Skip to main content
SpringerLink
Log in

Tonic Activity and Gravitational Control of the Postural Muscle

  • Published:
Human Physiology Aims and scope Submit manuscript

Abstract

The review describes and analyzes the available data on the mechanisms that control the structure and functional potential of a postural muscle, which works nearly unceasingly to allow humans and animals to actively exist on the Earth’s surface. Prof. I.B. Kozlovskaya and her students obtained, described, and systematized a great portion of the data. Many interesting facts and observations were documented in other labs and research centers, often under the influence of Kozlovskaya’s ideas. A concept of a tonic system is the most important part of her theoretical legacy. The tonic system is understood as an integral physiological system that includes not only slow muscle fibers and small-size motor neurons, which innervate them, but also brain (up to the striatum and motor cortex inclusively) and sensory mechanisms. A basic conclusion of the review is that gravity-dependent tonic contractile activity of postural muscles, which is controlled by the nervous system and afferent mechanisms, plays a key role in maintaining their structure, signaling pathways, and mechanical properties crucial for their continuous antigravity activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.
Fig. 8.
Fig. 9.
Fig. 10.

Similar content being viewed by others

REFERENCES

  1. Delp, M.D. and Duan, C., Composition and size of type I, IIA, IID/X, and IIB fibers and citrate synthase activity of rat muscle, J. Appl. Physiol., 1996, vol. 80, no. 1, pp. 261–270.

    CAS  PubMed  Google Scholar 

  2. Hodgson, J.A., Roy, R.R., Higuchi, N., et al., Does daily activity level determines muscle phenotype? J. Exp. Biol., 2005, vol. 208, pp. 3761–3770.

    PubMed  Google Scholar 

  3. Kozlovskaya, I., Dmitrieva, I., Grigorieva, L., et al., Gravitational mechanisms in the motor system. Studies in real and simulated weightlessness, in Stance and Motion: Facts and Concepts, Gurfinkel, V.S., Ioffe, M.Y., and Massion, J., Eds., Boston, MA: Springer-Verlag, 1988, pp. 37–48.

    Google Scholar 

  4. Shenkman, B.S. and Kozlovskaya, I.B., Cellular responses of human postural muscle to dry immersion, Front. Physiol., 2019, vol. 10, p. 187.

    PubMed  PubMed Central  Google Scholar 

  5. Yuganov, E.M., Kas’yan, I.I., and Asyamolov, B.F., Bioelectrical activity of skeletal muscle under condition of intermittent action of overloading and weightlessness, Izv. Akad. Nauk SSSR, Ser. Biol., 1963, vol. 5, pp. 746–754.

    Google Scholar 

  6. Alford, E.K., Roy, R.R., Hodgson, J.A., and Edgerton, V.R., Electromyography of rat soleus, medial gastrocnemius, and tibialis anterior during hind limb suspension, Exp. Neurol., 1987, vol. 96, pp. 635–649.

    CAS  PubMed  Google Scholar 

  7. Kawano, F., Nomura, T., Ishihara, A., et al., Afferent input-associated reduction of muscle activity in microgravity environment, Neuroscience, 2002, vol. 114, pp. 1133–1138.

    CAS  PubMed  Google Scholar 

  8. De-Doncker, L., Kasri, M., Picquet, F., and Falempin, M., Physiologically adaptive changes of the L5 afferent neuro-gram and of the rat soleus EMG activity during 14 days of hindlimb unloading and recovery, J. Exp. Biol., 2005, vol. 208, pp. 4585–4592.

    CAS  PubMed  Google Scholar 

  9. Kirenskaya, A.V., Kozlovskaya, I.B., and Sirota, M.G., Effect of immersion hypokinesia on the characteristics of the rhythmic activity of the motor units of the soleus muscle, Fiziol. Chel., 1986, vol. 12, pp. 627–632.

    Google Scholar 

  10. Ohira, Y., Yoshinaga, T., Ohara, M., et al., The role of neural and mechanical influences in maintaining normal fast and slow muscle properties, Cells Tissues Organs, 2006, vol. 182, pp. 129–142. https://doi.org/10.1159/000093963

    Article  CAS  PubMed  Google Scholar 

  11. Canon, F. and Goubel, F., Changes in stiffness induced by hindlimb suspension in rat soleus muscle, Pflugers Arch., 1995, vol. 429, no. 3, pp. 332–337.

    CAS  PubMed  Google Scholar 

  12. Shenkman, B.S., From slow to fast: hypogravity-induced remodeling of muscle fiber myosin phenotype, Acta Nat., 2016, vol. 8, no. 4, pp. 47–59.

    CAS  Google Scholar 

  13. Baldwin, K.M., Haddad, F., Pandorf, C.E., et al., Alterations in muscle mass and contractile phenotype in response to unloading models: role of transcriptional/pretranslational mechanisms, Front. Physiol., 2013, vol. 4, p. 284. https://doi.org/10.3389/fphys.201

    Article  PubMed  PubMed Central  Google Scholar 

  14. Grigor’ev, A.I., Kozlovskaya, I.B., and Shenkman, B.S., The role of support afferents in organisation of the tonic muscle system, Ross. Fiziol. Zh. im. I.M. Sechenova, 2004, vol. 90, no. 5, pp. 508–521.

    PubMed  Google Scholar 

  15. Mounier, Y., Montel, V., Picquet, F., et al., Dual effect of deafferentation on contractile characteristics and sarcoplasmic reticulum properties in rat soleus fibers, J. Appl Physiol., 2005, vol. 99, no. 2, pp. 542–548.

    CAS  PubMed  Google Scholar 

  16. Shenkman, B.S., Nemirovskaya, T.L., Mukhina, A.M., et al., The effect of antagonist muscle inactivation on atrophic processes in the musculus soleus of the rat under gravitational unload, Dokl. Biol. Sci., 2005, vol. 400, no. 1, pp. 35–38.

    Google Scholar 

  17. Shapovalova, K.B., Neostriatum i regulyatsiya proizvol’nogo dvizheniya (Neostriatum and regulation of voluntary movement), St. Petersburg, 2015.

  18. Demertzi, A., van Ombergen, A., Tomilovskaya, E., et al., Cortical reorganization in an astronaut’s brain after long-duration spaceflight, Brain Struct. Funct., 2016, vol. 221, no. 5, pp. 2873–2876. https://doi.org/10.1007/s00429-015-1054-3

    Article  PubMed  Google Scholar 

  19. Luxa, N., Salanova, M., Schiffl, G., et al., Increased myofiber remodelling and NFATc1-myonuclear translocation in rat postural skeletal muscle after experimental vestibular deafferentation, J. Vestibular Res., 2013, vol. 23, pp. 187–193.

    Google Scholar 

  20. Fuller, C., Neurovestibular influences on muscle myosin phenotype, Proc. XII All-Russ. Conf. on Space Biology and Aerospace Medicine, Moscow, 2002, pp. 449–450.

  21. Kasri, M., Picquet, F., and Falempin, M., Effects of unilateral and bilateral labyrinthectomy on rat postural muscle properties: the soleus, Exp. Neurol., 2004, vol. 185, no. 1, pp. 143–153.

    CAS  PubMed  Google Scholar 

  22. Kawano, F., Ishihara, A., Stevens, J.L., et al., Tension and afferent input-associated responses of neuromuscular system of rats to hindlimb unloading and/or tenotomy, Am. J. Physiol.: Regul. Integr. Comp. Physiol., 2004, vol. 287, pp. 76–86.

    Google Scholar 

  23. Henriksen, E.J. and Tischler, M.E., Time course of the response of carbohydrate metabolism to unloading of the soleus, Metabolism, 1988, vol. 37, pp. 201–208.

    CAS  PubMed  Google Scholar 

  24. Shenkman, B.S., How postural muscle senses disuse? Early signs and signals, Int. J. Mol. Sci., 2020, vol. 21, no. 14, p. 5037. https://doi.org/10.3390/ijms21145037

    Article  CAS  PubMed Central  Google Scholar 

  25. Boulenguez, P., Liabeuf, S., Bos, R., et al., Down-regulation of the potassium-chloride cotransporter KCC2 contributes to spasticity after spinal cord injury, Nat. Med., 2010, vol. 16, no. 3, pp. 302–307. https://doi.org/10.1038/nm.2107

    Article  CAS  PubMed  Google Scholar 

  26. Edgerton, V.R. and Roy, R.R., Spasticity: a switch from inhibition to excitation, Nat. Med., 2010, vol. 16, no. 3, pp. 270–271. https://doi.org/10.1038/nm0310-270

    Article  CAS  PubMed  Google Scholar 

  27. Roy, R.R. and Edgerton, V.R., Neurobiological perspective of spasticity as occurs after a spinal cord injury, Exp. Neurol., 2012, vol. 235, no. 1, pp. 116–122. https://doi.org/10.1016/j.expneurol.2012.01.017

    Article  PubMed  Google Scholar 

  28. Akhter, E.T., Griffith, R.W., English, A.W., and Alvarez, F.J., Removal of the potassium chloride co-transporter from the somatodendritic membrane of axotomized motoneurons is independent of BDNF/TrkB signaling but is controlled by neuromuscular innervation, eNeuro, 2019, vol. 6, no. 5. https://doi.org/10.1523/eneuro.0172-19.2019

  29. Kozlovskaya, I.B., Fundamental and applied objectives of investigations in immersion, Aviakosm. Ekol. Med., 2008, vol. 42, no. 5, pp. 3–7.

    Google Scholar 

  30. Furby, A., Mounier, Y., Stevens, L., et al., Effect of chronic stimulation on rat soleus skinned fibers during hindlimb suspension, Muscle Nerve, 1993, vol. 16, pp. 720–726.

    CAS  PubMed  Google Scholar 

  31. Leterme, D. and Falempin, M., Compensatory effects of chronic electrostimulation on unweighted rat soleus muscle, Pflugers Arch., 1994, vol. 426, pp. 155–160.

    CAS  PubMed  Google Scholar 

  32. Dupont, E., Cieniewski-Bernard, C., Bastide, B., and Stevens, L., Electrostimulation during hindlimb unloading modulates PI3K-AKT downstream targets without preventing soleus atrophy and restores slow phenotype through ERK, Am. J. Physiol.: Regul. Integr. Comp. Physiol., 2011, vol. 300, pp. 408–417.

    Google Scholar 

  33. Canon, F., Goubel, F., and Guezennec, C.Y., Effects of chronic low frequency stimulation on contractile elastic properties of hindlimb suspended rat soleus muscle, Eur. J. Appl. Physiol. Occup. Physiol., 1998, vol. 77, nos. 1–2, pp. 118–124.

    CAS  PubMed  Google Scholar 

  34. Guo, B.S., Cheung, K.K., Yeung, S.S., et al., Electrical stimulation influences satellite cell proliferation and apoptosis in unloading-induced muscle atrophy in mice, PLoS One, 2012, vol. 7, no. 1.

  35. Zhang, B.T., Yeung, S.S., Liu, Y., et al., The effects of low frequency electrical stimulation on satellite cell activity in rat skeletal muscle during hindlimb suspension, BMC Cell Biol., 2010, vol. 11, no. 87.

  36. Rennie, M.J., Why muscle stops building when it’s working, J. Physiol., 2005, vol. 569, no. 1, p. 3.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Ernandes-Korvo, R., Kozlovskaya, I.B., Kreidich, Yu.V., et al., Effect of a 7-day space flight on the structure and function of the human locomotor apparatus, Kosm. Biol. Aviakosm. Med., 1983, vol. 17, no. 2, pp. 37–44.

    Google Scholar 

  38. Lomonosova, Yu.N., Kalamkarov, G.R., Bugrova, A.E., et al., Protective effect of L-arginine administration on proteins of unloaded m. soleus, Biochemistry (Moscow), 2011, vol. 76, no. 5, pp. 571–580.

    CAS  PubMed  Google Scholar 

  39. Kyparos, A., Feeback, D.L., Layne, C.S., et al., Mechanical stimulation of the plantar foot surface attenuates soleus muscle atrophy induced by hindlimb unloading in rats, J. Appl. Physiol., 2005, vol. 99, no. 2, pp. 739–746. https://doi.org/10.1152/japplphysiol.00771.2004

    Article  PubMed  Google Scholar 

  40. Tyganov, S.A., Mochalova, E.P., Belova, S.P., et al., Effects of plantar mechanical stimulation on anabolic and catabolic signaling in rat postural muscle under short-term gravitational unloading, Front. Physiol., 2019, vol. 10, art. ID 1252. https://doi.org/10.3389/fphys.2019.01252

    Article  PubMed  PubMed Central  Google Scholar 

  41. Polge, C., Heng, A.E., Jarzaguet, M., et al., Muscle actin is polyubiquitinylated in vitro and in vivo and targeted for breakdown by the E3 ligase MuRF1, FASEB J., 2011, vol. 25, no. 11, pp. 3790–3802. https://doi.org/10.1096/fj.11-180968

    Article  CAS  PubMed  Google Scholar 

  42. Cohen, S., Brault, J.J., Gygi, S.P., et al., During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation, J. Cell Biol., 2009, vol. 185, no. 6, pp. 1083–1095. https://doi.org/10.1083/jcb.200901052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Martin, T.P., Edgerton, V.R., and Grindeland, R.E., Influence of spaceflight on rat skeletal muscle, J. Appl. Physiol., 1988, vol. 65, pp. 2318–2325.

    CAS  PubMed  Google Scholar 

  44. Desplanches, D., Mayet, M.H., Ilyina-Kakueva, E.I., et al., Structural and metabolic properties of rat muscle exposed to weightlessness aboard Cosmos 1887, Eur. J. Appl. Physiol. Occup. Physiol., 1991, vol. 63, pp. 288–292.

    CAS  PubMed  Google Scholar 

  45. Ohira, Y., Yoshinaga, T., Ohara, M., et al., Myonuclear domain and myosin phenotype in human soleus after bed rest with or without loading, J. Appl. Physiol., 1999, vol. 87, pp. 1776–1785.

    CAS  PubMed  Google Scholar 

  46. Templeton, G.H., Sweeney, H.L., Timson, B.F., et al., Changes in fiber composition of soleus muscle during rat hindlimb suspension, J. Appl. Physiol., 1988, vol. 65, pp. 1191–1195.

    CAS  PubMed  Google Scholar 

  47. Desplanches, D., Mayet, M.H., Sempore, B., and Flandrois, R., Structural and functional responses to prolonged hindlimb suspension in rat muscle, J. Appl. Physiol., 1987, vol. 63, pp. 558–563.

    CAS  PubMed  Google Scholar 

  48. Vikne, H., Strøm, V., Pripp, A.H., and Gjøvaag, T., Human skeletal muscle fiber type percentage and area after reduced muscle use: a systematic review and meta-analysis, Scand. J. Med., Sci. Sports, 2020, vol. 30, no. 8, pp. 1298–1317. https://doi.org/10.1111/sms.13675

    Article  Google Scholar 

  49. Schiaffino, S. and Reggiani, C., Fiber types in mammalian skeletal muscles, Physiol. Rev., 2011, vol. 91, no. 4, pp. 1447–1531. https://doi.org/10.1152/physrev.00031.2010

    Article  CAS  PubMed  Google Scholar 

  50. Shenkman, B.S., Lyubaeva, E.V., Popov, D.V., et al., Effects of chronic low-frequency electrical stimulation of human knee extensor muscles exposed to static passive stretching, Hum. Physiol., 2006, vol. 32, no. 1, pp. 74–80.

    Google Scholar 

  51. Liu, Y., Randall, W.R., and Schneider, M.F., Activity-dependent and -independent nuclear fluxes of HDAC4 mediated by different kinases in adult skeletal muscle, J. Cell Biol., 2005, vol. 168, pp. 887–897.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Liu, Y., Shen, T., Randall, W.R., and Schneider, M.F., Signaling pathways in activity-dependent fiber type plasticity in adult skeletal muscle, J. Muscle Res. Cell Motil., 2005, vol. 26, pp. 13–21.

    PubMed  Google Scholar 

  53. Potthoff, M.J., Wu, H., Arnold, M.A., et al., Histone deacetylase degradation and MEF2 activation promote the formation of slow-twitch myofibers, J. Clin. Investig., 2007, vol. 117, pp. 2459–2467.

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Röckl, K.S., Hirshman, M.F., Brandauer, J., et al., Skeletal muscle adaptation to exercise training: AMP-activated protein kinase mediates muscle fiber type shift, Diabetes, 2007, vol. 56, pp. 2062–2069.

    PubMed  Google Scholar 

  55. McGee, S.L. and Hargreaves, M., AMPK-mediated regulation of transcription in skeletal muscle, Clin. Sci., 2010, vol. 118, pp. 507–518.

    CAS  Google Scholar 

  56. Zhao, X., Sternsdorf, T., Bolger, T.A., et al., Regulation of MEF2 by histone deacetylase 4 and SIRT1 deacetylase-mediated lysine modifications, Mol. Cell. Biol., 2005, vol. 25, pp. 8456–8464.

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Frey, N., Richardson, J.A., and Olson, E.N., Calsarcins, a novel family of sarcomeric calcineurin-binding proteins, Proc. Natl. Acad. Sci. U.S.A., 2000, vol. 97, pp. 14632–14637.

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Rothermel, B., Vega, R.B., Yang, J., et al., A protein encoded within the Down syndrome critical region is enriched in striated muscles and inhibits calcineurin signaling, J. Biol. Chem., 2000, vol. 275, pp. 8719–8725.

    CAS  PubMed  Google Scholar 

  59. Yang, J., Rothermel, B., Vega, R.B., et al., Independent signals control expression of the calcineurin inhibitory proteins MCIP1 and MCIP2 in striated muscles, Circ. Res., 2000, vol. 87, pp. 61–68.

    Google Scholar 

  60. Shen, T., Cseresnyés, Z., Liu, Y., et al., Regulation of the nuclear export of the transcription factor NFATc1 by protein kinases after slow fibre type electrical stimulation of adult mouse skeletal muscle fibres, J. Physiol., 2007, vol. 579, pp. 535–551.

    CAS  PubMed  Google Scholar 

  61. Sharlo, K., Paramonova, I., Turtikova, O., et al., Plantar mechanical stimulation prevents calcineurin-NFATc1 inactivation and slow-to-fast fiber type shift in rat soleus muscle under hindlimb unloading, J. Appl. Physiol., 2019, vol. 126, pp. 1769–1781.

    CAS  PubMed  Google Scholar 

Download references

ACKNOWLEDGMENTS

We are grateful to S.A. Tyganov (Laboratory of Myology, Institute of Biomedical Problems) for help in figure preparation.

Funding

This work was supported by the Russian Foundation for Basic Research (project no. 20-34-70 022) and the Program of Basic Research at the Institute of Biomedical Problems.

Author information

Authors and Affiliations

  1. Institute of Biomedical Problems, Russian Academy of Sciences, Moscow, Russia

    B. S. Shenkman, T. M. Mirzoev & I. B. Kozlovskaya

Authors
  1. B. S. Shenkman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. M. Mirzoev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. B. Kozlovskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to B. S. Shenkman.

Ethics declarations

Conflict of interests. The authors declare that they have no conflict of interest.

This work does not contain any studies involving animals or human subjects performed by any of the authors.

Additional information

Translated by T. Tkacheva

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shenkman, B.S., Mirzoev, T.M. & Kozlovskaya, I.B. Tonic Activity and Gravitational Control of the Postural Muscle. Hum Physiol 47, 744–756 (2021). https://doi.org/10.1134/S0362119721070100

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0362119721070100

Keywords:

Search

Navigation