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Human hands-and-knees crawling movement analysis based on time-varying synergy and synchronous synergy theories

Department of Electronic Science and Technology, University of Science and Technology of China, Hefei 230026, Anhui, P.R. China

Special Issues: Advanced Computer Methods and Programs in Biomedicine

This paper aims to investigate human hands-and-knees crawling movement from the aspect of synchronous (SYN) and time-varying (TV) muscle synergy analysis. Nine healthy children and 11 children with cerebral palsy were recruited. During hands-and-knees crawling, surface electromyography (sEMG) signals from 12 main muscles of upper limbs and trunk were recorded, and muscle synergies were extracted based on TV synergy and SYN synergy theories. From the perspectives of repeatability, symmetry and similarity, the abilities of these two types of synergies to characterize crawling movement and to distinguish normal and abnormal crawling were explored. We found that: First, SYN synergy is better than TV synergy in depicting the body symmetry during crawling movement. However, TV synergy is more suitable than SYN synergy for distinguishing normal and abnormal crawling from the perspective of symmetry. Second, the abilities of SYN synergy and TV synergy in depicting the crawling repeatability are not comparable, and both have the potential to depict the crawling abnormality from the perspective of repeatability. Third, from the angle of inter-subject similarity, SYN synergy has the potential to describe the abnormal crawling pattern. However, the large individual differences suggest that TV synergy is a poor choice. This study provides a new way to analyze crawling movement from the perspective of neuromuscular control, and the research findings are meaningful for clinical assessment of abnormal crawling.
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Keywords crawling; cerebral palsy; synchronous synergy; time-varying synergy; surface electromyography

Citation: Teng Li, Xiang Chen, Shuai Cao, Xu Zhang, Xun Chen. Human hands-and-knees crawling movement analysis based on time-varying synergy and synchronous synergy theories. Mathematical Biosciences and Engineering, 2019, 16(4): 2492-2513. doi: 10.3934/mbe.2019125


  • 1. S. K. Patrick, J. A. Noah and J. F. Yang, Developmental constraints of quadrupedal coordination across crawling styles in human infants, J. Neurophysiol., 107 (2012), 3050–3061.
  • 2. M. Hildebrand, Symmetrical gaits of primates, Am. J. Phys. Anthropol., 26 (1967), 119–130.
  • 3. S. K. Patrick, J. A. Noah and J. F. Yang, Interlimb coordination in human crawling reveals similarities in development and neural control with quadrupeds, J. Neurophysiol., 101 (2009) 603–613.
  • 4. M. J. MacLellan, G. Catavitello and Y. P. Ivanenko, et al., Planar covariance of upper and lower limb elevation angles during hand-foot crawling in healthy young adults, Exp. Brain Res., 235 (2017), 3287–3294.
  • 5. S. Ma, X. Chen and S. Cao, et al., Investigation on inter-limb coordination and motion stability, intensity and complexity of trunk and limbs during hands-knees crawling in human adults, Sensors, 17 (2017), 1–15 .
  • 6. X. Chen, X. C. Niu and D. Wu, et al., Investigation of the intra- and inter-Limb muscle coordination of hands-and-knees crawling in human adults by means of muscle synergy analysis, Entropy, 19 (2017), 1–15.
  • 7. Q. L. Xiong, X. Y. Wu and N. Xiao, et al. The variability of co-activation pattern of antagonist muscles in human infant crawling, Annual International Conference of the IEEE Engineering in Medicine and Biology Society, (2016), 331–334.
  • 8. Q. L. Xiong, X. Y. Wu and N. Xiao, et al. Antagonist muscle co-activation of limbs in human infant crawling: A pilot study, Annual International Conference of the IEEE Engineering in Medicine and Biology Society, (2015), 2115–2118.
  • 9. M. J. MacLellan, Y. P. Ivanenko and G. Cappellini, et al., Features of hand-foot crawling behavior in human adults, J. Neurophysiol., 107 (2012), 114–125.
  • 10. S. Gallagher, J. Pollard and W. L. Porter, Locomotion in restricted space: Kinematic and electromyographic analysis of stoopwalking and crawling, Gait Posture, 33 (2011), 71–76.
  • 11. K. E. Adolph, B. Vereijken and M. A. Denny, Learning to crawl, Child Dev., 69 (1998): 1299–1312.
  • 12. M. Bottos, M. L. Puato and A. Vianello, et al., Locomotion pattern in cerebral palsy syndromes, Dev. Med. Child Neurol., 37 (1995), 883–899.
  • 13. M. Hirashima and T. Oya, How does the brain solve muscle redundancy? Filling the gap between optimization and muscle synergy hypotheses. Neurosci. Res., 104 (2016), 80–87.
  • 14. S. Aoi and T. Funato, Neuromusculoskeletal models based on the muscle synergy hypothesis for the investigation of adaptive motor control in locomotion via sensory-motor coordination, Neurosci. Res., 104 (2016), 88–95.
  • 15. A. d'Avella and F. Lacquaniti, Control of reaching movements by muscle synergy combinations. Front. Comput. Neurosci, 7 (2013), 1–7.
  • 16. V. C. K. Cheung, A. d'Avella and M. C. Tresch, et al., Central and sensory contributions to the activation and organization of muscle synergies during natural motor behaviors, J. Neurosci., 25 (2005), 6419–6434.
  • 17. Y. P. Ivanenko, R. E. Poppele and F. Lacquaniti, Five basic muscle activation patterns account for muscle activity during human locomotion. J. Neurophysiol., 556 (2004), 267–282.
  • 18. A. d'Avella, P. Saltiel and E. Bizzi, Combinations of muscle synergies in the construction of a natural motor behavior. Nat. Neurosci., 6 (2003), 300–308.
  • 19. E. Chiovetto, B. Berret and I. Delis, et al., Investigating reduction of dimensionality during single-joint elbow movements: a case study on muscle synergies, Front. Comput. Neurosci., 7 (2013), 1–12.
  • 20. L. Tang, F. Li and S. Cao, et al., Muscle synergy analysis in children with cerebral palsy, J. Neural. Eng., 12 (2015), 1–12.
  • 21. K. M. Steele, A. Rozumalski and M. H. Schwartz, Muscle synergies and complexity of neuromuscular control during gait in cerebral palsy, Dev. Med. Child Neurol., 57 (2015), 1176–1182.
  • 22. A. S. Oliveira, L. Gizzi and D. Farina, et al. Motor modules of human locomotion: influence of EMG averaging, concatenation, and number of step cycles. Front. Hum. Neurosci., 8 (2014), 1–9.
  • 23. E. Zwaan, J. G. Becher and J. Harlaar, Synergy of EMG patterns in gait as an objective measure of muscle selectivity in children with spastic cerebral palsy, Gait Posture, 35 (2012), 111–115.
  • 24. K. Czupryna and J. Nowotny, Changes of kinematics parameters of pelvis during walking under the influence of means facilitates treatment of cerebral palsied children, Ortop. Traumatol. Rehabil., 14 (2012), 453–465.
  • 25. N. Dominici, Y. P. Ivanenko and G. Cappellini, et al., Locomotor primitives in newborn babies and their development, Science, 334 (2011), 997–999.
  • 26. G. T. Oviedo and L. H. Ting, Subject-specific muscle synergies in human balance control are consistent across different biomechanical contexts, J. Neurophysiol., 103 (2010), 3084–3098.
  • 27. M. C. Tresch and A. Jarc, The case for and against muscle synergies. Curr. Opin. Neurobiol., 19 (2009), 601–607.
  • 28. L. H. Ting and J. L. McKay, Neuromechanics of muscle synergies for posture and movement. Curr. Opin. Neurobiol., 17 (2007), 622–628.
  • 29. J. Roh, W. Z. Rymer and E. J. Perreault, et al, Alterations in upper limb muscle synergy structure in chronic stroke survivors, J. Neurophysiol., 109 (2013), 768–781.
  • 30. V. C. K. Cheung, A. Turolla and M. Agostini, et al., Muscle synergy patterns as physiological markers of motor cortical damage, Proc. Natl. Acad. Sci. U.S.A., 109 (2012), 14652–14656.
  • 31. Z. Gao, L. Chen and Q. Xiong, et al. Degraded synergistic recruitment of sEMG oscillations for cerebral palsy infants crawling, Front. Neurol., 9 (2018), 1–12.
  • 32. A. d'Avella and M. C. Tresch. Modularity in the motor system: Decomposition of muscle patterns as combinations of time-varying synergies, Adv. Neural. Inf. Process. Syst., (2002), 141–148.
  • 33. A. d'Avella, A. Portone and L. Fernandez, et al., Control of fast-reaching movements by muscle synergy combinations, J. Neurosci., 26 (2006), 7791–7810.
  • 34. H. J. Hermens, B. Freriks and C. D. Klug, et al., Development of recommendations for SEMG sensors and sensor placement procedures, J. Electromyogr. Kinesiol., 10 (2000), 361–374.
  • 35. D. D. Lee and H. S. Seung, Learning the parts of objects by non-negative matrix factorization, Nature, 401 (1999), 788–791.
  • 36. Q. Huang, D. Tao and X. Li, et al., Parallelized Evolutionary Learning for Detection of Biclusters in Gene Expression Data, IEEE/ACM Trans Comput. Biol. Bioinform., 9 (2012), 560–570.
  • 37. L. Tang, X. Chen and S. Cao, et al., Assessment of Upper Limb Motor Dysfunction for Children with Cerebral Palsy Based on Muscle Synergy Analysis, Front. Hum. Neurosci, 11 (2017), 1–13.
  • 38. A. D'Avella and E. Bizzi, Shared and specific muscle synergies in natural motor behaviors, Proc. Natl. Acad. Sci. U.S.A., 102 (2005), 3076–3081.
  • 39. S. A. Overduin, A. d'Avella and J. Roh, et al., Modulation of muscle synergy recruitment in primate grasping, J. Neurosci., 28 (2008), 880–892.


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