Skip to main content
Log in

Modulation of Blood Flow in the Skin of Human Legs during Transcutaneus Electrical Stimulation of the Spinal Cord

  • Published:
Human Physiology Aims and scope Submit manuscript

Abstract

Changes in blood supply to the skin of the anterior-lateral surface of the shin of 12 healthy subjects were detected. The analysis was performed using laser Doppler flowmetry during transcutaneous electrical spinal cord stimulation (TSCS) by subthreshold bipolar pulses with a frequency of 30 Hz. The TSCS at T7 and L1 vertebrae level leads to a significant increase in cutaneous blood flow. With a stimulus intensity of 90% of the motor threshold, the increase in skin perfusion during stimulation at L1 was about 74%, and during stimulation at T7, 38%, relative to the baseline. We suggest that vasodilation and hyperemia of the skin during TSCS occur mainly due to the antidromic stimulation of sensory nerve fibers. Nitric oxide (NO) is an important modulator that promotes vasodilation in TSCS. It is released by the nerve endings and the layer of endothelial cells. Inhibition of cystathionine-γ-lyase significantly reduces the increase in skin blood flow during TSCS. Therefore, it was concluded that H2S, as well as NO, is also involved in the vasodilation in the skin during TSCS.

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.

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. Garstang, S.V. and Miller-Smith, S.A., Autonomic nervous system dysfunction after spinal cord injury, Phys. Med. Rehabil. Clin. N. Am., 2007, vol. 18, no. 2, p. 275.

    Article  Google Scholar 

  2. Harkema, S., Gerasimenko, Y., Hodes, J., et al., Effect of epidural stimulation of thelumbosacral spinal cord on voluntary movement, standing, and assisted step-ping after motor complete paraplegia: a case study, Lancet, 2011, vol. 377, no. 9781, p. 1938.

    Article  Google Scholar 

  3. Gerasimenko, Y., Gorodnichev, R., Moshonkina, T., et al., Transcutaneous electrical spinal cord stimulation in humans, Ann. Phys. Rehabil. Med., 2015, vol. 58, no. 4, p. 225.

    Article  Google Scholar 

  4. Gerasimenko, Y., Gorodnichev, R., Puhov, A., et al., Initiation and modulation of locomotor circuitry output with multisite transcutaneous electrical stimulation of the spinal cord in noninjured humans, J. Neurophysiol., 2014, vol. 113, no. 3, p. 834.

    Article  Google Scholar 

  5. Lobov, G.I., Shcherbakova, N.A., Gorodnichev, R.M., et al., Effect of transcutaneous electrical spinal cord stimulation on the blood flow in the skin of lower limbs, Hum. Physiol., 2017, vol. 43, no. 5, p. 518.

    Article  Google Scholar 

  6. Lobov, G.I., Gerasimenko, Yu.P., and Moshonkina, T.R., Mechanisms of vasodilation in skin during lumbar transcutaneous spinal cord stimulation, Hum. Physiol., 2019, vol. 45, no. 4, p. 389.

    Article  CAS  Google Scholar 

  7. Johnson, J.M., Minson, C.T., and Kellogg, Jr., D.L., Cutaneous vasodilator and vasoconstrictor mechanisms in temperature regulation, Compr. Physiol., 2014, vol. 4, no. 1, p. 33.

    Article  Google Scholar 

  8. Ozüm, Ü., Akyol, M., Balaban, H., et al., Effect of cervical spinal cord electrical stimulation on nitric oxide levels in brain and dermal tissues: an evaluation using by real-time nitric oxide measurement, Acta Neurochir. (Wien), 2012, vol. 154, no. 9, p. 1641.

    Article  Google Scholar 

  9. Branco, L.G., Soriano, R.N., and Steiner, A.A., Gaseous mediators in temperature regulation, Compr. Physiol., 2014, vol. 4, no. 4, p. 1301

    Article  Google Scholar 

  10. Streeter, E., Hart, J., and Badoer, E., An investigation of the mechanisms of hydrogen sulfide-induced vasorelaxation in rat middle cerebral arteries, Naunyn-Schmiedebergs Arch. Pharmakol., 2012, vol. 385, no. 10, p. 991.

    Article  CAS  Google Scholar 

  11. Aslan, S.C., Legg Ditterline, B.E., Park, M.C., et al., Epidural spinal cord stimulation of lumbosacral networks modulates arterial blood pressure in individuals with spinal cord injury-induced cardiovascular deficits, Front. Physiol., 2018, vol. 9, p. 565.

    Article  Google Scholar 

  12. Phillips, A.A., Squair, J.W., Sayenko, D.G., et al., An autonomic neuroprosthesis: noninvasive electrical spinal cord stimulation restores autonomic cardiovascular function in individuals with spinal cord injury, J. Neurotrauma, 2018, vol. 35, no. 3, p. 446.

    Article  Google Scholar 

  13. Krupatkin, A.I. and Sidorov, V.V., Funktsional’naya diagnostika sostoyaniya mikrotsirkulyatorno-tkanevykh sistem (Rukovodstvo dlya vrachei) (Functional Diagnostics of Microcirculatory Tissue System State: Handbook for Physicians), Moscow: Librokom, 2013.

  14. Dellon, A.L., Höke, A., Williams, E.H., et al., The sympathetic innervation of the human foot, Plast. Reconstr. Surg., 2012, vol. 129, no. 4, p. 905.

    Article  CAS  Google Scholar 

  15. van Duijnhoven, N.T., Janssen, T.W., Green, D.J., et al., Effect of functional electrostimulation on impaired skin vasodilator responses to local heating in spinal cord injury, J. Appl. Physiol., 2009, vol. 106, no. 4, p. 1065.

    Article  Google Scholar 

  16. Smith, C.J., Craighead, D.H., and Alexander, L.M., Effects of vehicle microdialysis solutions on cutaneous vascular responses to local heating, J. Appl. Physiol., 2017, vol. 123, no. 6, p. 1461.

    Article  CAS  Google Scholar 

  17. Wong, B.J., Sensory nerves and nitric oxide contribute to reflex cutaneous vasodilation in humans, Am. J. Physiol.-Regul. Integr. Comp. Physiol., 2013, vol. 304, no. 8, p. R651.

    Article  CAS  Google Scholar 

  18. Bruning, R.S., Santhanam, L., Stanhewicz, A.E., et al., Endothelial nitric oxide synthase mediates cutaneous vasodilation during local heating and is attenuated in middle-aged human skin, J. Appl. Physiol., 2012, vol. 112, no. 12, p. 2019.

    Article  CAS  Google Scholar 

  19. Croom, J.E., Foreman, R.D., Chandler, M.J., and Barron, K.W., Cutaneous vasodilation during dorsal column stimulation is mediated by dorsal roots and CGRP, Am. J. Physiol., 1997, vol. 272, no. 2, p. H950.

    Article  CAS  Google Scholar 

  20. Yan, L., Yinghui, T., Bo, Y., et al., Effect of calcitonin gene-related peptide on nitric oxide production in osteoblasts: an experimental study, Cell Biol. Int., 2011, vol. 35, no. 8, p. 757.

    Article  CAS  Google Scholar 

  21. Wu, M., Komori, N., Qin, C., et al., Roles of peripheral terminals of transient receptor potential vanilloid-1 containing sensory fibers in spinal cord stimulation-induced peripheral vasodilation, Brain Res., 2007, vol. 1156, p. 80.

    Article  CAS  Google Scholar 

  22. Idigo, W.O., Reilly, S., Zhang, M.H., et al., Regulation of endothelial nitric-oxide synthase (NOS) S-glutathionylation by neuronal NOS: evidence of a functional interaction between myocardial constitutive NOS isoforms, J. Biol. Chem., 2012, vol. 287, no. 52, p. 43 665.

    Article  Google Scholar 

  23. Hosoki, R., Matsuki, N., and Kimura, H., The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide, Biochem. Biophys. Res. Commun., 1997, vol. 237, no. 3, p. 527.

    Article  CAS  Google Scholar 

  24. Bełtowski, J., Hydrogen sulfide in pharmacology and medicine. An update, Pharmacol. Rep., 2015, vol. 67, no. 3, p. 647.

    Article  Google Scholar 

  25. Kimura, H., The physiological role of hydrogen sulfide and beyond, Nitric Oxide, 2014, vol. 41, p. 4.

    Article  CAS  Google Scholar 

  26. Zhao, W., Zhang, J., Lu, Y., and Wang, R., The vasorelaxant effect of H2S as a novel endogenous gaseous K(ATP) channel opener, EMBO J., 2001, vol. 20, no. 21, p. 6008.

    Article  CAS  Google Scholar 

  27. Li, L., Rose, P., and Moore, P.K., Hydrogen sulfide and cell signaling, Annu. Rev. Pharmacol. Toxicol., 2011, vol. 51, p. 169.

    Article  CAS  Google Scholar 

Download references

Funding

The study was financially supported by the Program “Fundamental Scientific Research for the Long-Term Development and Ensuring the Competitiveness of Society and the State” (Topic 63.4, (0113-2019-0006)), Russian Foundation for Basic Research, project no. 16-29-08277 and the Basic Research Program of the Presidium of the Russian Academy of Sciences no. 1.42.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to G. I. Lobov.

Ethics declarations

Conflict of interests. The authors declare no apparent or potential conflicts of interest related to the publication of this article.

Statement of compliance with standards of research involving humans as subjects. All studies were carried out in accordance with the principles of biomedical ethics formulated in the Helsinki Declaration of 1964 and its subsequent updates and approved by the local bioethical committee of the Institute of Physiology, RAS (St. Petersburg). Each study participant submitted voluntary written informed consent, signed by him after explaining to him the potential risks and benefits, as well as the nature of the forthcoming study.

Additional information

Translated by I. Shipounova

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lobov, G.I., Gerasimenko, Y.P. & Moshonkina, T.R. Modulation of Blood Flow in the Skin of Human Legs during Transcutaneus Electrical Stimulation of the Spinal Cord. Hum Physiol 46, 384–390 (2020). https://doi.org/10.1134/S0362119720040088

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0362119720040088

Keywords:

Navigation