Abstract
The aim of this study was to develop a methodology based on muscle synergies to investigate whether rectilinear and curvilinear walking shared the same neuro-motor organization, and how this organization was fine-tuned by the walking condition. Thirteen healthy subjects walked on rectilinear and curvilinear paths. Electromyographic data from thirteen back and lower-limb muscles were acquired, together with kinematic data using inertial sensors. Four macroscopically invariant muscle synergies, extracted through non-negative matrix factorization, proved a shared modular organization across conditions. The fine-tuning of muscle synergies was studied through non-negative matrix reconstruction, applied by fixing muscle weights or activation profiles to those of the rectilinear condition. The activation profiles tended to be recruited for a longer period and with a larger amplitude during curvilinear walking. The muscles of the posterior side of the lower limb were those mainly influenced by the fine-tuning, with the muscles inside the rotation path being more active than the outer muscles. This study shows that rectilinear and curvilinear walking share a unique motor command. However, a fine-tuning in muscle synergies is introduced during curvilinear conditions, adapting the kinematic strategy to the new biomechanical needs.
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References
Allen, J. L., and R. R. Neptune. Three-dimensional modular control of human walking. J. Biomech. 45:2157–2163, 2012.
Ambrosini, E., C. De Marchis, A. Pedrocchi, G. Ferrigno, M. Monticone, M. Schmid, T. D’Alessio, S. Conforto, and S. Ferrante. Neuro-Mechanics of Recumbent Leg Cycling in Post-Acute Stroke Patients. Ann. Biomed. Eng. 44:3238–3251, 2016.
Bizzi, E., and V. C. K. Cheung. The neural origin of muscle synergies. Front. Comput. Neurosci. 7:51, 2013.
Burden, A., M. Trew, and V. Baltzopoulos. Normalisation of gait EMGs: A re-examination. J. Electromyogr. Kinesiol. 13:519–532, 2003.
Bussmann, J. B., W. L. Martens, J. H. Tulen, F. C. Schasfoort, H. J. van den Berg-Emons, and H. J. Stam. Measuring daily behavior using ambulatory accelerometry: the Activity Monitor. Behav. Res. Methods. Instrum. Comput. 33:349–356, 2001.
Campanini, I., A. Merlo, P. Degola, R. Merletti, G. Vezzosi, and D. Farina. Effect of electrode location on EMG signal envelope in leg muscles during gait. J. Electromyogr. Kinesiol. 17:515–526, 2007.
Cappellini, G., Y. P. Ivanenko, R. E. Poppele, and F. Lacquaniti. Motor patterns in human walking and running. J. Neurophysiol. 95:3426–3437, 2006.
Cheung, V. C. K., A. d’Avella, and E. Bizzi. Adjustments of motor pattern for load compensation via modulated activations of muscle synergies during natural behaviors. J. Neurophysiol. 101:1235–1257, 2008.
Cheung, V. C. K., A. d’Avella, M. C. Tresch, and E. Bizzi. Central and sensory contributions to the activation and organization of muscle synergies during natural motor behaviors. J. Neurosci. 25:6419–6434, 2005.
Cheung, V. C. K., A. Turolla, M. Agostini, S. Silvoni, C. Bennis, P. Kasi, S. Paganoni, P. Bonato, and E. Bizzi. Muscle synergy patterns as physiological markers of motor cortical damage. Proc. Natl. Acad. Sci. 109:14652–14656, 2012.
Chia Bejarano, N. E. Ambrosini, A. Pedrocchi, G. Ferrigno, M. Monticone, and S. Ferrante. A Novel Adaptive, Real-Time Algorithm to Detect Gait Events From Wearable Sensors. IEEE Trans. Neural Syst. Rehabil. Eng. 23:413–422, 2015.
Chvatal, S. A., and L. H. Ting. Common muscle synergies for balance and walking. Front. Comput. Neurosci. 7:48, 2013.
Clark, D. J., L. H. Ting, F. E. Zajac, R. R. Neptune, and S. A. Kautz. Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity post-stroke. J. Neurophysiol. 103:844–857, 2010.
Courtine, G., C. Papaxanthis, and M. Schieppati. Coordinated modulation of locomotor muscle synergies constructs straight-ahead and curvilinear walking in humans. Exp. Brain Res. 170:320–335, 2006.
Courtine, G., and M. Schieppati. Human walking along a curved path. II. Gait features and EMG patterns. Eur. J. Neurosci. 18:191–205, 2003.
Courtine, G., and M. Schieppati. Tuning of a Basic Coordination Pattern Constructs Straight-Ahead and Curved Walking in Humans. J. Neurophysiol. 91:1524–1535, 2004.
Dominici, N., Y. P. Ivanenko, G. Cappellini, A. D’Avella, V. Mondì, M. Cicchese, A. Fabiano, T. Silei, A. Di Paolo, C. Giannini, R. E. Poppele, and F. Lacquaniti. Locomotor primitives in newborn babies and their development. Science 334:997–999, 2011.
Duval, K., K. Luttin, and T. Lam. Neuromuscular strategies in the paretic leg during curved walking in individuals post-stroke. J. Neurophysiol. 106:280–290, 2011.
Ferrante, S., and N. Chia. Bejarano, E. Ambrosini, A. Nardone, A. M. Turcato, M. Monticone, G. Ferrigno, and A. Pedrocchi. A Personalized Multi-Channel FES Controller Based on Muscle Synergies to Support Gait Rehabilitation after Stroke. Front. Neurosci. 10:425, 2016.
Gizzi, L., J. F. Nielsen, F. Felici, Y. P. Ivanenko, and D. Farina. Impulses of activation but not motor modules are preserved in the locomotion of subacute stroke patients. J. Neurophysiol. 106:202–210, 2011.
Glaister, B. C., G. C. Bernatz, G. K. Klute, and M. S. Orendurff. Video task analysis of turning during activities of daily living. Gait Posture 25:289–294, 2007.
Godi, M., A. Nardone, and M. Schieppati. Curved walking in hemiparetic patients. J. Rehabil. Med. 42:858–865, 2010.
Godi, M., A. M. Turcato, M. Schieppati, and A. Nardone. Test-retest reliability of an insole plantar pressure system to assess gait along linear and curved trajectories. J. Neuroengineering Rehabil. 11:95, 2014.
Guglielmetti, S., A. Nardone, A. M. De Nunzio, M. Godi, and M. Schieppati. Walking along circular trajectories in Parkinson’s disease. Mov. Disord. 24:598–604, 2009.
Hayes, H. B., S. A. Chvatal, M. A. French, L. H. Ting, and R. D. Trumbower. Neuromuscular constraints on muscle coordination during overground walking in persons with chronic incomplete spinal cord injury. Clin. Neurophysiol. 125:2024–2035, 2014.
Hershler, C., and M. Milner. An Optimality Criterion for Processing Electromyographic (EMG) Signals Relating to Human Locomotion. IEEE Trans. Biomed. Eng. 25:413–420, 1978.
Honeine, J.-L., M. Schieppati, O. Gagey, and M.-C. Do. By counteracting gravity, triceps surae sets both kinematics and kinetics of gait. Physiol. Rep. 2:e00229, 2014.
Hug, F., N. A. Turpin, A. Couturier, and S. Dorel. Consistency of muscle synergies during pedaling across different mechanical constraints. J. Neurophysiol. 106:91–103, 2011.
Ivanenko, Y. P., G. Cappellini, N. Dominici, R. E. Poppele, and F. Lacquaniti. Coordination of locomotion with voluntary movements in humans. J. Neurosci. 25:7238–7253, 2005.
Ivanenko, Y. P., R. E. Poppele, and F. Lacquaniti. Five basic muscle activation patterns account for muscle activity during human locomotion. J. Physiol. 556:267–282, 2004.
Lee, D. D., and H. S. Seung. Learning the parts of objects by non-negative matrix factorization. Nature 401:788–791, 1999.
Lowry, K. A., J. S. Brach, R. D. Nebes, S. A. Studenski, and J. M. VanSwearingen. Contributions of Cognitive Function to Straight- and Curved-Path Walking in Older Adults. Arch. Phys. Med. Rehabil. 93:802–807, 2012.
McGowan, C. P., R. R. Neptune, D. J. Clark, and S. A. Kautz. Modular control of human walking: Adaptations to altered mechanical demands. J. Biomech. 43:412–419, 2010.
Monaco, V., A. Ghionzoli, and S. Micera. Age-related modifications of muscle synergies and spinal cord activity during locomotion. J. Neurophysiol. 104:2092–2102, 2010.
Muceli, S., A. T. Boye, A. D’Avella, and D. Farina. Identifying representative synergy matrices for describing muscular activation patterns during multidirectional reaching in the horizontal plane. J. Neurophysiol. 103:1532–1542, 2010.
Oliveira, A. S., L. Gizzi, D. Farina, and U. G. Kersting. Motor modules of human locomotion: influence of EMG averaging, concatenation, and number of step cycles. Front. Hum. Neurosci. 8:335, 2014.
Pirondini, E., M. Coscia, A. Crema, M. Mancuso, and S. Micera. How the selection of muscles influences their synergies? A preliminary study using real data. In: 6th International IEEE/EMBS Conference on Neural Engineering (NER) (IEEE), 2013, pp. 581–584.
Rosenblatt, N. J., and M. D. Grabiner. Measures of frontal plane stability during treadmill and overground walking. Gait Posture 31:380–384, 2010.
Routson, R. L., S. A. Kautz, and R. R. Neptune. Modular organization across changing task demands in healthy and poststroke gait. Physiol. Rep. 2:e12055, 2014.
Sawers, A., J. L. Allen, and L. H. Ting. Long-term training modifies the modular structure and organization of walking balance control. J. Neurophysiol. 114:3359–3373, 2015.
Shiavi, R., C. Frigo, and A. Pedotti. Electromyographic signals during gait: Criteria for envelope filtering and number of strides. Med. Biol. Eng. Comput. 36:171–178, 1998.
Sozzi, S., J.-L. Honeine, M.-C. Do, and M. Schieppati. Leg muscle activity during tandem stance and the control of body balance in the frontal plane. Clin. Neurophysiol. 124:1175–1186, 2013.
Ting, L. H., H. J. Chiel, R. D. Trumbower, J. L. Allen, J. L. McKay, M. E. Hackney, and T. M. Kesar. Neuromechanical principles underlying movement modularity and their implications for rehabilitation. Neuron 86:38–54, 2015.
Turcato, A., M. Godi, A. Giordano, M. Schieppati, and A. Nardone. The generation of centripetal force when walking in a circle: insight from the distribution of ground reaction forces recorded by plantar insoles. J. Neuroeng. Rehabil. 12:4, 2015.
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This research was supported by the Italian Ministry of Education, University and Research (Grant No. 2010R277FT) and the Italian Ministry of Health (Grant No. GR-2010-2312228).
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Associate Editor Thurmon E. Lockhart oversaw the review of this article.
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Chia Bejarano, N., Pedrocchi, A., Nardone, A. et al. Tuning of Muscle Synergies During Walking Along Rectilinear and Curvilinear Trajectories in Humans. Ann Biomed Eng 45, 1204–1218 (2017). https://doi.org/10.1007/s10439-017-1802-z
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DOI: https://doi.org/10.1007/s10439-017-1802-z