This study addressed the synergistic effects apparent at the cortical and muscular levels during locomotor activity performed under conditions in which the lower limbs are supported horizontally. The spatiotemporal structure of synergies was studied using data matrix factorization methods. Control of movement structure is shown to be realized primarily through three muscle synergies. Synchronization of the activity of the motor, associative, visual, and sensorimotor areas of the cortex on both sides is due to the specific characteristics of locomotion in conditions of gravitational unloading and the associated features of receptor signaling. The components identified, evidencing synchronization of different areas of the cortex on the right and left sides, may reflect control processes associated with the control of alternating activation of the flexor and extensor muscles of the contralateral limb in the process of locomotion. Data on the spatiotemporal structuring of cortical activity indicate separate control of muscle synergies via synchronization of cortical commands and the temporal organization of muscle synergies in the frequency range 0.30–8.00 Hz. These patterns may reflect operation of a rhythm-generating mechanism involved in controlling cyclic activity.
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Amundsen Huffmaster, S. L., Van Acker, G. M., 3rd, Luchies, C. W., and Cheney, P. D., “Muscle synergies obtained from comprehensive mapping of the primary motor cortex forelimb representation using high-frequency, long-duration ICMS,” J. Neurophysiol., 118, No. 1, 455–470 (2017).
Bernshtein, N. A., The Physiology of Movement and Activity, Nauka, Moscow (1990).
Bourguignon, M., Jousmäki, V., Dalal, S. S., et al., “Coupling between human brain activity and body movements: Insights from non-invasive electromagnetic recordings,” NeuroImage, 203, 116177 (2019).
Bradford, J. C., Lukos, J. R., and Ferris, D. P., “Electrocortical activity distinguishes between uphill and level walking in humans,” J. Neurophysiol., 115, No. 2, 958–966 (2016).
Churchland, M. M., Cunningham, J. P., Kaufman, M. T., et al., “Neural population dynamics during reaching,” Nature, 487, No. 7405, 51–6 (2012).
Danna-Dos-Santos, A., Degani, A. M., and Boonstra, T. W., “The influence of visual information on multi-muscle control during quiet stance: a spectral analysis approach,” Exp. Brain Res., 233, No. 2, 657–669 (2015).
De Marchis, C., Severini, G., Castronovo, A. M., et al., “Intermuscular coherence contributions in synergistic muscles during pedaling,” Exp. Brain Res., 233, No. 6, 1907–19 (2015).
De Vries, I. E., Daffertshofer, A., Stegeman, D. F., and Boonstra, T. W., “Functional connectivity in the neuromuscular system underlying bimanual coordination,” J. Neurophysiol., 116, No. 6, 2576–2585 (2016).
Frère, J., “Spectral properties of multiple myoelectric signals: New insights into the neural origin of muscle synergies,” Neuroscience, 355, 22–35 (2017).
Gel’fand, I. and Tsetlin, M., “Some ways of controlling complex systems,” UMN, 17, No. 1, 3–25 (1962).
Gerasimenko, Y. P., Lu, D. C., Modaber, M., et al., “Noninvasive reactivation of motor descending control after paralysis,” J. Neurotrauma, 32, No. 24, 1968–80 (2015).
Gorodnichev, R. M., Pivovarova, E. A., Puhov, A., et al., “Transcutaneous electrical stimulation of the spinal cord: a noninvasive tool for the activation of stepping pattern generators in humans,” Hum. Physiol., 38, No. 2, 158–167 (2012).
Grigor’ev, A. I., Kozlovskaya, I. B., and Shenkman, B. S., “The role of supporting afferentation in the organization of the tonic muscular system,” Ros. Fiziol. Zh., 90, No. 5, 507–521 (2004).
Gurfinkel’, V. S., Levik, Yu. S., Kazennikov, O. V., and Selionov, V. A., “Do humans have a stepping generator?” Fiziol. Cheloveka, 24, No. 3, 42–50 (1998).
Hall, T. M., de Carvalho, F., and Jackson, A., “A common structure underlies low-frequency cortical dynamics in movement, sleep, and sedation,” Neuron, 83, No. 5, 1185–99 (2014).
Hogan, N. and Sternad, D., “On rhythmic and discrete movements: reflections, definitions and implications for motor control,” Exp. Brain Res., 181, No. 1, 13–30 (2007).
Hug, F., Turpin, N. A., Couturier, A., and Dorel, S., “Consistency of muscle synergies during pedaling across different mechanical constraints,” J. Neurophysiol., 106, No. 1, 91–103 (2011).
Ivanenko, Y. P., Poppele, R. E., and Lacquaniti, F., “Motor control programs and walking,” Neuroscientist, 12, No. 4, 339–48 (2006).
Kulaichev, A. P., “The informativeness of coherence analysis in EEG studies,” Zh. Vyssh. Nerv. Deyat., 59, No. 6, 757–767 (2009).
Kurganskaya, M. E., Bobrov, P. D., Frolov, A. A., and Semenova, E. I., “Corticomuscular interaction during real and imaginary movements of the hand,” Zh. Vyssh. Nerv. Deyat., 70, No. 6, 738–751 (2020).
Latash, M., “Motor synergies and the equilibrium-point hypothesis,” Motor Control, 14, No. 3, 294–322 (2010).
Mallat, S. G., “A theory for multiresolution signal decomposition: the wavelet representation,” IEEE Trans. Pattern Analysis Machine Intell., 11, No. 7, 674–693 (1989).
Mehryar, P., Shourijeh, M., Rezaeian, T., et al., “Differences in muscle synergies between healthy subjects and transfemoral amputees during normal transient-state walking speed,” Gait Posture, 76, 98–103 (2020).
Mileti, I., Serra, A., Wolf, N., et al., “Muscle activation patterns are more constrained and regular in treadmill than in overground human locomotion,” Front. Bioeng. Biotechnol., 8, 581619 (2020).
Mima, T. and Hallett, M., “Corticomuscular coherence: a review,” J. Clin. Neurophysiol., 16, No. 6, 501–511 (1999).
Moiseev, S. A., “Spatiotemporal patterns of intermuscular interaction during locomotion induced by transcutaneous electrical stimulation of the spinal cord,” Zh. Evolyuts. Biokhim. Fiziol., 58, No. 6, 94–102 (2022).
Moiseev, S., Pukhov, A., Mikhailova, E., and Gorodnichev, R., “Methodological and computational aspects of extracting extensive muscle synergies in moderate-intensity locomotions,” J. Evol. Biochem. Phys., 58, 88–97 (2022).
Nakanishi, Y., Yanagisawa, T., Shin, D., et al., “Decoding fingertip trajectory from electrocorticographic signals in humans,” Neurosci. Res., 85, 20–7 (2014).
Nakanishi, Y., Yanagisawa, T., Shin, D., et al., “Prediction of three-dimensional arm trajectories based on ECoG signals recorded from human sensorimotor cortex,” PLoS One, 8, No. 8, e72085 (2013).
Overduin, S. A., d’Avella, A., Roh, J., et al., “Representation of muscle synergies in the primate brain,” J. Neurosci., 35, No. 37, 12615–24 (2015).
Ozdemir, R. A., Contreras-Vidal, J. L., and Paloski, W. H., “Cortical control of upright stance in elderly,” Mech. Aging Dev., 169, 19–31 (2018).
Pei, D., Olikkal, P., Adali, T., and Vinjamuri, R., “Reconstructing synergy-based hand grasp kinematics from electroencephalographic signals,” Sensors (Basel), 22, No. 14, 5349 (2022).
Reyes, A., Laine, C. M., Kutch, J. J., and Valero-Cuevas, F. J., “Beta band corticomuscular drive reflects muscle coordination strategies,” Front. Comput. Neurosci., 11, 17 (2017).
Roeder, L., Boonstra, T. W., Smith, S. S., and Kerr, G. K., “Dynamics of corticospinal motor control during overground and treadmill walking in humans,” J. Neurophysiol., 120, No. 3, 1017–1031 (2018).
Saito, H., Yokoyama H, Sasaki, A., et al., “Flexible recruitments of fundamental muscle synergies in the trunk and lower limbs for highly variable movements and postures,” Sensors (Basel), 21, No. 18, 6186 (2021).
Santuz, A., Ekizos, A., Janshen, L., et al., “Modular control of human movement during running: An open access data set,” Front. Physiol., 9, 1509 (2018).
Shin, D., Watanabe, H., Kambara, H., et al., “Prediction of muscle activities from electrocorticograms in primary motor cortex of primates,” PLoS One, 7, No. 10, e47992 (2012).
Weersink, J. B., de Jong, B. M., Halliday, D. M., and Maurits, N. M., “Intermuscular coherence analysis in older adults reveals that gait-related arm swing drives lower limb muscles via subcortical and cortical pathways,” J. Physiol., 599, No. 8, 2283–2298 (2021).
Yang, Y., Dewald, J., Van der Helm, F., and Schouten, A. C., “Unveiling neural coupling within the sensorimotor system: directionality and nonlinearity,” Eur. J. Neurosci., 48, No. 7, 2407–2415 (2018).
Yarossi, M., Brooks, D. H., Erdoğmuş, D., and Tunik, E., “Similarity of hand muscle synergies elicited by transcranial magnetic stimulation and those found during voluntary movement,” J. Neurophysiol., 128, No. 4, 994–1010 (2022).
Yokoyama, H., Kaneko, N., Ogawa, T., et al., “Cortical correlates of locomotor muscle synergy activation in humans: An electroencephalographic decoding study,” iScience, 15, 623–639 (2019).
Yokoyama, H., Kato, T., Kaneko, N., et al., “Basic locomotor muscle synergies used in land walking are finely tuned during underwater walking,” Sci. Rep., 11, No. 1, 18480 (2021).
Yoshimura, N., Tsuda, H., Kawase, T., et al., “Decoding finger movement in humans using synergy of EEG cortical current signals,” Sci. Rep., 7, No. 1, 11382 (2017).
Zandvoort, C. S., Van Dieën, J. H., Dominici, N., and Daffertshofer, A., “The human sensorimotor cortex fosters muscle synergies through cortico-synergy coherence,” NeuroImage, 199, 30–37 (2019).
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Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 73, No. 5, pp. 666–679, September–October, 2023.
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Moiseev, S.A., Gorodnichev, R.M. Spatiotemporal Patterns of Corticomuscular Interactions in Locomotion. Neurosci Behav Physi 54, 122–131 (2024). https://doi.org/10.1007/s11055-024-01574-1
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DOI: https://doi.org/10.1007/s11055-024-01574-1