Peculiarities of Afferent Innervation of Antagonist Muscles of the Bilateral Lower Legs During High-Speed Locomotor Movements

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Abstract

The article presents the specifics of intra-, intermuscular, and cross-manifestations of impulse activity of various groups of afferents (Ia, Ib, and II) of the antagonist muscles of the bilateral lower legs when performing high-speed locomotor movements. The study involved 9 male athletes specializing in short-distance running who performed a locomotor test – pushing a passive treadmill belt for 10 seconds at the fastest possible speed. Electromyograms of the antagonist muscles lower legs (m. tibialis anterior, m. gastrocnemius med.) were recorded during running, followed by its processing in the MatLab program and calculation of the impulse activity of primary and secondary afferents using mathematical model based on the prediction of the triggering of muscle spindles. It has been established that high-speed running is a cross intramuscular EMG pattern of tension of the antagonist muscles of the bilateral lower legs with a transition to their relaxation, which depends on the phase of movement. Such muscle innervation in the individual phases of a high-speed running step was manifested by effective intermuscular coordination of the flexor and extensor in the phases of stance and swing of the right leg, pronounced reciprocal relations of homonymous antagonistic muscles of the lower leg in the phases of swing of the right and stance of the left legs. Intramuscular proprioceptive afferentation of the antagonist muscles lower legs of high-speed movement is characterized by the manifestation of strong impulse activity of afferents Ib, moderate afferents II and weak Ia afferents of flexors and extensors of the of symmetrical legs. A phase-dependent modulation of the intermuscular afferentation of the primary and secondary fibers of the flexors and extensors of the bilateral lower legs in the phases of stance and swing of a high-speed running step is shown. The cross-interactions of afferent activity of homologous muscles of the bilateral lower legs in different phases of movement, characteristic of a high-speed running step, have been established. The identified features of intramuscular, intermuscular, and cross-limb afferent activity during running reflect their key role in regulating the inhibitory interneuron network of the spinal cord, which maintains targeted muscle contraction and modulates motor output parameters as a whole. The supposed reflex mechanisms of high-speed locomotor movements are discussed on the basis of well-known phenomena associated with the interaction of various afferent inputs to the spinal cord neuronal apparatus in the system of lower leg antagonist muscles.

About the authors

A. A. Chelnokov

Velikiye Luki State Academy of Physical Education and Sports

Email: and-chelnokov@yandex.ru
Velikiye Luki, Russia

M. G. Barkanov

Velikiye Luki State Academy of Physical Education and Sports

Velikiye Luki, Russia

D. A. Gladchenko

Velikiye Luki State Academy of Physical Education and Sports

Velikiye Luki, Russia

R. M. Gorodnichev

Velikiye Luki State Academy of Physical Education and Sports

Velikiye Luki, Russia

References

  1. Pearson KG (2004) Generating the walking gait: role of sensory feedback. Prog Brain Res 143: 123–129. https://doi.org/10.1016/S0079-6123(03)43012-4
  2. Cappellini G, Ivanenko YP, Poppele RE, Lacquaniti F (2006) Motor patterns in human walking and running. J Neurophysiol 95(6): 3426–3437. https://doi.org/10.1152/jn.00081.2006
  3. Rybak IA, Stecina K, Shevtsova NA, McCrea DA (2006) Modelling spinal circuitry involved in locomotor pattern generation: insights from the effects of afferent stimulation. J Physiol 577(Pt 2): 641–658. https://doi.org/10.1113/jphysiol.2006.118711
  4. Pierrot-Deseilligny E, Burke D (2012) The Circuitry of the Human Spinal Cord: Spinal and Corticospinal Mechanisms of Movement. United States: Cambridge Univer Press.
  5. 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
  6. Dubuc R, Cabelguen JM, Ryczko D (2023) Locomotor pattern generation and descending control: a historical perspective. J Neurophysiol 130(2): 401–416. https://doi.org/10.1152/jn.00204.2023
  7. Pleshchinskii IN, Alekseeva NL (1996) Spinal cord: afferent interactions. Hum Physiol 22(1): 123–130.
  8. Stachowski NJ, Dougherty KJ (2021) Spinal Inhibitory Interneurons: Gatekeepers of Sensorimotor Pathways. Int J Mol Sci 22(5): 2667. https://doi.org/10.3390/ijms22052667
  9. Gladchenko DA, Alekseeva IV, Chelnokov AA, Barkanov MG (2024) Modeling of Impulse Activity of Afferent Fibers of Antagonist Muscles during Transcutaneous Electrical Stimulation of the Spinal Cord During Walking. Hum Physiol 50: 25–34. https://doi.org/10.1134/S0362119723600091
  10. Capaday C, Stein RB (1987) Difference in the amplitude of the human soleus H reflex during walking and running. J Physiol 392: 513–522. https://doi.org/10.1113/jphysiol.1987.sp016794
  11. Simonsen EB, Dyhre-Poulsen P (1999) Amplitude of the human soleus H reflex during walking and running. J Physiol 515 (Pt 3): 929–939. https://doi.org/10.1111/j.1469-7793.1999.929ab.x
  12. Stephens MJ, Yang JF (1996) Short latency, non-reciprocal group I inhibition is reduced during the stance phase of walking in humans. Brain Res 743(1-2): 24–31. https://doi.org/10.1016/s0006-8993(96)00977-8
  13. Faist M, Hoefer C, Hodapp M, Dietz V, Berger W, Duysens J (2006) In humans Ib facilitation depends on locomotion while suppression of Ib inhibition requires loading. Brain Res 1076(1): 87–92. https://doi.org/10.1016/j.brainres.2005.12.069
  14. Grey MJ, Nielsen JB, Mazzaro N, Sinkjaer T (2007) Positive force feedback in human walking. J Physiol 581(Pt 1): 99–105. https://doi.org/10.1113/jphysiol.2007.130088
  15. Duysens J, Tax AA, Trippel M, Dietz V (1992) Phase-dependent reversal of reflexly induced movements during human gait. Exp Brain Res 90(2): 404–414. https://doi.org/10.1007/BF00227255
  16. Duysens J, Tax AA, Nawijn S, Berger W, Prokop T, Altenmüller E (1995) Gating of sensation and evoked potentials following foot stimulation during human gait. Exp Brain 105(3): 423–431. https://doi.org/10.1007/BF00233042
  17. Selverston AI (2010) Invertebrate central pattern generator circuits. Philos Trans R Soc Lond B Biol Sci 365(1551): 2329–2345. https://doi.org/10.1098/rstb.2009.0270
  18. Grillner S, El Manira A (2020) Current Principles of Motor Control, with Special Reference to Vertebrate Locomotion. Physiol Rev 100(1): 271–320. https://doi.org/10.1152/physrev.00015.2019
  19. Stubbs PW, Mrachacz-Kersting N (2009) Short-latency crossed inhibitory responses in the human soleus muscle. J Neurophysiol 102(6): 3596–3605. https://doi.org/10.1152/jn.00667.2009
  20. Stubbs PW, Nielsen JF, Sinkjær T, Mrachacz-Kersting N (2011) Phase modulation of the short-latency crossed spinal response in the human soleus muscle. J Neurophysiol 105(2): 503–511. https://doi.org/10.1152/jn.00786.2010
  21. Stevenson AJ, Geertsen SS, Andersen JB, Sinkjær T, Nielsen JB, Mrachacz-Kersting N (2013) Interlimb communication to the knee flexors during walking in humans. J Physiol 591(19): 4921–4935. https://doi.org/10.1113/jphysiol.2013.257949
  22. Hanna-Boutros B, Sangari S, Karasu A, Giboin LS, Marchand-Pauvert V (2014) Task-related modulation of crossed spinal inhibition between human lower limbs. J Neurophysiol 111(9): 1865–1876. https://doi.org/10.1152/jn.00838.2013
  23. Suzuki S, Nakajima T, Futatsubashi G, Mezzarane RA, Ohtsuka H, Ohki Y, Komiyama T (2016) Phase-dependent reversal of the crossed conditioning effect on the soleus Hoffmann reflex from cutaneous afferents during walking in humans. Exp Brain Res 234(2): 617–626. https://doi.org/10.1007/s00221-015-4463-x
  24. Gervasio S, Voigt M, Kersting UG, Farina D, Sinkjær T, Mrachacz-Kersting N (2017) Sensory Feedback in Interlimb Coordination: Contralateral Afferent Contribution to the Short-Latency Crossed Response during Human Walking. PLoS One 12(1): e0168557. https://doi.org/10.1371/journal.pone.0168557
  25. Barkanov MG, Gorodnichev RM (2022) Peculiarities of Induced Muscle Responses and Kinematic Parameters of High-Speed Locomotor Movements under Percutaneous Electrical Stimulation of Different Spinal Cord Areas. Hum Physiol 48: 526–534. https://doi.org/10.1134/S036211972204003X
  26. Voigt M, Bojsen-Møller F, Simonsen EB, Dyhre-Poulsen P (1995) The influence of tendon Youngs modulus, dimensions and instantaneous moment arms on the efficiency of human movement. J Biomech 28(3): 281–291. https://doi.org/10.1016/0021-9290(94)00071-b
  27. Voigt M, Simonsen EB, Dyhre-Poulsen P, Klausen K (1995) Mechanical and muscular factors influencing the performance in maximal vertical jumping after different prestretch loads. J Biomech 28(3): 293–307. https://doi.org/10.1016/0021-9290(94)00062-9
  28. Voigt M, Dyhre-Poulsen P, Simonsen EB (1998) Modulation of short latency stretch reflexes during human hopping. Acta Physiol Scand 163(2): 181–194. https://doi.org/10.1046/j.1365-201X.1998.00351.x
  29. Prochazka A, Gorassini M (1998) Ensemble firing of muscle afferents recorded during normal locomotion in cats. J Physiol 507 (Pt 1): 293–304. https://doi.org/10.1111/j.1469-7793.1998.293bu.x
  30. Mileusnic MP, Loeb GE (2009) Force estimation from ensembles of Golgi tendon organs. J Neural Eng 6(3): 036001. https://doi.org/10.1088/1741-2560/6/3/036001
  31. Enoka RM (2015) Neuromechanics of Human Movement. Champaign, IL, United States.
  32. Labrecque C, Belanger M (1994) The Effects of Low Intensity Cutaneous Stimulation on the H-Reflex Modulation during Static and Dynamic Cycling Movements. Dept Kinanthropol Soc Neurosci Abstr 20(715): 7.
  33. Витензон АС (1998) Закономерности нормальной и патологической ходьбы человека. М. ООО Зеркало-М. [Vitenzon AS (1998) Patterns of normal and pathological human walking. M. OOO Zerkalo-M. (In Russ)].
  34. Mummidisetty CK, Smith AC, Knikou M (2013) Modulation of reciprocal and presynaptic inhibition during robotic-assisted stepping in humans. Clin Neurophysiol 124(3): 557–564. https://doi.org/10.1016/j.clinph.2012.09.007
  35. Kido A, Tanaka N, Stein RB (2004) Spinal reciprocal inhibition in human locomotion. J Appl Physiol 96(5): 1969–1977. https://doi.org/10.1152/japplphysiol.01060.2003
  36. Stubbs PW, Nielsen JF, Sinkjaer T, Mrachacz-Kersting N (2011) Crossed spinal soleus muscle communication demonstrated by H-reflex conditioning. Muscle Nerve 43(6): 845–850. https://doi.org/10.1002/mus.21964
  37. Mrachacz-Kersting N, Geertsen SS, Stevenson AJ, Nielsen JB (2017) Convergence of ipsi- and contralateral muscle afferents on common interneurons mediating reciprocal inhibition of ankle plantarflexors in humans. Exp Brain Res 235(5): 1555–1564. https://doi.org/10.1007/s00221-016-4871-6
  38. Gervasio S, Farina D, Sinkjær T, Mrachacz-Kersting N (2013) Crossed reflex reversal during human locomotion. J Neurophysiol 109(9): 2335–2344. https://doi.org/10.1152/jn.01086.2012
  39. Mrachacz-Kersting N, Gervasio S, Marchand-Pauvert V (2018) Evidence for a Supraspinal Contribution to the Human Crossed Reflex Response During Human Walking. Front Hum Neurosci 12: 260. https://doi.org/10.3389/fnhum.2018.00260
  40. Hiraoka K (2021) Phase-Dependent Crossed Inhibition Mediating Coordination of Anti-phase Bilateral Rhythmic Movement: A Mini Review. Front Hum Neurosci 15: 668442. https://doi.org/10.3389/fnhum.2021.668442

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