Skip to main content

Advertisement

Log in

Restoration of Motor Functions in Spinal Rats by Electrical Stimulation of the Spinal Cord and Locomotor Training

  • Published:
Neuroscience and Behavioral Physiology Aims and scope Submit manuscript

The recovery of motor functions in chronic spinal rats with locomotor training on a treadmill combined with electrical stimulation of the spinal cord was studied. Training to a bipedal gait on a moving band with the body weight supported and use of either subcutaneous or epidural electrical stimulation (40 Hz) was performed for five days per week for 20–30 min. The dynamics of changes in locomotor capacity using subcutaneous and epidural electrical stimulation and their actions on the neural structures of the spinal cord could be similar. After three weeks of motor rehabilitation, a single stimulation at a frequency of 1 Hz evoked reflex monosynaptic potentials in the hindlimb muscles, while simultaneous rhythmic stimulation of two loci in the spinal cord at a frequency of 40 Hz initiated locomotor-like activity on the moving band of the treadmill. A more marked rhythm was seen after nine weeks of training, which coincided with the appearance of polysynaptic spinal reflexes. Administration of the serotonin receptor agonist quipazine enhanced polysynaptic activity in reflex responses and improved locomotion. Use of noninvasive subcutaneous stimulation in combination with locomotor training was found to be an effective method of activating neural locomotor networks to an extent comparable to that obtained with invasive epidural stimulation.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. W. C. De Groat, M. N. Kruse, M. A. Vizzard, et al., “Modification of urinary bladder function after spinal cord injury,” Adv. Neurology, 72, 347–364 (1997).

    Google Scholar 

  2. Yu. P. Gerasimenko, I. A. Lavrov, I. N. Bogacheva, et al., “Features of the formation of locomotor patterns in decerebrate cats on epidural stimulation of the spinal cord,” Ros. Fiziol. Zh., 89, No. 8, 1046– 1057 (2003).

    Google Scholar 

  3. S. Harkema, Y. Gerasimenko, J. Hodes, et al., “Effect of epidural stimulation of the lumbosacral spinal cord on voluntary movement, standing, and assisted stepping after motor complete paraplegia: A case study,” Lancet, 377, 1938–1947 (2011).

    Article  Google Scholar 

  4. U. S. Hofstoetter, B. Freundl, H. Binder, and K. Minassian, “Common neural structures activated by epidural and transcutaneous lumbar spinal cord stimulation: Elicitation of posterior root muscle reflexes,” PLoS One, 13, No. 1, e0192013 (2018), doi: https://doi.org/10.1371/journal.pone.0192013.

  5. K. Minassian and U. S. Hofstoetter, “Spinal cord stimulation and augmentative control strategies for leg movement after spinal paralysis in humans,” CNS Neurosci. Ther., 22, 262–270 (2016).

    Article  Google Scholar 

  6. S. P. Estes, J. A. Iddings, and E. C. Field-Fote, “Priming neural circuits to modulate spinal reflex excitability,” Front. Neurol., 8, 17 (2017), doi: https://doi.org/10.3389/fneur.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Y. Gerasimenko, R. Gorodnichev, A. Puhov, et al., “Initiation and modulation of locomotor circuitry output with multisite transcutaneous electrical stimulation of the spinal cord in noninjured humans,” J. Neurophysiol., 113, No. 3, 834–842 (2014).

    Article  Google Scholar 

  8. K. Minassian, U. S. Hofstoetter, S. M. Danner, et al., “Spinal rhythm generation by step-induced feedback and transcutaneous poster root stimulation in complete spinal cord-injured individuals,” Neurorehabil. Neural. Repair, 30, 233–243 (2016).

    Article  Google Scholar 

  9. Y. P. Gerasimenko, D. C. Lu, M. Modaber, et al., “Noninvasive reactivation of motor descending control after paralysis,” J. Neurotrauma, 32, No. 15, 1968–1980 (2015).

    Article  Google Scholar 

  10. R. R. Roy, D. L. Hutchison, D. J. Pierotti, et al., “EMF patterns of rat ankle extensors and fl exors during treadmill locomotion and swimming,” J. Appl. Physiol., 70, 2522–2529 (1991).

    Article  CAS  Google Scholar 

  11. R. M. Ichiyama, Y. P. Gerasimenko, H. Zhong, et al., “Hindlimb stepping movements in complete spinal rats induced by epidural spinal cord stimulation,” Neurosci. Lett., 383, No. 3, 339–344 (2005).

    Article  CAS  Google Scholar 

  12. D. G. Sayenko, D. A. Atkinson, T. C. Floyd, et al., “Effects of paired transcutaneous electrical stimulation delivered at single and dual sites over lumbosacral spinal cord,” Neurosci. Lett., 609, 229–234 (2015).

    Article  CAS  Google Scholar 

  13. R. J. Talmadge, R. R. Roy, V. J. Caiozzo, and V. R. Edgerton, “Mechanical properties of rat soleus after long-term spinal cord transaction,” J. Appl. Physiol., 93, No. 4, 1487–1497 (2002), doi: https://doi.org/10.1152/japplphysiol.00053.2002.

    Article  PubMed  Google Scholar 

  14. K. V. Baev, “Mechanisms of locomotion,” in: Physiology of the Nervous System, Nauka, Leningrad (1983).

  15. U. Sławińska, K. Miazga, an L. M. Jordan, “5-HT2 and 5-HT7 receptor agonists facilitate plantar stepping in chronic spinal rats through actions on different populations of spinal neurons,” Front. Neural Circuits, 8, 95 (2014).

  16. I. Lavrov, Y. Gerasimenko, M. Ichiyama, et al., “Plasticity of spinal cord reflexes after a complete transection in adult rats: Relationship to stepping ability,” J. Neurophysiol., 96, 1699–1710 (2006).

    Article  Google Scholar 

  17. P. E. Musienko, I. N. Bogacheva, A. A. Savokhin, et al., “Initiation of locomotor activity in decerebrate cats in noninvasive transcutaneous electrical stimulation of the spinal cord,” Ros. Fiziol. Zh., 99, No. 8, 917–927 (2013).

    CAS  Google Scholar 

  18. I. N. Bogacheva, P. E. Musienko, N. A. Shcherbakova, et al., “Analysis of locomotor activity in decerebrate cats using electromagnetic and epidural electrical stimulation of the spinal cord,” Ros. Fiziol. Zh., 98, No. 9, 1079–1093 (2012).

    CAS  Google Scholar 

  19. S. M. Danner, U. S. Hofstoetter, J. Ladenbauer, et al., “Can the human lumbar posterior columns be stimulated by transcutaneous spinal cord stimulation? A modeling study,” Artif. Organs, 35, No. 3, 257–262 (2011).

    Article  Google Scholar 

  20. A. Lundberg, “Multisensory control of spinal refl ex pathways,” Prog. Brain Res., 50, 11–28 (1979).

    Article  CAS  Google Scholar 

  21. A. M. Cabaj, H. Majczyński, E. Couto, et al., “Serotonin controls initiation of locomotion and afferent modulation of coordination via 5HT7 receptors in adult rats,” J. Physiol., 595, No. 1, 301–320 (2017).

    Article  CAS  Google Scholar 

  22. K. Fouad, G. A. Metz, D. Merkler, et al., “Treadmill training in incomplete spinal cord injured rats,” Behav. Brain Res., 115, 107–113 (2000).

    Article  CAS  Google Scholar 

  23. M. Wirz, G. Colombo, and V. Dietz, “Long term effects of locomotor training in spinal humans,” J. Neurol. Neurosurg. Psychiatry, 71, No. 1, 93–96 (2001).

    Article  CAS  Google Scholar 

  24. O. A. Nikitin, I. N. Bogacheva, P. E. Musienko, et al., “Afferent activation of the stepping movement generator in spinal cats in the early post-spinalization period,” Vestn. Tver. Gos. Univ. Ser. Biol. Ekol., 6, 22–30 (2007).

    Google Scholar 

  25. E. S. Tomilovskaya, T. R. Moshonkina, R. M. Gorodnichev, et al., “Mechanical stimulation of the support zones of the feet: a noninvasive means of activating the stepping movement generator in humans,” Fiziol. Cheloveka, 39, No. 5, 34–41 (2013).

    Google Scholar 

  26. N. Giroux, S. Rossignol, and T. A. Reader, “Autoradiographic study of alpha-1, alpha-noradrenergic and serotonin 1A receptors in the spinal cord of normal and chronically transected cats,” J. Comp. Neurol., 406, 402–414 (1999).

    Article  CAS  Google Scholar 

  27. B. J. Schmidt, and L. M. Jordan, “The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord,” Brain Res. Bull., 53, 689–710 (2000).

    Article  CAS  Google Scholar 

  28. V. Dietz, K. Nakazawa, M. Wirz, and T. Erni, “Level of spinal cord lesion determines locomotor activity in spinal man,” Exp. Brain Res., 128, 405–409 (1999).

    Article  CAS  Google Scholar 

  29. A. J. Fong, L. L. Cai, C. K. Otoshi, et al., “Spinal cord-transected mice learn to step in response to quipazine treatment and robotic training,” J. Neurosci., 25, No. 50, 11738–11747 (2005).

    Article  CAS  Google Scholar 

  30. D. Feraboli-Lohnherr, J. Y. Barthe, and D. Orsal, “Serotonin-induced activation of the network for locomotion in adult spinal rats,” J. Neurosci. Res., 55, 87–98 (1999).

    Article  CAS  Google Scholar 

  31. E. G. Gilerovich, T. R. Moshonkina, N. V. Pavlova, et al., “Morphofunctional studies of lesioned spinal cord in rats after activation of serotonin receptors and motor loading,” Dokl. Akad. Nauk., 428, No. 1, 413–415 (2009).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. V. Pavlova.

Additional information

Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 105, No. 5, pp. 565–577, May, 2019.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pavlova, N.V., Bogacheva, I.N., Bazhenova, E.Y. et al. Restoration of Motor Functions in Spinal Rats by Electrical Stimulation of the Spinal Cord and Locomotor Training. Neurosci Behav Physi 50, 599–606 (2020). https://doi.org/10.1007/s11055-020-00941-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11055-020-00941-y

Keywords

Navigation