damage. Proc. Natl Acad. Sci. USA 109, 14652–14656 (2012). 10.1073/pnas.1212056109
[27]
McCrea, D. A. & Rybak, I. A. Organization of mammalian locomotor rhythm and pattern generation. Brain Res. Rev. 57, 134–146 (2008). 10.1016/j.brainresrev.2007.08.006
[28]
Kurz, E., Faude, O., Roth, R., Zahner, L. & Donath, L. Ankle muscle activity modulation during single-leg stance differs between children, young adults and seniors. Eur. J. Appl. Physiol. 118, 239–247 (2018). 10.1007/s00421-017-3764-0
[29]
Woollacott, M. H. & Shumway-Cook, A. Changes in posture control across the life span–a systems approach. Phys. Ther. 70, 799–807 (1990). 10.1093/ptj/70.12.799
[30]
Oba, N., Sasagawa, S., Yamamoto, A. & Nakazawa, K. Difference in postural control during quiet standing between young children and adults: assessment with center of mass acceleration. PLoS One. 10, e0140235 (2015). 10.1371/journal.pone.0140235
[31]
Zelik, K. E., La Scaleia, V., Ivanenko, Y. P. & Lacquaniti, F. Can modular strategies simplify neural control of multidirectional human locomotion? J. Neurophysiol. 111, 1686–1702 (2014). 10.1152/jn.00776.2013
[32]
Sylos-Labini, F. et al. Distinct locomotor precursors in newborn babies. Proc. Natl Acad. Sci. USA 117, 9604–9612 (2020). 10.1073/pnas.1920984117
[33]
Todorov, E. & Jordan, M. I. Optimal feedback control as a theory of motor coordination. Nat. Neurosci. 5, 1226–1235 (2002). 10.1038/nn963
[34]
Hamner, S. R. & Delp, S. L. Muscle contributions to fore-aft and vertical body mass center accelerations over a range of running speeds. J. Biomech. 46, 780–787 (2013). 10.1016/j.jbiomech.2012.11.024
[35]
Tam, N., Santos-Concejero, J., Coetzee, D. R., Noakes, T. D. & Tucker, R. Muscle co-activation and its influence on running performance and risk of injury in elite Kenyan runners. J. Sports Sci. 35, 175–181 (2017). 10.1080/02640414.2016.1159717
[36]
Hamner, S. R., Seth, A. & Delp, S. L. Muscle contributions to propulsion and support during running. J. Biomech. 43, 2709–2716 (2010). 10.1016/j.jbiomech.2010.06.025
[37]
Hinrichs, R. N., Cavanagh, P. R. & Williams, K. R. Upper extremity function in running. I: center of mass and propulsion considerations. Int. J. Sport Biomech. 3, 222–241 (1987). 10.1123/ijsb.3.3.222
[38]
Chan, Z. Y., Zhang, J. H., Ferber, R., Shum, G. & Cheung, R. T. H. The effects of midfoot strike gait retraining on impact loading and joint stiffness. Phys. Ther. Sp. 42, 139–145 (2020). 10.1016/j.ptsp.2020.01.011
[39]
Shih, Y. O., Teng, H. L. & Powers, C. M. Lower extremity stiffness predicts ground reaction force loading rate in heel strike runners. Med. Sci. Sp. Exerc. 51, 1692–1697 (2019). 10.1249/mss.0000000000001963
[40]
Hunter, I. A new approach to modeling vertical stiffness in heel-toe distance runners. J. Sp. Sci. Med. 2, 139 (2003).
[41]
Arellano, C. J. & Kram, R. The effects of step width and arm swing on energetic cost and lateral balance during running. J. Biomech. 44, 1291–1295 (2011). 10.1016/j.jbiomech.2011.01.002
[42]
DeVita, P., Fellin, R. E., Seay, J. F., Ip, E., Stavro, N. & Messier, S. P. The relationships between age and running biomechanics. Med. Sci. Sp. Exerc. 48, 98–106 (2016). 10.1249/mss.0000000000000744
[43]
Yokoyama, H., Ogawa, T., Shinya, M., Kawashima, N. & Nakazawa, K. Speed dependency in α-motoneuron activity and locomotor modules in human locomotion: indirect evidence for phylogenetically conserved spinal circuits. Proc. R. Soc. B: Biol. Sci. 284, 20170290 (2017). 10.1098/rspb.2017.0290
[44]
Caggiano, V., Cheung, V. C. K. & Bizzi, E. An optogenetic demonstration of motor modularity in the mammalian spinal cord. Sci. Rep. 6, 35185 (2016). 10.1038/srep35185
[45]
Desrochers, E., Harnie, J., Doelman, A., Hurteau, M. F. & Frigon, A. Spinal control of muscle synergies for adult mammalian locomotion. J. Physiol. 597, 333–350 (2019). 10.1113/jp277018
[46]
Cheung, V. C. K., Niu, C. M., Li, S., Xie, Q. & Lan, N. A novel FES strategy for poststroke rehabilitation based on the natural organization of neuromuscular control. IEEE Rev. Biomed. Engin. 12, 154–167 (2019). 10.1109/rbme.2018.2874132
[47]
Clark, D. J., Ting, L. H., Zajac, F. E., Neptune, R. R. & Kautz, S. A. Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity post-stroke. J. Neurophysiol. 103, 844–857 (2010). 10.1152/jn.00825.2009
[48]
Hayes, H. B., Chvatal, S. A., French, M. A., Ting, L. H. & Trumbower, R. D. Neuromuscular constraints on muscle coordination during overground walking in persons with chronic incomplete spinal cord injury. Clin. Neurophysiol. 125, 2024–2035 (2014). 10.1016/j.clinph.2014.02.001
[49]
Wu, H. G., Miyamoto, Y. R., Castro, L. N. G., Ölveczky, B. P. & Smith, M. A. Temporal structure of motor variability is dynamically regulated and predicts motor learning ability. Nat. Neurosci. 17, 312 (2014). 10.1038/nn.3616
[50]
Cheung, V. C. K., Zheng, X. C., Cheung, R. T. H. & Chan, R. H. M. Modulating the structure of motor variability for skill learning through specific muscle synergies in elderlies and young adults. IEEE Open J. Engin. Med. Biol. 1, 33–40 (2020). 10.1109/ojemb.2019.2963666

Showing 50 of 65 references

Metrics
148
Citations
65
References
Details
Published
Aug 31, 2020
Vol/Issue
11(1)
License
View
Funding
Research Grants Council, University Grants Committee Award: 24115318
Hong Kong Polytechnic University Award: n/a
Chinese University of Hong Kong Award: FIA2016/A/04
Cite This Article
Vincent C. K. Cheung, Ben M. F. Cheung, Janet H. Zhang, et al. (2020). Plasticity of muscle synergies through fractionation and merging during development and training of human runners. Nature Communications, 11(1). https://doi.org/10.1038/s41467-020-18210-4
Related

You May Also Like

Inferring tumour purity and stromal and immune cell admixture from expression data

Kosuke Yoshihara, Maria Shahmoradgoli · 2013

7,687 citations

Inference and analysis of cell-cell communication using CellChat

Suoqin Jin, Christian F. Guerrero-Juarez · 2021

6,760 citations

In situ click chemistry generation of cyclooxygenase-2 inhibitors

Atul Bhardwaj, Jatinder Kaur · 2017

6,689 citations