Functional Activity of Reciprocal Inhibition of α-Motor Neurons of Antagonistic Muscles in Different Types of Muscle Contractions of Submaximal and Maximal Force

Abstract

INTRODUCTION: Currently, the results of investigation of different types of spinal inhibition in isometric voluntary contraction of muscles have been published. There are separate reports devoted to the role of recurrent and presynaptic inhibition in the regulation of isometric and anisometric voluntary contractions of submaximal and maximal strength.

AIM: To evaluate the effect of the type and strength of muscle contraction with and without performing Jendrassik maneuver on the manifestation of reciprocal inhibition of α-motor neurons of antagonistic muscles of the lower leg.

MATERIALS AND METHODS: The study involved 8 healthy men aged 20–22 years. Reciprocal inhibition was evaluated by suppression of the amplitude of testing H-reflex of m. soleus in conditioning stimulation of n. peroneus profundus, and of testing stimulation of n. tibialis with 3 msec interval between stimuli. Reciprocal inhibition was recorded in concentric, eccentric and isometric contractions with 50% and 100% of maximal voluntary contraction (MVC) with and without Jendrassic maneuver.

RESULTS: In performing concentric, eccentric and isometric contractions of lower leg muscles with increase in strength from 50% to 100% of MVC, the activity of reciprocal inhibition decreased. Reciprocal inhibition was most evident in concentric contraction with 50% of MVC strength, less evident in eccentric contraction and was lowest in isometric contraction. With the maximal strength, reciprocal inhibition was most expressed in isometric contraction, less expressed in concentric contraction and was weakest in eccentric contraction. With Jendrassik maneuver, reduction of reciprocal inhibition was more expressed in different types of MVCs in comparison with parameters obtained with 50% of MVC. Using Jendrassic maneuver with 50% and 100% of MVC effort, strongest reciprocal inhibition was recorded in isometric contraction, weaker inhibition in concentric contraction and weakest in eccentric contraction. The effect of Jendrassik maneuver was manifested by weakening of reciprocal inhibition in concentric and eccentric contraction of submaximal force, and by its enhancement in isometric contraction.

CONCLUSION: Variability of manifestation of reciprocal inhibition of α-motor neurons of antagonistic muscles of lower leg in different types of muscle contractions of submaximal and maximal strength is associated with the fact that the pool of segmental motor neurons of m. soleus is controlled not only by a wide spectrum of excitatory cortico- and reticulospinal influences, but also by other kinds of inhibition, thus providing coordinated motor actions.

Keywords

reciprocal inhibition / H-reflex / spinal cord / motor neurons / maximal voluntary contraction / concentric contraction / eccentric contraction / isometric contraction / Jendrassik maneuver

References

[1] Côté MP, Murray LM, Knikou M. Spinal Control of Locomotion: Individual Neurons, Their Circuits and Functions. Front Physiol. 2018;25(9):784. doi: 10.3389/fphys.2018.00784

[2] Côté M.P., Murray L.M., Knikou M. Spinal Control of Locomotion: Individual Neurons, Their Circuits and Functions // Frontiers in Physiology. 2018. Vol. 25, No. 9. P. 784. doi: 10.3389/fphys.2018.00784

[3] Chelnokov AA, Roshchina LV, Gladchenko DA, et al. The Effect of Transcutaneous Electrical Spinal Cord Stimulation on the Functional Activity of Spinal Inhibition in the System of Synergistic Muscles of the Lower Leg in Humans. Human Physiology. 2022;48(2):121–33. (In Russ). doi: 10.1134/s0362119722020037

[4] Chelnokov A.A., Roshchina L.V., Gladchenko D.A., et al. The Effect of Transcutaneous Electrical Spinal Cord Stimulation on the Functional Activity of Spinal Inhibition in the System of Synergistic Muscles of the Lower Leg in Humans // Human Physiology. 2022. Vol. 48, No. 2. P. 121–133. doi: 10.1134/s0362119722020037

[5] Sherrington CS. The Integrative Action of the Nervous System. New Haven, CT: Yale University Press; 1906.

[6] Sherrington C.S. The Integrative Action of the Nervous System. New Haven, CT: Yale University Press; 1906.

[7] Pierrot–Deseilligny E, Burke D. The Circuitry of the Human Spinal Cord: Spinal and Corticospinal Mechanisms of Movement. United Kingdom: Cambridge University Press; 2012.

[8] Pierrot–Deseilligny E., Burke D. The Circuitry of the Human Spinal Cord: Spinal and Corticospinal Mechanisms of Movement. United Kingdom: Cambridge University Press; 2012.

[9] Jankowska E, Padel Y, Tanaka R. Disynaptic inhibition of spinal motoneurones from the motor cortex in the monkey. J Physiol. 1976; 258(2):467–87. doi: 10.1113/jphysiol.1976.sp011431

[10] Jankowska E., Padel Y., Tanaka R. Disynaptic inhibition of spinal motoneurones from the motor cortex in the monkey // The Journal of Physiology. 1976. Vol. 258, No. 2. P. 467–487. doi: 10.1113/jphysiol.1976.sp011431

[11] Nielsen J, Petersen N, Deuschl G, et al. Task-related changes in the effect of magnetic brain stimulation on spinal neurones in man. J Physiol. 1993;471(1):223–43. doi: 10.1113/jphysiol.1993.sp019899

[12] Nielsen J., Petersen N., Deuschl G., et al. Task-related changes in the effect of magnetic brain stimulation on spinal neurones in man // The Journal of Physiology. 1993. Vol. 471, No. 1. P. 223–243. doi: 10.1113/jphysiol.1993.sp019899

[13] Crone C, Nielsen J. Spinal mechanisms in man contributing to reciprocal inhibition during voluntary dorsiflexion of the foot. J Physiol. 1989;416(1):255–72. doi: 10.1113/jphysiol.1989.sp017759

[14] Crone C., Nielsen J. Spinal mechanisms in man contributing to reciprocal inhibition during voluntary dorsiflexion of the foot // The Journal of Physiology. 1989. Vol. 416, No. 1. P. 255–272. doi: 10.1113/jphysiol.1989.sp017759

[15] Crone C, Nielsen J. Central control of disynaptic reciprocal inhibition in humans. Acta Physiol Scand. 1994;152(4):351–63. doi: 10.1111/j.1748-1716.1994.tb09817.x

[16] Crone C., Nielsen J. Central control of disynaptic reciprocal inhibition in humans // Acta Physiologica Scandinavica. 1994. Vol. 152, No. 4. P. 351–363. doi: 10.1111/j.1748-1716.1994.tb09817.x

[17] Dragert K, Zehr EP. Differential modulation of reciprocal inhibition in ankle muscles during rhythmic arm cycling. Neurosci Lett. 2013;534:269–73. doi: 10.1016/j.neulet.2012.11.038

[18] Dragert K., Zehr E.P. Differential modulation of reciprocal inhibition in ankle muscles during rhythmic arm cycling // Neuroscience Letters. 2013. Vol. 534. P. 269–273. doi: 10.1016/j.neulet.2012.11.038

[19] Yavuz US, Negro F, Diedrichs R, et al. Reciprocal inhibition between motor neurons of the tibialis anterior and triceps surae in humans. J Neurophysiol. 2018;119(5):1699–706. doi: 10.1152/jn.00424.2017

[20] Yavuz U.S., Negro F., Diedrichs R., et al. Reciprocal inhibition between motor neurons of the tibialis anterior and triceps surae in humans // Journal of Neurophysiology. 2018. Vol. 119, No. 5. P. 1699–1706. doi: 10.1152/jn.00424.2017

[21] Mummidisetty CK, Smith AC, Knikou M. Modulation of reciprocal and presynaptic inhibition during robotic-assisted stepping in humans. Clin Neurophysiol. 2013;124(3):557–64. doi: 10.1016/j.clinph.2012.09.007

[22] Mummidisetty C.K., Smith A.C., Knikou M. Modulation of reciprocal and presynaptic inhibition during robotic-assisted stepping in humans // Clinical Neurophysiology. 2013. Vol. 124, No. 3. P. 557–564. doi: 10.1016/j.clinph.2012.09.007

[23] Jessop T, De Paola A, Casaletto L, et al. Short-term plasticity of human spinal inhibitory circuits after isometric and isotonic ankle training. Eur J Appl Physiol. 2013;113(2):273–84. doi: 10.1007/s00421-012-2438-1

[24] Jessop T., De Paola A., Casaletto L., et al. Short-term plasticity of human spinal inhibitory circuits after isometric and isotonic ankle training // European Journal of Applied Physiology. 2013. Vol. 113, No. 2. P. 273–284. doi: 10.1007/s00421-012-2438-1

[25] Hirabayashi R, Kojima S, Edama M, et al. Activation of the Supplementary Motor Areas Enhances Spinal Reciprocal Inhibition in Healthy Individuals. Brain Sci. 2020;10(9):587. doi: 10.3390/brainsci10090587

[26] Hirabayashi R., Kojima S., Edama M., et al. Activation of the Supplementary Motor Areas Enhances Spinal Reciprocal Inhibition in Healthy Individuals // Brain Sciences. 2020. Vol. 10, No. 9. P. 587. doi: 10.3390/brainsci10090587

[27] Enoka RM. Eccentric contractions require unique activation strategies by the nervous system. J Appl Physiol. 1996;81(6):2339–46. doi: 10.1152/jappl.1996.81.6.2339

[28] Enoka R.M. Eccentric contractions require unique activation strategies by the nervous system // Journal of Applied Physiology. 1996. Vol. 81, No. 6. Р. 2339–2346. doi: 10.1152/jappl.1996.81.6.2339

[29] Duchateau J, Enoka RM. Neural control of shortening and lengthening contractions: influence of task constraints. J Physiol. 2008;586(24):5853–64. doi: 10.1113/jphysiol.2008.160747

[30] Duchateau J., Enoka R.M. Neural control of shortening and lengthening contractions: influence of task constraints // The Journal of Physiology. 2008. Vol. 586, No. 24. Р. 5853–5864. doi: 10.1113/jphysiol.2008.160747

[31] Duchateau J, Enoka RM. Neural control of lengthening contractions. J Exp Biol. 2016;219(Pt 2):197–204. doi: 10.1242/jeb.123158

[32] Duchateau J., Enoka R.M. Neural control of lengthening contractions // The Journal of Experimental Biology. 2016. Vol. 219, Pt. 2. Р. 197–204. doi: 10.1242/jeb.123158

[33] Duclay J, Martin A. Evoked H-reflex and V-wave responses during maximal isometric, concentric, and eccentric muscle contraction. J Neurophysiol. 2005;94(5):3555–62. doi: 10.1152/jn.00348.2005

[34] Duclay J., Martin A. Evoked H-reflex and V-wave responses during maximal isometric, concentric, and eccentric muscle contraction // Journal of Neurophysiology. 2005. Vol. 94, No. 5. Р. 3555–3562. doi: 10.1152/jn.00348.2005

[35] Duclay J, Pasquet B, Martin A, et al. Specific modulation of corticospinal and spinal excitabilities during maximal voluntary isometric, shortening and lengthening contractions in synergist muscles. J Physiol. 2011;589(11): 2901–16. doi: 10.1113/jphysiol.2011.207472

[36] Duclay J., Pasquet B., Martin A., et al. Specific modulation of corticospinal and spinal excitabilities during maximal voluntary isometric, shortening and lengthening contractions in synergist muscles // The Journal of Physiology. 2011. Vol. 589, No. 11. Р. 2901–2916. doi: 10.1113/jphysiol.2011.207472

[37] Duclay J, Pasquet B, Martin A, et al. Specific modulation of spinal and cortical excitabilities during lengthening and shortening submaximal and maximal contractions in plantar flexor muscles. J Appl Physiol. 2014;117(12):1440–50. doi: 10.1152/japplphysiol.00489.2014

[38] Duclay J., Pasquet B., Martin A., et al. Specific modulation of spinal and cortical excitabilities during lengthening and shortening submaximal and maximal contractions in plantar flexor muscles // Journal of Applied Physiology. 2014. Vol. 117, No. 12. Р. 1440–1450. doi: 10.1152/japplphysiol.00489.2014

[39] Nielsen J, Kagamihara Y. The regulation of disynaptic reciprocal Ia inhibition during co-contraction of antagonistic muscles in man. J Physiol. 1992;456:373–91. doi: 10.1113/jphysiol.1992.sp019341

[40] Nielsen J., Kagamihara Y. The regulation of disynaptic reciprocal Ia inhibition during co-contraction of antagonistic muscles in man // The Journal of Physiology. 1992. Vol. 456. Р. 373–391. doi: 10.1113/jphysiol.1992.sp019341

[41] Chelnokov AA, Gladchenko DA, Fedorov SA, et al. Age-related features of spinal inhibition of skeletal muscles in males in the regulation of voluntary movements. Human Physiology. 2017;43(1):28–36. (In Russ). doi: 10.7868/s0131164616060060

[42] Челноков А.А., Гладченко Д.А., Федоров С.А., и др. Возрастные особенности спинального торможения скелетных мышц у лиц мужского пола в регуляции произвольных движений // Физиология человека. 2017. Т. 43, № 1. С. 35–44. doi: 10.7868/s0131164616060060

[43] Matsuya R, Ushiyama J, Ushiba J. Inhibitory interneuron circuits at cortical and spinal levels are associated with individual differences in corticomuscular coherence during isometric voluntary contraction. Sci Rep. 2017;7:е44417. doi: 10.1038/srep44417

[44] Matsuya R., Ushiyama J., Ushiba J. Inhibitory interneuron circuits at cortical and spinal levels are associated with individual differences in corticomuscular coherence during isometric voluntary contraction // Scientific Reports. 2017. Vol. 7. P. е44417. doi: 10.1038/srep44417

[45] Hirabayashi R, Edama M, Kojima S, et al. Effects of Reciprocal Ia Inhibition on Contraction Intensity of Co-contraction. Front Hum Neurosci. 2019;12:е527. doi: 10.3389/fnhum.2018.00527

[46] Hirabayashi R., Edama M., Kojima S., et al. Effects of Reciprocal Ia Inhibition on Contraction Intensity of Co-contraction // Frontiers in Human Neuroscience. 2019. Vol. 12. P. е527. doi: 10.3389/fnhum.2018.00527

[47] Barrue–Belou S., Marque P., Duclay J. Recurrent inhibition is higher in eccentric compared to isometric and concentric maximal voluntary contractions. Acta Physiol. 2018;223(4):e13064. doi: 10.1111/apha.13064

[48] Barrué–Belou S., Marque P., Duclay J. Recurrent inhibition is higher in eccentric compared to isometric and concentric maximal voluntary contractions // Acta Physiologica. 2018. Vol. 223, No. 4. P. e13064. doi: 10.1111/apha.13064

[49] Bogdanov SM, Gladchenko DA, Roshchina LV, et al. Effect of supraspinal influences on the manifestation of presynaptic inhibition Ia afferents in different types of muscle contraction in humans. RUDN Journal of Medicine. 2020;24(4):338–44. (In Russ). doi: 10.22363/2313-0245-2020-24-4-338-344

[50] Богданов С.М., Гладченко Д.А., Рощина Л.В., и др. Эффект супраспинальных влияний на проявление пресинаптического торможения Ia афферентов при разных типах мышечного сокращения у человека // Вестник Российского университета дружбы народов. Серия: Медицина. 2020. Т. 24, № 4. С. 338–344. doi: 10.22363/2313-0245-2020-24-4-338-344

[51] Schieppati M. The Hoffmann reflex: a means of assessing spinal reflex excitability and its descending control in man. Prog Neurobiol. 1987;28(4):345–76. doi: 10.1016/0301-0082(87)90007-4

[52] Schieppati M. The Hoffmann reflex: a means of assessing spinal reflex excitability and its descending control in man // Progress in Neurobiology. 1987. Vol. 28, No. 4. Р. 345–376. doi: 10.1016/0301-0082(87)90007-4

[53] Chelnokov AA Gorodnichev RM. Age-Related Features of the Formation of Spinal Inhibition of Skeletal Muscles in Males. Human Physiology. 2015;41(6):86–94. (In Russ). doi: 10.7868/s0131164615060028

[54] Челноков А.А. Городничев Р.М. Возрастные особенности формирования спинального торможения скелетных мышц у лиц мужского пола // Физиология человека. 2015. Т. 41, № 6. С. 86–94. doi: 10.7868/s0131164615060028

[55] Delwaide PJ, Toulouse P. Jendrassik maneuver vs controlled contractions conditioning the excitability of soleus monosynaptic reflexes. Arch Phys Med Rehabil. 1980;61(11):505–10.

[56] Delwaide P.J., Toulouse P. Jendrassik maneuver vs controlled contractions conditioning the excitability of soleus monosynaptic reflexes // Archives of Physical Medicine and Rehabilitation. 1980. Vol. 61, No. 11. P. 505–510.

[57] Gregory JE, Wood SA, Proske U. An investigation into mechanisms of reflex reinforcement by the Jendrassik manoeuvre. Exp Brain Res. 2001;138(3):366–74. doi: 10.1007/s002210100707

[58] Gregory J.E., Wood S.A., Proske U. An investigation into mechanisms of reflex reinforcement by the Jendrassik manoeuvre // Experimental Brain Research. 2001. Vol. 138, No. 3. Р. 366–374. doi: 10.1007/s002210100707

[59] Bikmullina RKh, Rozental' AN, Pleshchinskii IN. Inhibitory systems of the spinal cord in the control of interactions of functionally coupled muscles. Human Physiology. 2007;33(1):105–15. (In Russ). doi: 10.1134/s0362119707010173

[60] Bikmullina R.Kh., Rozental' A.N., Pleshchinskii I.N. Inhibitory systems of the spinal cord in the control of interactions of functionally coupled muscles // Human Physiology. 2007. Vol. 33, No. 1. P. 105–115. doi: 10.1134/s0362119707010173

[61] Chelnokov AA, Buchatskaya IN. Functional features of human spinal inhibition during voluntary motor activity. Theory and Practice of Physical Culture. 2015;(6):11–3. (In Russ).

[62] Челноков А.А., Бучацкая И.Н. Функциональные особенности спинального торможения человека при произвольной двигательной активности // Теория и практика физической культуры. 2015. № 6. С. 11–13.

[63] Pleshchinsky IN, Alekseeva NL. Spinal cord: afferent interactions. Human Physiology. 1996;22(1):123–30. (In Russ).

[64] Плещинский И.Н., Алексеева Н.Л. Спинной мозг: афференные взаимодействия // Физиология человека. 1996. Т. 22, № 1. С. 123–130.

[65] Yanagawa S, Shindo M, Nakagawa S. Increase in Ib inhibition by antagonistic voluntary contraction in man. J Physiol. 1991;440:311–23. doi: 10.1113/jphysiol.1991.sp018710

[66] Yanagawa S., Shindo M., Nakagawa S. Increase in Ib inhibition by antagonistic voluntary contraction in man // The Journal of Physiology. 1991. Vol. 440. P. 311–323. doi: 10.1113/jphysiol.1991.sp018710

[67] Iles JF, Pisini JV. Cortical modulation of transmission in spinal reflex pathways of man. J Physiol. 1992;455:425–46. doi: 10.1113/jphysiol.1992.sp019309

[68] Iles J.F., Pisini J.V. Cortical modulation of transmission in spinal reflex pathways of man // The Journal of Physiology. 1992. Vol. 455. P. 425–446. doi: 10.1113/jphysiol.1992.sp019309

[69] Nielsen J, Petersin N. Changes in the effect of magnetic brain stimulation accompanying voluntary dynamic contraction in man. J Physiol. 1995;484(Pt 3):777–89. doi: 10.1113/jphysiol.1995.sp020703

[70] Nielsen J., Petersin N. Changes in the effect of magnetic brain stimulation accompanying voluntary dynamic contraction in man // The Journal of Physiology. 1995. Vol. 484, Pt. 3. P. 777–789. doi: 10.1113/jphysiol.1995.sp020703

[71] Kubota S, Uehara K, Morishita T, et al. Inter-individual variation in reciprocal Ia inhibition is dependent on the descending volleys delivered from corticospinal neurons to Ia interneurons. J Electromyogr Kinesiol. 2014;24(1):46–51. doi: 10.1016/j.jelekin.2013.11.004

[72] Kubota S., Uehara K., Morishita T., et al. Inter-individual variation in reciprocal Ia inhibition is dependent on the descending volleys delivered from corticospinal neurons to Ia interneurons // Journal of Electromyography and Kinesiology. 2014. Vol. 24, No. 1. P. 46–51. doi: 10.1016/j.jelekin.2013.11.004

[73] Matsugi A, Mori N, Uehara S, et al. Effect of cerebellar transcranial magnetic stimulation on soleus Ia presynaptic and reciprocal inhibition. Neuroreport. 2015;26(3):139–43. doi: 10.1097/wnr.0000000000000315

[74] Matsugi A., Mori N., Uehara S., et al. Effect of cerebellar transcranial magnetic stimulation on soleus Ia presynaptic and reciprocal inhibition // Neuroreport. 2015. Vol. 26, No. 3. P. 139–143. doi: 10.1097/wnr. 0000000000000315

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