The role of supporting afferentation in the formation of muscle synergies patterns in locomotion

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Abstract

The features of the spatial-temporal structuring of intermuscular interaction during locomotion in conditions of full and partial unloading of body weight were studied. The extraction of muscle synergies was performed using the principal component analysis. It is established that the stability of muscle modules and stereotypical patterns of their temporary activation with varying degrees of afferentation are due to the implementation of motor synergy programs. It was revealed that only the presence, but not the power of the afferent flow from the receptor complex of the lower extremities makes a significant contribution to the formation of inter-extremity synergetic patterns and regulation of the degree of involvement of muscles in synergy. The formation of various time profiles in the structure of synergies is due to the redundancy of the organization of control structures, thanks to which reliable management of physiological functions is carried out. The implementation of synergy programs weakly depends on the magnitude and nature of proprioceptive and supportive afferentation. Only the presence, but not the power, of the afferent flow from the receptor complex of the lower extremities makes a significant contribution to the formation of interfacial synergetic patterns and the regulation of the degree of muscle involvement in synergy.

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S. A. Moiseev

Velikiye Luki State Academy of Physical Education and Sports

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Email: sergey_moiseev@vlgafc.ru
Russian Federation, Velikiye Luki

References

  1. Гурфинкель ВС, Левик ЮС, Казенников ОВ, Селионов ВА (1998) Существует ли генератор шагательных движений у человека? Физиол чел 24(3): 42–50. [Gurfinkel’ VS, Levik YUS, Kazennikov OV, Selionov VA (1998) Sushchestvuet li generator shagatel’nyh dvizhenij u cheloveka? Fiziol chel 24(3): 42–50. (In Russ)]
  2. Gorodnichev RM, Pivovarova EA, Pukhov A, Moiseev SA, Savokhin AA, Moshonkina TR, Shcherbakova NA, Kilimnik VA, Selionov VA, Kozlovskaya IB, Edzherton R., Gerasimenko YP (2012) Transcutaneous Electrical Stimulation of the Spinal Cord: A Noninvasive Tool for the Activation of Stepping Pattern Generators in Humans. Hum Physiol 38(2): 158–167. https://doi.org/10.1134/S0362119712020065
  3. Бернштейн НА (1966) Очерки по физиологии движений и физиологии активности. М.: Медицина. 349 c. [Bernshtejn NA (1966) Ocherki po fiziologii dvizhenij i fiziologii aktivnosti. M.: Medicina. 349 c. (In Russ)]
  4. Гельфанд ИМ, Гурфинкель ВС, Фомин СВ, Цетлин МЛ (1966) Модели структурно-функциональной организации некоторых биологических систем. М.: Наука 322 с. [Gel’fand IM, Gurfinkel’ VS, Fomin SV, Cetlin ML (1966) Modeli strukturno-funkcional’noj organizacii nekotoryh biologicheskih sistem. M.: Nauka 322 s. (In Russ)]
  5. Шенкман БС, Мирзоев ТМ, Козловская ИБ (2020) Тоническая активность и гравитационный контроль постуральной мышцы. Авиакосмическая и экологическая медицина 54(6): 58–72. [Shankman BS, Mirzoev TM, Kozlovskaya And B (2020) Tonic activity and gravitational control of the postural muscle. Aerospace and Environmental Medicine 54(6): 58–72. (In Russ)]. https://doi.org/10.21687/0233-528X-2020-54-6-58-72
  6. Козловская ИБ (2017) Гравитация и позно-тоническая двигательная система/ Авиакосм и эколог мед 51(3):5. [Kozlovskaya IB (2017) Gravitaciya i pozno-tonicheskaya dvigatel’naya sistema/ Aviakosm i ekolog med 51(3):5. (In Russ)] https://doi.org/10.21687/0233-528X-2017-51-3-5-21
  7. Cheung VC, d’Avella A, Tresch MC, Bizzi E (2005) Central and sensory contributions to the activation and organization of muscle synergies during natural motor behaviors. J Neurosci 25 (27): 6419–6434. https://doi.org/10.1523/JNEUROSCI.4904-04.2005
  8. Rybak IA, Dougherty KJ, Shevtsova NA (2015) Organization of the Mammalian Locomotor CPG: Review of Computational Model and Circuit Architectures Based on Genetically Identified Spinal Interneurons (1,2,3). eNeuro 2(5): ENEURO.0069–15.2015. https://doi.org/10.1523/ENEURO.0069-15.2015
  9. Yokoyama H, Kato T, Kaneko N, Kobayashi H, Hoshino M, Kokubun T, Nakazawa K. (2021) Basic locomotor muscle synergies used in land walking are finely tuned during underwater walking. Sci Rep 11(1): 18480. https://doi.org/10.1038/s41598-021-98022-8
  10. Holubarsch J, Helm M, Ringhof S, Gollhofer A, Freyler K, Ritzmann R (2019) Stumbling reactions in hypo and hyper gravity – muscle synergies are robust across different perturbations of human stance during parabolic flights. Sci Rep 9(1): 10490. https://doi.org/10.1038/s41598-019-47091-x
  11. Vernazza-Martin S, Martin N, Massion J (2000) Kinematic synergy adaptation to microgravity during forward trunk movement. J Neurophysiol 83(1): 453–464. https://doi.org/10.1152/jn.2000.83.1.453.PMID: 10634887
  12. Altenburger K, Bumke O, Foerster O (1937) Allgemeine neurologie. Handbuch der Neurologie. Verlag von Julius Springer. Berlin. S.747.
  13. Moiseev S, Pukhov A, Mikhailova E, Gorodnichev R (2022) Methodological and computational aspects of extracting extensive muscle synergies in moderate-intensity locomotions. J Evol Biochem Phys 58: 88–97. https://doi.org/10.1134/S0022093022010094
  14. Hagio S, Ishihara A, Terada M, Tanabe H, Kibushi B, Higashibata A, Yamada S, Furukawa S, Mukai C, Ishioka N, Kouzaki M (2022) Muscle synergies of multidirectional postural control in astronauts on Earth after a long-term stay in space. J Neurophysiol 127(5): 1230–1239. https://doi.org/10.1152/jn.00232.2021
  15. Kerkman JN, Zandvoort CS, Daffertshofer A, Dominici N (2022) Body Weight Control Is a Key Element of Motor Control for Toddlers’ Walking. Front Netw Physiol 2: 844607. https://doi.org/10.3389/fnetp.2022.844607
  16. Yokoyama H, Kato T, Kaneko N, Kobayashi H, Hoshino M, Kokubun T, Nakazawa K (2021) Basic locomotor muscle synergies used in land walking are finely tuned during underwater walking. Sci Rep 11(1): 18480. https://doi.org/10.1038/s41598-021-98022-8
  17. Rybak IA, Dougherty KJ, Shevtsova NA (2015) Organization of the Mammalian Locomotor CPG: Review of Computational Model and Circuit Architectures Based on Genetically Identified Spinal Interneurons (1,2,3). eNeuro 2(5): ENEURO.0069–15.2015. https://doi.org/10.1523/ENEURO.0069–15.2015
  18. Балабан ПМ, Воронцов ДД, Дьяконова ВЕ, Дьяконова ТЛ, Захаров ИС, Коршунова ТА, Орлов ОЮ, Павлова ГА, Панчин ЮВ, Сахаров ДА, Фаликман МВ (2013) Центральные генераторы паттерна. Журн высш нервн деяте им ИП Павлова 63(5): 520–541. [Balaban PM, Vorontsov D, Diakonova VE, Diakonova T L, Zakharov I S, Korshunova TA, Orlov O Yu, Pavlova GA, Panchin Yu V, Sakharov DA, Falikman MV (2013) Central pattern generators. J High Nerv Activ named IP Pavlov 63(5): 520–541. (In Russ)]. https://doi.org/10.7868/S0044467713050031
  19. Аршавский ЮИ, Делягина ТГ, Орловский ГН (2015) Центральные генераторы: механизм работы и их роль в управлении автоматизированными движениями. Журн высш нервн деяте им ИП Павлова 65(2): 156–187. [Arshavsky YI, Delyagina TK, Orlovsky GN (2015) Central generators: the mechanism of operation and their role in the management of automated movements. J High Nerv Activ named IP Pavlov 65(2):156–187. (In Russ)]. https://doi.org/10.7868/S0044467715020033
  20. Сентаготаи Я, Арбиб М (1976) Концептуальные модели нервной системы. – Москва. Мир. 198 с. [Sentagotai Ya, Arbib M (1976) Conceptual models of the nervous system. – Moscow. Mir. 198 p. (In Russ)].
  21. Томиловская ЕС, Мошонкина ТР, Городничев РМ, Шигуева ТА, Закирова АЗ, Пивоварова ЕА, Савохин АА, Селионов ВА, Семенов ЮС, Бревнов ВВ, Китов ВВ, Герасименко ЮП, Козловская ИБ (2013) Механическая стимуляция опорных зон стоп: неинвазивный способ активации генераторов шагательных движений у человека. Физиол чел 39(5): 34–41. [Tomilovskaya EC, Moshonkina TR, Gorodnichev RM, Shigueva TA, Zakirova AZ, Pivovarova EA, Savokhin AA, Selionov VA, Semenov JUS, Brevnov BB, Kitov BB, Gerasimenko YP, Kozlovskaya IB (2013) Mechanical stimulation of the support zones of the feet: a non-invasive method of activating generators of walking movements in humans. Hum Physiol 39(5): 34–41. (In Russ)]. https://doi.org/10.7868/S0131164613050159
  22. Gerasimenko Y, Edgerton R, Harkema V, Kozlovskaya I (2020) Gravity dependent mechanisms of sensorimotor regulation of posture and locomotion. Aerospace Environment Med 54: 27–42.
  23. Орловский ГН (1969) Спонтанная и вызванная локомоция таламической кошки. Биофизика 14(5): 1095–1102. [Orlovsky GN (1969) Spontaneous and induced locomotion of the thalamic cat. Biophysics 14(5): 1095–1102. (In Russ)]. https://doi.org/10.7868/S0044467715020033
  24. McCrea DA, Rybak IA (2008) Organization of mammalian locomotor rhythm and pattern generation. Brain Res Rev 57(1): 134–146. https://doi.org/10.1016/j.brainresrev.2007.08.006.
  25. Моисеев СА, Городничев РМ (2023) Особенности синергетического взаимодействия скелетных мышц нижних конечностей под воздействием электрической стимуляции спинного мозга. Физиол чел 49(1): 91–103. [Moiseev SA, Gorodnichev RM (2023) Features of synergetic interaction of skeletal muscles of the lower extremities under the influence of electrical stimulation of the spinal cord. Hum Physiol 49(1): 91–103. (In Russ)]. https://doi.org/10.31857/S0131164622100319.
  26. Городничев РМ, Пухов АМ, Моисеев СА, Иванов СМ, Маркевич ВВ, Богачева ИН, Гришин АА, Мошонкина ТР, Герасименко ЮП (2021) Регуляция фаз шагательного цикла при неинвазивной электрической стимуляции спинного мозга. Физиол чел 47(1): 73–83. [Gorodnichev RM, Pukhova M, Moiseev S A, Ivanov SM, Markevich V, Bogacheva YIN, Grishin A, Moshonkina T R, Gerasimenko YP (2021) Regulation of the phases of the walking cycle with noninvasive electrical stimulation of the spinal cord. Hum Physiol 47(1): 73–83. (In Russ)]. https://doi.org/10.31857/S0131164621010057
  27. Latash ML (2012) The bliss (not the problem) of motor abundance (not redundancy). Exp Brain Res. 217(1): 1–5. https://doi.org/doi: 10.1007/s00221-012-3000-4.
  28. Latash M (2016) Structured variability as a signature of biological processes. Voprosy Psikhologii, 2016(3): 120–126.
  29. Scholz JP, Schöner G (1999) The uncontrolled manifold concept: identifying control variables for a functional task. Exp Brain Res 126(3):289–306. https://doi.org/doi: 10.1007/s002210050738
  30. Латаш МЛ (2020) Физика живого движения и восприятия. Москва. Когито-Центр. 358 с. [Latash ML (2020) Physics of Living Motion and Perception. Moscow. Kogito-Center. 358 p. (In Russ)].

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2. Fig. 1. Device for vertical body weight signage (a), a sample of interference (b) and processed (c) electromyograms of the muscles of the lower extremities when walking. 1 – anterior tibial muscle, etc., 2 – calf medial muscle, etc., 3 – rectus femoris, etc., 4 – biceps femoris, etc., 5-8 the same muscles of the left lower limb, 9th goniogram.

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3. Fig. 2. Patterns of temporary activation of muscle synergies during walking under conditions of varying degrees of weight loss. On the abscissa axis – the progress of the step cycle, on the ordinate axis – ie. #1, 2, 3 – the number of the component (synergy). Thin lines are the average intra–individual profiles, bold lines are the average group profile. The degree of body weight signage: (a) – without signage, (b) – 25%, (c) – 50%, (d) – 100%, (e) – pushing the passive treadmill tape.

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4. Fig. 3. Weight coefficients of muscle synergies when walking in conditions of varying degrees of body weight loss. On the abscissa axis – the degree of signage, on the ordinate axis – the coefficients. #1, 2, 3 – the number of the component (synergy). * – Statistically significant differences at p<0.05 relative to walking without a sign (0%). The solid line shows the “synergy vectors". Skeletal muscles: (a) – anterior tibial muscle, (b) – calf medial muscle, (c) – rectus femoris, (d) – biceps femoris, (e), (f), (g), (h) – the same muscles of the left lower limbs.

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