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Current Medical Science

, Volume 38, Issue 5, pp 903–909 | Cite as

Effect of Paired Associative Stimulation on Motor Cortex Excitability in Rats

  • Xiang-yu Zhang
  • Yan-fang Sui
  • Tie-cheng GuoEmail author
  • Sai-hua Wang
  • Yan Hu
  • Yin-shan Lu
Article

Abstract

Paired associative stimulation (PAS), combining transcranial magnetic stimulation (TMS) with electrical peripheral nerve stimulation (PNS) in pairs with an optimal interstimulus interval (ISI) in between, has been shown to influence the excitability of the motor cortex (MC) in humans. However, the underlying mechanisms remain unclear. This study was designed to explore an optimal protocol of PAS, which can modulate the excitability of MC in rats, and to investigate the underlying mechanisms. The resting motor thresholds (RMTs) of TMS-elicited motor evoked potentials (MEPs) recorded from the gastrocnemius muscle and the latency of P1 component of somatosensory evoked potentials (SEPs) induced by electrical tibial nerve stimulation were determined in male Sprague-Dawley rats (n=10). Sixty rats were then randomly divided into 3 groups: a PAS group (further divided into 10 subgroups at various ISIs calculated by using the latency of P1, n=5, respectively), a TMS (only) group (n=5) and a PNS (only) group (n=5). Ninety repetitions of PAS, TMS and PNS were administered to the rats in the 3 groups, respectively, at the frequency of 0.05 Hz and the intensity of TMS at 120% RMT and that of PNS at 6 mA. RMTs and motor evoked potentials’ amplitude (MEPamp) were recorded before and immediately after the interventions. It was found that the MEPamp significantly decreased after PAS at ISI of 5 ms (P<0.05), while the MEPamp significantly increased after PAS at ISI of 15 ms, as compared with those before the intervention (P<0.05). However, the RMT did not change significantly after PAS at ISI of 5 ms or 15 ms (P>0.05). PAS at other ISIs as well as the sole use of TMS and PNS induced no remarkable changes in MEPamp and RMT. In conclusion, PAS can influence motor cortex excitability in rats. Neither TMS alone nor PNS alone shows significant effect.

Key words

paired associative stimulation transcranial magnetic stimulation peripheral nerves electrical stimulation resting motor thresholds motor evoked potentials somatosensory evoked potentials 

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References

  1. 1.
    Stefan K, Kunesch E, Cohen LG, et al. Induction of plasticity in the human motor cortex by paired associative stimulation. Brain, 2000,123(Pt 3):572–584Google Scholar
  2. 2.
    Meunier S, Russmann H, Simonetta-Moreau M, et al. Changes in spinal excitability after PAS. J Neurophysiol, 2007,97(4):3131–3135Google Scholar
  3. 3.
    Kumru H, Albu S, Rothwell J, et al. Modulation of motor cortex excitability by paired peripheral and transcranial magnetic stimulation. Clin Neurophysiol, 2017,128(10):2043–2047Google Scholar
  4. 4.
    Cortes M, Thickbroom GW, Valls-Sole J, et al. Spinal associative stimulation: A non-invasive stimulation paradigm to modulate spinal excitability. Clin Neurophysiol, 2011,122(11):2254–2259Google Scholar
  5. 5.
    Wolters A, Sandbrink F, Schlottmann A, et al. A temporally asymmetric hebbian rule governing plasticity in the human motor cortex. J Neurophysiol, 2003,89(5):2339–2345Google Scholar
  6. 6.
    Stefan K, Kunesch E, Benecke R, et al. Mechanisms of enhancement of human motor cortex excitability induced by interventional paired associative stimulation. J Physiol, 2002,543(Pt 2):699–708Google Scholar
  7. 7.
    Castel-Lacanal E, Marque P, Tardy J, et al. Induction of cortical plastic changes in wrist muscles by paired associative stimulation in the recovery phase of stroke patients. Neurorehabil Neural Repair, 2009,23(4):366–372Google Scholar
  8. 8.
    Jung P, Ziemann U. Homeostatic and nonhomeostatic modulation of learning in human motor cortex. J Neurosci, 2009,29(17):5597–5604Google Scholar
  9. 9.
    Jayaram G, Stinear JW. Contralesional paired associative stimulation increases paretic lower limb motor excitability post-stroke. Exp Brain Res, 2008,185(4):563–570Google Scholar
  10. 10.
    Rogers LM, Brown DA, Stinear JW. The effects of paired associative stimulation on knee extensor motor excitability of individuals post-stroke: a pilot study. Clin Neurophysiol, 2011,122(6):1211–1218Google Scholar
  11. 11.
    Michou E, Mistry S, Jefferson S, et al. Targeting unlesioned pharyngeal motor cortex improves swallowing in healthy individuals and after dysphagic stroke. Gastroenterology, 2012,142(1):29–38Google Scholar
  12. 12.
    Michou E, Mistry S, Jefferson S, et al. Characterizing the mechanisms of central and peripheral forms of neurostimulation in chronic dysphagic stroke patients. Brain Stimul, 2014,7(1):66–73Google Scholar
  13. 13.
    Stinear JW, Hornby TG. Stimulation-induced changes in lower limb corticomotor excitability during treadmill walking in humans. JPhysiol, 2005,567(Pt 2):701–711Google Scholar
  14. 14.
    Stefan K, Wycislo M, Classen J. Modulation of associative human motor cortical plasticity by attention. J Neurophysiol, 2004,92(1):66–72Google Scholar
  15. 15.
    Ziemann U. TMS induced plasticity in human cortex. Rev Neurosci, 2004,15(4):253–266Google Scholar
  16. 16.
    Quartarone A, Rizzo V, Bagnato S, et al. Rapid-rate paired associative stimulation of the median nerve and motor cortex can produce long-lasting changes in motor cortical excitability in humans. J Physiol, 2006,575(Pt 2):657–670Google Scholar
  17. 17.
    Fratello F, Veniero D, Curcio G, et al. Modulation of corticospinal excitability by paired associative stimulation: reproducibility of effects and intraindividual reliability. Clin Neurophysiol, 2006,117(12):2667–2674Google Scholar
  18. 18.
    Müller JF, Orekhov Y, Liu Y, et al. Homeostatic plasticity in human motor cortex demonstrated by two consecutive sessions of paired associative stimulation. Eur J Neurosci, 2007,25(11):3461–3468Google Scholar
  19. 19.
    Sale MV, Ridding MC, Nordstrom MA. Factors influencing the magnitude and reproducibility of corticomotor excitability changes induced by paired associative stimulation. Exp Brain Res, 2007,181(4):615–626Google Scholar
  20. 20.
    Müller-Dahlhaus JF, OrekhovY Liu Y, et al. Interindividual variability and age-dependency of motor cortical plasticity induced by paired associative stimulation. Exp Brain Res, 2008,187(3):467–475Google Scholar
  21. 21.
    Mrachacz-Kersting N, Fong M, Murphy BA, et al. Changes in excitability of the cortical projections to the human tibialis anterior after paired associative stimulation. J Neurophysiol, 2007,97(3):1951–1958Google Scholar
  22. 22.
    Amaya F, Paulus W, Treue S, et al. Transcranial magnetic stimulation and PAS-induced cortical neuroplasticity in the awake rhesus monkey. Clin Neurophysiol, 2010,121(12):2143–2151Google Scholar
  23. 23.
    Heidegger T, Krakow K, Ziemann U. Effects of antiepileptic drugs on associative LTP-like plasticity in human motor cortex. Eur J Neurosci, 2010,32(7):1215–1222Google Scholar
  24. 24.
    Korchounov A, Ziemann U. Neuromodulatory neurotransmitters influence LTP-like plasticity in human cortex: a pharmaco-TMS study. Neuropsychopharmacology, 2011,36(9):1894–1902Google Scholar
  25. 25.
    Ilic NV, Milanovic S, Krstic J, et al. Homeostatic modulation of stimulation-dependent plasticity in human motor cortex. Physiol Res, 2011,60 Suppl 1:S107–S112Google Scholar
  26. 26.
    Voytovych H, Kriváneková L, Ziemann U. Lithium: A switch from LTD-to LTP-like plasticity in human cortex. Neuropharmacology, 2012,63(2):274–279Google Scholar
  27. 27.
    Prior MM, Stinear JW. Phasic spike-timingdependent plasticity of human motor cortex during walking. Brain Res, 2006,1110(1):150–158Google Scholar
  28. 28.
    Jayaram G, Santos L, Stinear JW. Spike-timingdependent plasticity induced in resting lower limb cortex persists during subsequent walking. Brain Res, 2007,1153:92–97Google Scholar
  29. 29.
    Shulga A, Lioumis P, Kirveskari E, et al. The use of F-response in defining interstimulus intervals appropriate for LTP-like plasticity induction in lower limb spinal paired associative stimulation. J Neurosci Methods, 2015,242:112–117Google Scholar
  30. 30.
    Shin H, Han T, Paik N. Effect of consecutive application of paired associative stimulation on motor recovery in a rat stroke model: a preliminary study. Int J Neurosci, 2009,118(6):807–820Google Scholar
  31. 31.
    Toleikis JR. Intraoperative monitoring using somatosensory evoked potentials. J Clin Monit Comput, 2005,19(3):241–258Google Scholar
  32. 32.
    Zhang YP, Shields LB, Zhang Y, et al. Use of magnetic stimulation to elicit motor evoked potentials, somatosensory evoked potentials, and H-reflexes in non-sedated rodents. J Neurosci Methods, 2007,165(1):9–17Google Scholar
  33. 33.
    Zhang S, Huang F, Gates M, et al. Somatosensory evoked potentials can be recorded on the midline of the skull with subdermal electrodes in non-sedated rats elicited by magnetic stimulation of the tibial nerve. J Neurosci Methods, 2012,208(2):114–118Google Scholar
  34. 34.
    Agrawal G, Kerr C, Thakor NV, et al. Characterization of graded multicenter animal spinal cord injury study contusion spinal cord injury using somatosensoryevoked potentials. Spine, 2010,35(11):1122–1127Google Scholar
  35. 35.
    Lee SY, Kim BR, Han EY. Association between evoked potentials and balance recovery in subacute hemiparetic stroke patients. Ann Rehabil Med, 2015,39(3):451–461Google Scholar
  36. 36.
    Hwang P, Sohn MK, Kim C, et al. Tibial somatosensory evoked potential can prognosticate for ambulatory function in subacute hemiplegic stroke. J Clin Neurosci, 2016,26:122–125Google Scholar
  37. 37.
    Sakatani K, Iizuka H, Young W. Somatosensory evoked potentials in rat cerebral cortex before and after middle cerebral artery occlusion. Stroke, 1990,21(1):124–132Google Scholar
  38. 38.
    Hendricks HT, Pasman JW, van Limbeek J, et al. Motor evoked potentials of the lower extremity in predicting motor recovery and ambulation after stroke: a cohort study. Arch Phys Med Rehabil, 2003,84(9):1373–1379Google Scholar
  39. 39.
    Kaelin-Lang A, Luft AR, Sawaki L, et al. Modulation of human corticomotor excitability by somatosensory input. J Physiol, 2002,540(2):623–633Google Scholar
  40. 40.
    Luft A, Kaelin-Lang A, Hauser T, et al. Modulation of rodent cortical motor excitability by somatosensory input. Exp Brain Res, 2002,142(4):562–569Google Scholar
  41. 41.
    Kim YH, You SH, Ko MH, et al. Repetitive transcranial magnetic stimulation-induced corticomotor excitability and associated motor skill acquisition in chronic stroke. Stroke, 2006,37(6):1471–1476Google Scholar
  42. 42.
    Takeuchi N, Tada T, Toshima M, et al. Inhibition of the unaffected motor cortex by 1 Hz repetitive transcranical magnetic stimulation enhances motor performance and training effect of the paretic hand in patients with chronic stroke. J Rehabil Med, 2008,40(4):298–303Google Scholar
  43. 43.
    Conforto AB, Ferreiro KN, Tomasi C, et al. Effects of somatosensory stimulation on motor function after subacute stroke. Neurorehabil Neural Repair, 2010,24(3):263–272Google Scholar
  44. 44.
    Yang L, Wang SH, Hu Y, et al. Effects of repetitive transcranial magnetic stimulation on astrocytes proliferation and nNOS expression in neuropathic pain rats. Curr Med Sci, 2018,38(3):482–490Google Scholar
  45. 45.
    Ridding MC, Taylor JL. Mechanisms of motorevoked potential facilitation following prolonged dual peripheral and central stimulation in humans. J Physiol, 2001,537(2):623–631Google Scholar
  46. 46.
    Bisio A, Avanzino L, Gueugneau N, et al. Observing and perceiving: a combined approach to induce plasticity in human motor cortex. Clin Neurophysiol, 2015,126(6):1212–1220Google Scholar

Copyright information

© Huazhong University of Science and Technology 2018

Authors and Affiliations

  • Xiang-yu Zhang
    • 1
    • 2
  • Yan-fang Sui
    • 1
    • 3
  • Tie-cheng Guo
    • 1
    Email author
  • Sai-hua Wang
    • 1
    • 4
  • Yan Hu
    • 1
    • 5
  • Yin-shan Lu
    • 1
  1. 1.Department of Rehabilitation Medicine, Tongji Hospital, Tongji Medical CollegeHuazhong University of Science and TechnologyWuhanChina
  2. 2.Department of Rehabilitation Medicinethe 5th Hospital of Zhengzhou UniversityZhengzhouChina
  3. 3.Department of Rehabilitation Medicinethe 1st People’s Hospital of HaikouHaikouChina
  4. 4.Department of Rehabilitation Medicinethe 1st Hospital of WuhanWuhanChina
  5. 5.Department of Rehabilitation Medicine, Zhongnan HospitalWuhan UniversityWuhanChina

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