Recovery cycles of posterior root-muscle reflexes evoked by transcutaneous spinal cord stimulation and of the H reflex in individuals with intact and injured spinal cord

Autoři: Ursula S. Hofstoetter aff001;  Brigitta Freundl aff002;  Heinrich Binder aff002;  Karen Minassian aff001
Působiště autorů: Center for Medical Physics and Biomedical Engineering, Medical University Vienna, Vienna, Austria aff001;  Neurological Center, Maria Theresien Schloessel, Otto Wagner Hospital, Vienna, Austria aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227057


Posterior root-muscle (PRM) reflexes are short-latency spinal reflexes evoked by epidural or transcutaneous spinal cord stimulation (SCS) in clinical and physiological studies. PRM reflexes share key physiological characteristics with the H reflex elicited by electrical stimulation of large-diameter muscle spindle afferents in the tibial nerve. Here, we compared the H reflex and the PRM reflex of soleus in response to transcutaneous stimulation by studying their recovery cycles in ten neurologically intact volunteers and ten individuals with traumatic, chronic spinal cord injury (SCI). The recovery cycles of the reflexes, i.e., the time course of their excitability changes, were assessed by paired pulses with conditioning-test intervals of 20–5000 ms. Between the subject groups, no statistical difference was found for the recovery cycles of the H reflexes, yet those of the PRM reflexes differed significantly, with a striking suppression in the intact group. When comparing the reflex types, they did not differ in the SCI group, while the PRM reflexes were more strongly depressed in the intact group for durations characteristic for presynaptic inhibition. These differences may arise from the concomitant stimulation of several posterior roots containing afferent fibers of various lower extremity nerves by transcutaneous SCS, producing multi-source heteronymous presynaptic inhibition, and the collective dysfunction of inhibitory mechanisms after SCI contributing to spasticity. PRM-reflex recovery cycles additionally obtained for bilateral rectus femoris, biceps femoris, tibialis anterior, and soleus all demonstrated a stronger suppression in the intact group. Within both subject groups, the thigh muscles showed a stronger recovery than the lower leg muscles, which may reflect a characteristic difference in motor control of diverse muscles. Based on the substantial difference between intact and SCI individuals, PRM-reflex depression tested with paired pulses could become a sensitive measure for spasticity and motor recovery.

Klíčová slova:

Depression – Electromyography – Functional electrical stimulation – Legs – Muscle analysis – Reflexes – Spinal cord injury


1. Minassian K, Jilge B, Rattay F, Pinter MM, Binder H, Gerstenbrand F, et al. Stepping-like movements in humans with complete spinal cord injury induced by epidural stimulation of the lumbar cord: electromyographic study of compound muscle action potentials. Spinal Cord. 2004;42: 401–416. doi: 10.1038/ 15124000

2. Minassian K, Persy I, Rattay F, Dimitrijevic MR, Hofer C, Kern H. Posterior root-muscle reflexes elicited by transcutaneous stimulation of the human lumbosacral cord. Muscle Nerve. 2007;35: 327–336. doi: 10.1002/mus.20700 17117411

3. Ladenbauer J, Minassian K, Hofstoetter US, Dimitrijevic MR, Rattay F. Stimulation of the human lumbar spinal cord with implanted and surface electrodes: A computer simulation study. IEEE Trans Neural Syst Rehabil Eng. 2010;18: 637–645. doi: 10.1109/TNSRE.2010.2054112 21138794

4. Hofstoetter US, Freundl B, Binder H, Minassian K. Common neural structures activated by epidural and transcutaneous lumbar spinal cord stimulation: Elicitation of posterior root-muscle reflexes. PLoS One. 2018;13: e0192013. doi: 10.1371/journal.pone.0192013 29381748

5. Rattay F, Minassian K, Dimitrijevic MR. Epidural electrical stimulation of posterior structures of the human lumbosacral cord: 2. quantitative analysis by computer modeling. Spinal Cord. 2000;38: 473–489. doi: 10.1038/ 10962608

6. Minassian K, Persy I, Rattay F, Pinter MM, Kern H, Dimitrijevic MR. Human lumbar cord circuitries can be activated by extrinsic tonic input to generate locomotor-like activity. Hum Mov Sci. 2007;26: 275–295. doi: 10.1016/j.humov.2007.01.005 17343947

7. Capogrosso M, Wenger N, Raspopovic S, Musienko P, Beauparlant J, Bassi Luciani L, et al. A computational model for epidural electrical stimulation of spinal sensorimotor circuits. J Neurosci. 2013;33: 19326–19340. doi: 10.1523/JNEUROSCI.1688-13.2013 24305828

8. Formento E, Minassian K, Wagner F, Mignardot JB, Le Goff-Mignardot CG, Rowald A, et al. Electrical spinal cord stimulation must preserve proprioception to enable locomotion in humans with spinal cord injury. Nat Neurosci. 2018;21: 1728–1741. doi: 10.1038/s41593-018-0262-6 30382196

9. Courtine G, Harkema SJ, Dy CJ, Gerasimenko YP, Dyhre-Poulsen P. Modulation of multisegmental monosynaptic responses in a variety of leg muscles during walking and running in humans. J Physiol. 2007;582: 1125–1139. doi: 10.1113/jphysiol.2007.128447 17446226

10. Sayenko DG, Angeli C, Harkema SJ, Edgerton VR, Gerasimenko YP. Neuromodulation of evoked muscle potentials induced by epidural spinal-cord stimulation in paralyzed individuals. J Neurophysiol. 2014;111: 1088–1099. doi: 10.1152/jn.00489.2013 24335213

11. Angeli CA, Boakye M, Morton RA, Vogt J, Benton K, Chen Y, et al. Recovery of Over-Ground Walking after Chronic Motor Complete Spinal Cord Injury. N Engl J Med. 2018;379: 1244–1250. doi: 10.1056/NEJMoa1803588 30247091

12. Gill ML, Grahn PJ, Calvert JS, Linde MB, Lavrov IA, Strommen JA, et al. Neuromodulation of lumbosacral spinal networks enables independent stepping after complete paraplegia. Nat Med. 2018;24: 1677–1682. doi: 10.1038/s41591-018-0175-7 30250140

13. Wagner FB, Mignardot J-B, Le Goff-Mignardot CG, Demesmaeker R, Komi S, Capogrosso M, et al. Targeted neurotechnology restores walking in humans with spinal cord injury. Nature. 2018;563: 65–71. doi: 10.1038/s41586-018-0649-2 30382197

14. Calvert JS, Grahn PJ, Strommen JA, Lavrov IA, Beck LA, Gill ML, et al. Electrophysiological Guidance of Epidural Electrode Array Implantation over the Human Lumbosacral Spinal Cord to Enable Motor Function after Chronic Paralysis. J Neurotrauma. 2019;36: 1451–1460. doi: 10.1089/neu.2018.5921 30430902

15. Murg M, Binder H, Dimitrijevic MR. Epidural electric stimulation of posterior structures of the human lumbar spinal cord: 1. muscle twitches—a functional method to define the site of stimulation. Spinal Cord. 2000;38: 394–402. doi: 10.1038/ 10962598

16. Minassian K, Hofstoetter US, Dzeladini F, Guertin PA, Ijspeert A. The Human Central Pattern Generator for Locomotion: Does It Exist and Contribute to Walking? Neuroscientist. 2017;23: 649–663. doi: 10.1177/1073858417699790 28351197

17. Hofstoetter US, Krenn M, Danner SM, Hofer C, Kern H, McKay WB, Mayr W, Minassian K. Augmentation of Voluntary Locomotor Activity by Transcutaneous Spinal Cord Stimulation in Motor-Incomplete Spinal Cord-Injured Individuals. Artif Organs. 2015;39:E176–186. doi: 10.1111/aor.12615 26450344

18. Minassian K, Hofstoetter US, Danner SM, Mayr W, Bruce JA, McKay WB, et al. Spinal rhythm generation by step-induced feedback and transcutaneous posterior root stimulation in complete spinal cord-injured individuals. Neurorehabil Neural Repair. 2016;30:233–243. doi: 10.1177/1545968315591706 26089308

19. Gad P, Gerasimenko Y, Zdunowski S, Turner A, Sayenko D, Lu DC, et al. Weight Bearing Over-ground Stepping in an Exoskeleton with Non-invasive Spinal Cord Neuromodulation after Motor Complete Paraplegia. Front Neurosci. 2017;11:333. doi: 10.3389/fnins.2017.00333 28642680

20. Sayenko DG, Rath M, Ferguson AR, Burdick JW, Havton LA, Edgerton VR, et al. Self-Assisted Standing Enabled by Non-Invasive Spinal Stimulation after Spinal Cord Injury. J Neurotrauma. 2019;36: 1435–1450. doi: 10.1089/neu.2018.5956 30362876

21. Hofstoetter U, Freundl B, Danner S, Krenn M, Mayr W, Binder H, et al. Transcutaneous spinal cord stimulation induces temporary attenuation of spasticity in individuals with spinal cord injury. J Neurotrauma. 2019 Aug 9. doi: 10.1089/neu.2019.6588 31333064

22. Hofstoetter US, Minassian K, Hofer C, Mayr W, Rattay F, Dimitrijevic MR. Modification of reflex responses to lumbar posterior root stimulation by motor tasks in healthy subjects. Artif Organs. 2008;32: 644–648. doi: 10.1111/j.1525-1594.2008.00616.x 18782137

23. Saito A, Masugi Y, Nakagawa K, Obata H, Nakazawa K. Repeatability of spinal reflexes of lower limb muscles evoked by transcutaneous spinal cord stimulation. Tremblay F, editor. PLoS One. 2019;14: e0214818. doi: 10.1371/journal.pone.0214818 30947310

24. Milosevic M, Masugi Y, Obata H, Sasaki A, Popovic MR, Nakazawa K. Short-term inhibition of spinal reflexes in multiple lower limb muscles after neuromuscular electrical stimulation of ankle plantar flexors. Exp Brain Res. 2019;237: 467–476. doi: 10.1007/s00221-018-5437-6 30460394

25. Andrews JC, Stein RB, Roy FD. Reduced postactivation depression of soleus H reflex and root evoked potential after transcranial magnetic stimulation. J Neurophysiol. 2015;114: 485–492. doi: 10.1152/jn.01007.2014 25995355

26. Minassian K, Hofstoetter US, Rattay F. Transcutaneous lumbar posterior root stimulation for motor control studies and modification of motor activity after spinal cord injury. In: Dimitrijevic M, Kakulas B, McKay W, Vrbova G, editors. Restorative neurology of spinal cord injury. New York: Oxford University Press; 2011. pp. 226–255.

27. Hoffmann P. Beiträge zur Kenntnis der menschlichen Reflexe mit besonderer Berücksichtigung der elektrischen Erscheinungen. Arch Anat Physiol. 1910;1: 223–246.

28. Hoffmann P. Über die Beziehungen der Sehnenreflexe zur willkürlichen Bewegung und zum Tonus. Z Biol. 1918;68: 351–370.

29. Magladery JW, McDougal DB. Electrophysiological studies of nerve and reflex activity in normal man. I. Identification of certain reflexes in the electromyogram and the conduction velocity of peripheral nerve fibers. Bull Johns Hopkins Hosp. 1950;86: 265–290. 15414383

30. Burke D, Gandevia SC, McKeon B. The afferent volleys responsible for spinal proprioceptive reflexes in man. J Physiol. 1983;339: 535–552. doi: 10.1113/jphysiol.1983.sp014732 6887033

31. Burke D, Gandevia SC, McKeon B. Monosynaptic and oligosynaptic contributions to human ankle jerk and H-reflex. J Neurophysiol. 1984;52: 435–448. doi: 10.1152/jn.1984.52.3.435 6090608

32. Magladery JW, Porter WE, Park AM, Teasdall RD. Electrophysiological studies of nerve and reflex activity in normal man. IV. The two-neurone reflex and identification of certain action potentials from spinal roots and cord. Bull Johns Hopkins Hosp. 1951;88: 499–519. 14839348

33. Katz R. Presynaptic inhibition in humans: a comparison between normal and spastic patients. J Physiol Paris. 1999;93: 379–385. doi: 10.1016/s0928-4257(00)80065-0 10574126

34. Dy CJ, Gerasimenko YP, Edgerton VR, Dyhre-Poulsen P, Courtine G, Harkema SJ. Phase-dependent modulation of percutaneously elicited multisegmental muscle responses after spinal cord injury. J Neurophysiol. 2010;103: 2808–2820. doi: 10.1152/jn.00316.2009 20357075

35. Hoffmann P. Untersuchungen über die refraktäre Periode des menschlichen Rückenmarks. Z Biol. 1924;81: 37–48.

36. Schenck E. [Studies on the silent period following a bineuronal (proprioreceptive) reflex in man]. Pflugers Arch Gesamte Physiol Menschen Tiere. 1951;253: 286–300. doi: 10.1007/bf00363395 14833863

37. Paillard J. Réflexes et Régulations d’Origine Proprioceptive chez l’Homme. Etude Neurophysiologique et Psychophysiologique. Paris: Librairie Arnette; 1955.

38. Magladery J, Teasdall R, Park A, Porter W. Electrophysiological studies of nerve and reflex activity in normal man. V. Excitation and inhibition of two-neurone reflexes by afferent impulses in the same trunk. Bull Johns Hopkins Hosp. 1951;88: 520–537. 14839349

39. Olsen PZ, Diamantopoulos E. Excitability of spinal motor neurones in normal subjects and patients with spasticity, Parkinsonian rigidity, and cerebellar hypotonia. J Neurol Neurosurg Psychiatry. 1967;30: 325–331. doi: 10.1136/jnnp.30.4.325 6055341

40. Schieppati M. The Hoffmann reflex: a means of assessing spinal reflex excitability and its descending control in man. Prog Neurobiol. 1987;28: 345–376. doi: 10.1016/0301-0082(87)90007-4 3588965

41. Minassian K, Hofstoetter U, Rattay F, Mayr W, Dimitirjevic M. Posterior root-muscle reflexes and the H reflex in humans: Electrophysiological comparison. Neuroscience Meeting Planner, Chicago, IL: Society for Neuroscience (online). 2009. Program No. 658.12.

42. Andrews JC, Stein RB, Roy FD. Post-activation depression in the human soleus muscle using peripheral nerve and transcutaneous spinal stimulation. Neurosci Lett. 2015;589: 144–149. doi: 10.1016/j.neulet.2015.01.041 25600855

43. Eccles JC, Schmidt RF, Willis WD. Presynaptic inhibition of the spinal monosynaptic reflex pathway. J Physiol. 1962;161: 282–297. doi: 10.1113/jphysiol.1962.sp006886 13889059

44. Iles JF, Roberts RC. Inhibition of monosynaptic reflexes in the human lower limb. J Physiol. 1987;385: 69–87. doi: 10.1113/jphysiol.1987.sp016484 2958622

45. Crone C, Nielsen J. Methodological implications of the post activation depression of the soleus H-reflex in man. Exp Brain Res. 1989;78: 28–32. doi: 10.1007/bf00230683 2591515

46. Hultborn H, Illert M, Nielsen J, Paul A, Ballegaard M, Wiese H. On the mechanism of the post-activation depression of the H-reflex in human subjects. Exp Brain Res. 1996;108: 450–462. doi: 10.1007/bf00227268 8801125

47. Nielsen J, Petersen N, Ballegaard M, Biering-Sørensen F, Kiehn O. H-reflexes are less depressed following muscle stretch in spastic spinal cord injured patients than in healthy subjects. Exp Brain Res. 1993;97: 173–176. doi: 10.1007/bf00228827 8131827

48. Faist M, Mazevet D, Dietz V, Pierrot-Deseilligny E. A quantitative assessment of presynaptic inhibition of Ia afferents in spastics. Differences in hemiplegics and paraplegics. Brain A J Neurol. 1994;117: 1449–1455.

49. Schindler-Ivens S, Shields RK. Low frequency depression of H-reflexes in humans with acute and chronic spinal-cord injury. Exp Brain Res. 2000;133: 233–241. doi: 10.1007/s002210000377 10968224

50. Nielsen J, Willerslev-Olsen M, Lorentzen J. Pathophysiology of Spasticity. In: Pandyan A, Hermens H, Conway B, editors. Neurological Rehabilitation Spasticity and Contractures in Clinical Practice and Research. Boca Raton: Imprint CRC Press; 2018. pp. 25–57.

51. Elbasiouny SM, Moroz D, Bakr MM, Mushahwar VK. Management of spasticity after spinal cord injury: current techniques and future directions. Neurorehabil Neural Repair. 2010;24: 23–33. doi: 10.1177/1545968309343213 19723923

52. Grey MJ, Klinge K, Crone C, Lorentzen J, Biering-Sørensen F, Ravnborg M, et al. Post-activation depression of soleus stretch reflexes in healthy and spastic humans. Exp Brain Res. 2008;185: 189–197. doi: 10.1007/s00221-007-1142-6 17932663

53. Bergmans J, Delwaide PJ, Gadea-Ciria M. Short-latency effects of low-threshold muscular afferent fibers on different motoneuronal pools of the lower limb in man. Exp Neurol. 1978;60: 380–385. doi: 10.1016/0014-4886(78)90091-2 658210

54. Pierrot-Deseilligny E, Burke D. The Circuitry of the Human Spinal Cord. Cambridge: Cambridge University Press; 2012.

55. Delwaide PJ, Cordonnier M, Charlier M. Functional relationships between myotatic reflex arcs of the lower limb in man: investigation by excitability curves. J Neurol Neurosurg Psychiatry. 1976;39: 545–554. doi: 10.1136/jnnp.39.6.545 950566

56. Lamy JC, Wargon I, Baret M, Ben Smail D, Milani P, Raoul S, et al. Post-activation depression in various group I spinal pathways in humans. Exp Brain Res. 2005;166: 248–262. doi: 10.1007/s00221-005-2360-4 16078020

57. Kirshblum S, Waring W. Updates for the International Standards for Neurological Classification of Spinal Cord Injury. Phys Med Rehabil Clin N Am. 2014;25: 505–517. doi: 10.1016/j.pmr.2014.04.001 25064785

58. Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther. 1987;67: 206–207. doi: 10.1093/ptj/67.2.206 3809245

59. Hulme A, MacLennan WJ, Ritchie RT, John VA, Shotton PA. Baclofen in the elderly stroke patient its side-effects and pharmacokinetics. Eur J Clin Pharmacol. 1985;29: 467–469. doi: 10.1007/bf00613463 3912190

60. Tse FL, Jaffe JM, Bhuta S. Pharmacokinetics of orally administered tizanidine in healthy volunteers. Fundam Clin Pharmacol. 1987;1: 479–488. doi: 10.1111/j.1472-8206.1987.tb00581.x 3447935

61. Mathias CJ, Luckitt J, Desai P, Baker H, el Masri W, Frankel HL. Pharmacodynamics and pharmacokinetics of the oral antispastic agent tizanidine in patients with spinal cord injury. J Rehabil Res Dev. 1989;26: 9–16. 2600869

62. Shellenberger MK, Groves L, Shah J, Novack GD. A controlled pharmacokinetic evaluation of tizanidine and baclofen at steady state. Drug Metab Dispos. 1999;27: 201–204. 9929503

63. Malanga G, Reiter RD, Garay E. Update on tizanidine for muscle spasticity and emerging indications. Expert Opin Pharmacother. 2008;9: 2209–2215. doi: 10.1517/14656566.9.12.2209 18671474

64. Baumgärtner MG, Cautreels W, Langenbahn H. Biotransformation and pharmacokinetics of tetrazepam in man. Arzneimittelforschung. 1984;34: 724–729. 6148954

65. Bun H, Philip F, Berger Y, Necciari J, Al-Mallah NR, Serradimign A, et al. Plasma levels and pharmacokinetics of single and multiple dose of tetrazepam in healthy volunteers. Arzneimittelforschung. 1987;37: 199–202. 2883980

66. Delwaide PJ, Pennisi G. Tizanidine and electrophysiologic analysis of spinal control mechanisms in humans with spasticity. Neurology. 1994;44: S21–27. 7970007

67. Pierrot-Deseilligny E, Mazevet D. The monosynaptic reflex: a tool to investigate motor control in humans. Interest and limits. Clin Neurophysiol. 2000;30: 67–80.

68. Knikou M. The H-reflex as a probe: pathways and pitfalls. J Neurosci Methods. 2008;171: 1–12. doi: 10.1016/j.jneumeth.2008.02.012 18394711

69. Kohn AF, Floeter MK, Hallett M. Presynaptic inhibition compared with homosynaptic depression as an explanation for soleus H-reflex depression in humans. Exp Brain Res. 1997;116: 375–380. doi: 10.1007/pl00005765 9348136

70. Kagamihara Y, Hayashi A, Okuma Y, Nagaoka M, Nakajima Y, Tanaka R. Reassessment of H-reflex recovery curve using the double stimulation procedure. Muscle Nerve. 1998;21: 352–360. doi: 10.1002/(sici)1097-4598(199803)21:3<352::aid-mus9>;2-9 9486864

71. Morita H, Shindo M, Yanagawa S, Yanagisawa N. Neuromuscular response in man to repetitive nerve stimulation. Muscle Nerve. 1993;16: 648–654. doi: 10.1002/mus.880160611 8389002

72. Kiernan MC, Mogyoros I, Burke D. Differences in the recovery of excitability in sensory and motor axons of human median nerve. Brain A J Neurol. 1996;119: 1099–1105.

73. Eccles JC, Fatt P, Koketsu K. Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurones. J Physiol. 1954;126: 524–562. doi: 10.1113/jphysiol.1954.sp005226 13222354

74. Beswick F, Evanson J. Homosynaptic depression of the monosynaptic reflex following its activation. J Physiol. 1957;135: 400–411. doi: 10.1113/jphysiol.1957.sp005719 13406749

75. Kuno M. Mechanism of facilitation and depression of the excitatory synaptic potential in spinal motoneurons. J Physiol. 1964;175: 100–112. doi: 10.1113/jphysiol.1964.sp007505 14241151

76. Shimamura M, Mori S, Matsushima S, Fujimori B. On the spino-bulbo-spinal reflex in dogs, monkeys and man. Jpn J Physiol. 1964;14: 411–421. doi: 10.2170/jjphysiol.14.411 14200821

77. Taborikova H, Provini L, Decandia M. Evidence that muscle stretch evokes long-loop reflexes from higher centres. Brain Res. 1966;2: 192–194. doi: 10.1016/0006-8993(66)90026-6 5968923

78. Taborikova H, Sax DS. Conditioning of H-reflexes by a preceding subthreshold H-reflex stimulus. Brain A J Neurol. 1969;92: 203–212.

79. Bianconi R, Granit R, Reis DJ. The effect of extensor muscle spindles and tendon organs on homonymous motoneurones in relation to gamma-bias and curarization. Acta Physiol Scand. 1964;61: 331–347. 14209252

80. Nakazawa K, Kawashima N, Akai M. Enhanced stretch reflex excitability of the soleus muscle in persons with incomplete rather than complete chronic spinal cord injury. Arch Phys Med Rehabil. 2006;87: 71–75. doi: 10.1016/j.apmr.2005.08.122 16401441

81. Calancie B, Broton JG, Klose KJ, Traad M, Difini J, Ayyar DR. Evidence that alterations in presynaptic inhibition contribute to segmental hypo- and hyperexcitability after spinal cord injury in man. Electroencephalogr Clin Neurophysiol. 1993;89: 177–186. doi: 10.1016/0168-5597(93)90131-8 7686850

82. Ishikawa K, Ott K, Porter RW, Stuart D. Low frequency depression of the H wave in normal and spinal man. Exp Neurol. 1966;15: 140–156. doi: 10.1016/0014-4886(66)90039-2 5934660

83. Cisi RRL, Kohn AF. H-reflex depression simulated by a biologically realistic motoneuron network. Conf Proc IEEE Eng Med Biol Soc. 2007;2007: 2713–2716. doi: 10.1109/IEMBS.2007.4352889 18002555

84. Kohn AF, Floeter MK, Hallett M. A model-based approach for the quantification of H reflex depression in humans. Conf Proc IEEE Eng Med Biol Soc. 1995;1995: 1233–1234.

85. Diamantopoulos E, Zander Olsen P. Excitability of motor neurones in spinal shock in man. J Neurol Neurosurg Psychiatry. 1967;30: 427–431. doi: 10.1136/jnnp.30.5.427 6062993

86. Zhu Y, Starr A, Haldeman S, Chu JK, Sugerman RA. Soleus H-reflex to S1 nerve root stimulation. Electroencephalogr Clin Neurophysiol. 1998;109: 10–14. doi: 10.1016/s0924-980x(97)00058-1 11003059

87. Kitano K, Koceja DM. Spinal reflex in human lower leg muscles evoked by transcutaneous spinal cord stimulation. J Neurosci Methods. 2009;180: 111–115. doi: 10.1016/j.jneumeth.2009.03.006 19427537

88. Danner SM, Hofstoetter US, Ladenbauer J, Rattay F, Minassian K. Can the Human Lumbar Posterior Columns Be Stimulated by Transcutaneous Spinal Cord Stimulation? A Modeling Study. Artif Organs. 2011;35: 257–262. doi: 10.1111/j.1525-1594.2011.01213.x 21401670

89. Lang J, Geisel U. [Lumbosacral part of the dural sac and the topography of its contents]. Morphol Med. 1983;3: 27–46. 6877253

90. Hultborn H, Meunier S, Morin C, Pierrot-Deseilligny E. Assessing changes in presynaptic inhibition of I a fibres: a study in man and the cat. J Physiol. 1987;389: 729–756. doi: 10.1113/jphysiol.1987.sp016680 3681741

91. Meunier S, Penicaud A, Pierrot-Deseilligny E, Rossi A. Monosynaptic Ia excitation and recurrent inhibition from quadriceps to ankle flexors and extensors in man. J Physiol. 1990;423: 661–675. doi: 10.1113/jphysiol.1990.sp018046 2388162

92. Meunier S, Pierrot-Deseilligny E, Simonetta M. Pattern of monosynaptic heteronymous Ia connections in the human lower limb. Exp Brain Res. 1993;96: 534–544. doi: 10.1007/bf00234121 8299754

93. Morin C, Pierrot-Deseilligny E, Hultborn H. Evidence for presynaptic inhibition of muscle spindle Ia afferents in man. Neurosci Lett. 1984;44: 137–142. doi: 10.1016/0304-3940(84)90071-5 6231494

94. Nielsen J, Petersen N. Is presynaptic inhibition distributed to corticospinal fibres in man? J Physiol. 1994;477: 47–58. doi: 10.1113/jphysiol.1994.sp020170 8071888

95. Nielsen J, Petersen N, Crone C. Changes in transmission across synapses of Ia afferents in spastic patients. Brain A J Neurol. 1995;118: 995–1004.

96. Mizuno Y, Tanaka R, Yanagisawa N. Reciprocal group I inhibition on triceps surae motoneurons in man. J Neurophysiol. 1971;34: 1010–1017. doi: 10.1152/jn.1971.34.6.1010 4329961

97. Morita H, Crone C, Christenhuis D, Petersen NT, Nielsen JB. Modulation of presynaptic inhibition and disynaptic reciprocal Ia inhibition during voluntary movement in spasticity. Brain A J Neurol. 2001;124: 826–837.

98. Mao CC, Ashby P, Wang M, McCrea D. Synaptic connections from large muscle afferents to the motoneurons of various leg muscles in man. Exp Brain Res. 1984;56: 341–350. doi: 10.1007/bf00236290 6090196

99. Hofstoetter US, McKay WB, Tansey KE, Mayr W, Kern H, Minassian K. Modification of spasticity by transcutaneous spinal cord stimulation in individuals with incomplete spinal cord injury. J Spinal Cord Med. 2014;37: 202–211. doi: 10.1179/2045772313Y.0000000149 24090290

100. Estes SP, Iddings JA, Field-Fote EC. Priming Neural Circuits to Modulate Spinal Reflex Excitability. Front Neurol. 2017;8: 17. doi: 10.3389/fneur.2017.00017 28217104

Článek vyšel v časopise


2019 Číslo 12