Repeated transspinal stimulation decreases soleus H-reflex excitability and restores spinal inhibition in human spinal cord injury
Autoři:
Maria Knikou aff001; Lynda M. Murray aff001
Působiště autorů:
Klab4Recovery Research Laboratory, Department of Physical Therapy, College of Staten Island, The City University of New York, Staten Island, New York, United States of America
aff001; PhD Program in Biology and Collaborative Neuroscience Program, Graduate Center of The City University of New York, New York, New York, United States of America
aff002
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0223135
Souhrn
Transcutaneous spinal cord or transspinal stimulation over the thoracolumbar enlargement, the spinal location of motoneurons innervating leg muscles, modulates neural circuits engaged in the control of movement. The extent to which daily sessions (e.g. repeated) of transspinal stimulation affects soleus H-reflex excitability in individuals with chronic spinal cord injury (SCI) remains largely unknown. In this study, we established the effects of repeated cathodal transspinal stimulation on soleus H-reflex excitability and spinal inhibition in individuals with and without chronic SCI. Ten SCI and 10 healthy control subjects received monophasic transspinal stimuli of 1-ms duration at 0.2 Hz at subthreshold and suprathreshold intensities of the right soleus transspinal evoked potential (TEP). SCI subjects received an average of 16 stimulation sessions, while healthy control subjects received an average of 10 stimulation sessions. Before and one or two days post intervention, we used the soleus H reflex to assess changes in motoneuron recruitment, homosynaptic depression following single tibial nerve stimuli delivered at 0.1, 0.125, 0.2, 0.33 and 1.0 Hz, and postactivation depression following paired tibial nerve stimuli at the interstimulus intervals of 60, 100, 300, and 500 ms. Soleus H-reflex excitability was decreased in both legs in motor incomplete and complete SCI but not in healthy control subjects. Soleus H-reflex homosynaptic and postactivation depression was present in motor incomplete and complete SCI but was of lesser strength to that observed in healthy control subjects. Repeated transspinal stimulation increased homosynaptic depression in all SCI subjects and remained unaltered in healthy controls. Postactivation depression remained unaltered in all subject groups. Lastly, transspinal stimulation decreased the severity of spasms and ankle clonus. The results indicate decreased reflex hyperexcitability and recovery of spinal inhibitory control in the injured human spinal cord with repeated transspinal stimulation. Transspinal stimulation is a noninvasive neuromodulation method for restoring spinally-mediated afferent reflex actions after SCI in humans.
Klíčová slova:
Electrodes – Neurophysiology – Functional electrical stimulation – Depression – Legs – Ankles – Reflexes – Spinal cord injury
Zdroje
1. Knikou M, Conway BA. Reflex effects of induced muscle contraction in normal and spinal cord injured subjects. Muscle Nerve 2002; 26: 374–382. doi: 10.1002/mus.10206 12210367
2. Knikou M, Conway BA. Effects of electrically induced muscle contraction on flexion reflex in human spinal cord injury. Spinal Cord 2005; 43: 640–648. doi: 10.1038/sj.sc.3101772 15968304
3. Christiansen L, Perez MA. Targeted-plasticity in the corticospinal tract after human spinal cord injury. Neurotherapeutics 2018; 15: 618–627. doi: 10.1007/s13311-018-0639-y 29946981
4. Dimitrijevic MR, Gerasimenko Y, Pinter MM. Evidence for a spinal central pattern generator in humans. Ann N Y Acad Sci. 1998; 860: 360–376. doi: 10.1111/j.1749-6632.1998.tb09062.x 9928325
5. Harkema S, Gerasimenko Y, Hodes J, Burdick J, Angeli C, Chen Y. 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. 2011; 377: 1938–1947. doi: 10.1016/S0140-6736(11)60547-3 21601270
6. Hofstoetter US, Knikou M, Guertin PA, Minassian K. Probing the human spinal locomotor circuits by phasic step-induced feedback and by tonic electrical and pharmacological neuromodulation. Curr Pharm Des. 2017; 23: 1805–1820. doi: 10.2174/1381612822666161214144655 27981912
7. Knikou M. Neurophysiological characterization of transpinal evoked potentials in human leg muscles. Bioelectromagnetics. 2013; 34: 630–640. doi: 10.1002/bem.21808 24115026
8. Knikou M, Dixon L, Santora D, Ibrahim MM. Transspinal constant-current long-lasting stimulation: a new method to induce cortical and corticospinal plasticity. J Neurophysiol. 2015; 114: 1486–1499. doi: 10.1152/jn.00449.2015 26108955
9. Sayenko DG, Atkinson DA, Dy CJ, Gurley KM, Smith VL, Angeli C, et al. Spinal segment-specific transcutaneous stimulation differentially shapes activation pattern among motor pools in humans. J Appl Physiol. 2015; 118: 1364–1374. doi: 10.1152/japplphysiol.01128.2014 25814642
10. Murray LM, Knikou M. Transspinal stimulation increases motoneuron output of multiple segments in human spinal cord injury. PLoS One. 2019; 14(3): e0213696. doi: 10.1371/journal.pone.0213696 30845251
11. Knikou M, Murray LM. Neural interactions between transspinal evoked potentials and muscle spindle afferents in humans. J Electromyogr Kinesiol. 2018; 43: 174–183. doi: 10.1016/j.jelekin.2018.10.005 30352388
12. Hofstoetter US, Krenn M, Danner SM, Hofer C, Kern H, McKay WB, et al. Augmentation of voluntary locomotor activity by transcutaneous spinal cord stimulation in motor-incomplete spinal cord-injured individuals. Artif Organs. 2015; 39: 176–186.
13. 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
14. 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/sj.sc.3101615 15124000
15. Elbasiouny SM, Mushahwar VK. Modulation of motoneuronal firing behavior after spinal cord injury using intraspinal microstimulation current pulses: a modeling study. J Appl Physiol. 2007; 103: 276–286. doi: 10.1152/japplphysiol.01222.2006 17234800
16. Elbasiouny SM, Mushahwar VK. Suppressing the excitability of spinal motoneurons by extracellularly applied electrical fields: insights from computer simulations. J Appl Physiol. 2007; 103: 1824–1836. doi: 10.1152/japplphysiol.00362.2007 17702836
17. Murray LM, Knikou M. Remodeling brain activity by repetitive cervicothoracic transspinal stimulation after human spinal cord injury. Front Neurol. 2017; 8: 50. doi: 10.3389/fneur.2017.00050 28265259
18. Knikou M. Transpinal and transcortical stimulation alter corticospinal excitability and increase spinal output. PLoS One. 2014; 9(7): e102313. doi: 10.1371/journal.pone.0102313 25007330
19. Knikou M. Plantar cutaneous input modulates differently spinal reflexes in subjects with intact and injured spinal cord. Spinal Cord. 2007; 45: 69–77. doi: 10.1038/sj.sc.3101917 16534501
20. 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
21. Adams MM, Ginis KA, Hicks AL. The spinal cord injury spasticity evaluation tool: development and evaluation. Arch Phys Med Rehab. 2007; 88: 1185–1192. doi: 10.1016/j.apmr.2007.06.012 17826466
22. Savic G, Bergstrom EMK, Frankel HL, Jamous MA, Jones PW. Inter-rater reliability of motor and sensory examinations performed according to American Spinal Injury Association standards. Spinal Cord. 2007; 45: 444–451. doi: 10.1038/sj.sc.3102044 17387316
23. Klimstra M, Zehr EP. A sigmoid function is the best fit for the ascending limb of the Hoffmann reflex recruitment curve. Exp Brain Res. 2008; 186: 93–105. doi: 10.1007/s00221-007-1207-6 18046545
24. Smith AC, Rymer WZ, Knikou M. Locomotor training modifies soleus monosynaptic motoneuron responses in human spinal cord injury. Exp Brain Res. 2015; 233: 89–103. doi: 10.1007/s00221-014-4094-7 25205562
25. 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
26. Eccles JC, Rall W. Effects induced in a monosynaptic reflex path by its activation. J Neurophysiol. 1951; 14: 353–376. doi: 10.1152/jn.1951.14.5.353 14861671
27. 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
28. 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
29. Katz R, Morin C, Pierrot-Deseilligny E, Hibino R. Conditioning of H reflex by a preceding subthreshold tendon reflex stimulus. J Neurol Neurosurg Psychiatry. 1977; 40: 575–580. doi: 10.1136/jnnp.40.6.575 903772
30. 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
31. Côté MP, Murray LM, Knikou M. Spinal control of locomotion: individual neurons, their circuits and functions. Front Physiol. 2018; 9: 784. doi: 10.3389/fphys.2018.00784 29988534
32. Lin S, Li Y, Lucas-Osma AM, Hari K, Stephens MJ, Singla R, et al. Locomotor-related V3 interneurons initiate and coordinate muscles spasms after spinal cord injury. J Neurophysiol. 2019; 121: 1352–1367. doi: 10.1152/jn.00776.2018 30625014
33. Aymard C, Katz R, Lafitte C, Lo E, Pénicaud A, Pradat-Diehl P, et al. Presynaptic inhibition and homosynaptic depression: a comparison between lower and upper limbs in normal human subjects and patients with hemiplegia. Brain. 2000; 123: 1688–1702. doi: 10.1093/brain/123.8.1688 10908198
34. 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
35. Knikou M. Hip-phase-dependent flexion reflex modulation and expression of spasms in patients with spinal cord injury. Exp Neurol. 2007; 204: 171–181. doi: 10.1016/j.expneurol.2006.10.006 17125766
36. Norton JA, Bennett DJ, Knash ME, Murray KC, Gorassini MA. Changes in sensory-evoked synaptic activation of motoneurons after spinal cord injury in man. Brain. 2008; 131: 1478–1491. doi: 10.1093/brain/awn050 18344559
37. D’Amico JM, Murray KC, Li Y, Chan KM, Finlay MG, Bennett DJ, et al. Constitutively active 5-HT2/α1 receptors facilitate muscle spasms after human spinal cord injury. J Neurophysiol. 2013; 109:1473–1484. doi: 10.1152/jn.00821.2012 23221402
38. ElBasiouny SM, Schuster JE, Heckman CJ. Persistent inward currents in spinal motoneurons: important for normal function but potentially harmful after spinal cord injury and in amyotrophic lateral sclerosis. Clin Neurophysiol. 2010; 121: 1669–1679. doi: 10.1016/j.clinph.2009.12.041 20462789
39. Kim H. Impact of the localization of dendritic calcium persistent inward current on the input-output properties of spinal motoneuron pool: a computational study. J Appl Physiol. 2017; 123: 1166–1187. doi: 10.1152/japplphysiol.00034.2017 28684585
40. Hunter JP, Ashby P. Segmental effects of epidural spinal cord stimulation in humans. J Physiol. 1994; 474: 407–419. doi: 10.1113/jphysiol.1994.sp020032 8014902
41. Tsentsevitsky A, Nurullin L, Nikolsky E, Malomouzh A. Metabotropic and ionotropic glutamate receptors mediate the modulation of acetylcholine release at the frog neuromuscular junction. J Neurosci Res. 2017; 95: 1391–1401. doi: 10.1002/jnr.23977 27770577
42. Trussell LO, Zhang S, Raman IM. Desensitization of AMPA receptors upon multiquantal neurotransmitter release. Neuron. 1993; 10: 1185–1196. doi: 10.1016/0896-6273(93)90066-z 7686382
43. Frischknecht R, Heine M, Perrais D, Seidenbecher CI, Choquet D, Gundelfinger ED. Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat Neurosci. 2009; 12: 897–904. doi: 10.1038/nn.2338 19483686
44. Eccles JC, O’Connor WJ. Abortive impulses at the neuro-muscular junction. J Physiol Lond. 1941; 100: 318–328. doi: 10.1113/jphysiol.1941.sp003945 16991529
45. Bergmans J. Spontaneous activity of single nerve fibres induced by repetitive activation. Arch Int Physiol Biochim. 1969; 77: 354–356. 4184318
46. Táboriková H, Sax DS. Conditioning of H-reflexes by a preceding subthreshold H-reflex stimulus. Brain. 1969; 92: 203–212. doi: 10.1093/brain/92.1.203 5774028
47. Eccles JC, Sasaki K, Strata P. Interpretation of the potential fields generated in the cerebellar cortex by a mossy fibre volley. Exp Brain Res. 1967; 3: 58–80. doi: 10.1007/bf00234470 6031000
48. Chofflon M, Lachat JM, Rüegg DG. A transcortical loop demonstrated by stimulation of low-threshold muscle afferents in the awake monkey. J Physiol Lond. 1982; 323: 393–402. doi: 10.1113/jphysiol.1982.sp014079 7097578
49. Knikou M, Mummidisetty CK. Locomotor training improves premotoneuronal control after chronic spinal cord injury. J Neurophysiol. 2014; 111: 2264–2275. doi: 10.1152/jn.00871.2013 24598526
50. Knikou M. Functional reorganization of soleus H-reflex modulation during stepping after robotic-assisted step training in people with complete and incomplete spinal cord injury. Exp Brain Res. 2013; 228: 279–296. doi: 10.1007/s00221-013-3560-y 23708757
51. Knikou M. Neural control of locomotion and training-induced plasticity after spinal and cerebral lesions. Clin Neurophysiol. 2010; 121: 1655–1668. doi: 10.1016/j.clinph.2010.01.039 20427232
52. Côté MP, Azzam GA, Lemay MA, Zhukareva V, Houlé JD. Activity-dependent increase in neurotrophic factors is associated with an enhanced modulation of spinal reflexes after spinal cord injury. J Neurotrauma. 2011; 28: 299–309. doi: 10.1089/neu.2010.1594 21083432
53. Côté MP, Gandhi S, Zambrotta M, Houlé JD. Exercise modulates chloride homeostasis after spinal cord injury. J Neurosci. 2014; 34: 8976–8987. doi: 10.1523/JNEUROSCI.0678-14.2014 24990918
54. Wang Y, Pillai S, Wolpaw JR, Chen XY. Motor learning changes GABAergic terminals on spinal motoneurons in normal rats. Eur J Neurosci. 2006; 23: 141–150. doi: 10.1111/j.1460-9568.2005.04547.x 16420424
55. Wang Y, Pillai S, Wolpaw JR, Chen XY. H-reflex down-conditioning greatly increases the number of identifiable GABAergic interneurons in rat ventral horn. Neurosci Lett. 2009; 452: 124–129. doi: 10.1016/j.neulet.2009.01.054 19383426
56. Thompson AK, Pomerantz FR, Wolpaw JR. Operant conditioning of a spinal reflex can improve locomotion after spinal cord injury in humans. J Neurosci. 2013; 33: 2365–2375. doi: 10.1523/JNEUROSCI.3968-12.2013 23392666
Článok vyšiel v časopise
PLOS One
2019 Číslo 9
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania