Does trans-spinal direct current stimulation alter phrenic motoneurons and respiratory neuromechanical outputs in humans? A double-blind, Sham-controlled, Randomized, Crossover study

Journal of Neuroscience

Volumn 34, Issue 43, 2014, Pages 14420-14429

  Niérat, Marie CéCile ^b   Similowski, Thomas ^a,b,c   Lamy, Jean Charles ^a  

^a SORBONNE UNIVERSITÉ   (France)

^b INSERM   (France)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

humans; phrenic motoneurons; plasticity; spinal DC stimulation

Indexed keywords

ACTION POTENTIAL; ADULT; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BREATHING; ELECTROCARDIOGRAPHY; ELECTROMYOGRAPHY; EVOKED MUSCLE RESPONSE; FEMALE; HEART RATE VARIABILITY; HUMAN; HUMAN EXPERIMENT; MALE; MOTONEURON; MUSCLE ACTION POTENTIAL; NERVE CELL PLASTICITY; NORMAL HUMAN; PLETHYSMOGRAPHY; RANDOMIZED CONTROLLED TRIAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); RESPIRATION CONTROL; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION; BREATHING MECHANICS; CONTROLLED STUDY; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; MIDDLE AGED; PHRENIC NERVE; PHYSIOLOGY; PROCEDURES; TRANSCUTANEOUS NERVE STIMULATION; YOUNG ADULT;

ADULT; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; ELECTROMYOGRAPHY; EVOKED POTENTIALS, MOTOR; FEMALE; HUMANS; MALE; MIDDLE AGED; MOTOR NEURONS; PHRENIC NERVE; RESPIRATORY MECHANICS; TRANSCUTANEOUS ELECTRIC NERVE STIMULATION; YOUNG ADULT;

EID: 84908077895     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1288-14.2014     Document Type: Article

References (82)

1. Aguilar J, Pulecchi F, Dilena R, Oliviero A, Priori A, Foffani G (2011) Spinal direct current stimulation modulates the activity of gracile nucleus and primary somatosensory cortex in anaesthetized rats. J Physiol 589:4981–4996. CrossRef Medline
2. Ahmed Z (2011) Trans-spinal direct current stimulation modulates motor cortex-induced muscle contraction in mice. J Appl Physiol 110:1414–1424. CrossRef Medline
3. Ahmed Z (2013) Effects of cathodal trans-spinal direct current stimulation on mouse spinal network and complex multijoint movements. J Neurosci 33:14949-14957. CrossRef Medline
4. Ahmed Z (2014) Trans-spinal direct current stimulation alters muscle tone in mice with and without spinal cord injury with spasticity. J Neurosci 34:1701–1709. CrossRef Medline
5. Ahmed Z, Wieraszko A (2012) Trans-spinal direct current enhances corticospinal output and stimulation-evoked release of glutamate analog, D-2,3-H-3-aspartic acid. J Appl Physiol 112:1576-1592. CrossRef Medline
6. Alanis J (1953) Effects of direct current on motor neurones. J Physiol 120: 569–578. Medline
7. Aminoff MJ, Sears TA (1971) Spinal integration of segmental, cortical and breathing inputs to thoracic respiratory motoneurones. J Physiol 215: 557–575. Medline
8. Ardolino G, Bossi B, Barbieri S, Priori A (2005) Non-synaptic mechanisms underlie the after-effects of cathodal transcutaneous direct current stimulation of the human brain. J Physiol 568:653-663. CrossRef Medline
9. Azabou E, Roche N, Sharshar T, Bussel B, Lofaso F, Petitjean M (2013) Transcranial direct-current stimulation reduced the excitability of diaphragmatic corticospinal pathways whatever the polarity used. Respir Physiol Neurobiol 189:183–187. CrossRef Medline
10. Bendixen HH, Smith GM, Mead J (1964) Pattern of ventilation in young adults. J Appl Physiol 19:195–198. Medline
11. Berger AJ (1979) Phrenic moto-neurons in the cat: subpopulations and nature of respiratory drive potentials. J Neurophysiol 42:76-90. Medline
12. Bocci T, Vannini B, Torzini A, Mazzatenta A, Vergari M, Cogiamanian F, Priori A, Sartucci F (2014) Cathodal transcutaneous spinal direct current stimulation (tsDCS) improves motor unit recruitment in healthy subjects. Neurosci Lett 578:75–79. CrossRef Medline
13. Boucsein W, Fowles DC, Grimnes S, Ben-Shakhar G, Roth WT, Dawson ME, Filion DL (2012) Publication recommendations for electrodermal measurements. Psychophysiology 49:1017–1034. CrossRef Medline
14. Chitravanshi VC, Sapru HN (1996) NMDAas well as non-NMDA receptors mediate the neurotransmission of inspiratory drive to phrenic motoneurons in the adult rat. Brain Res 715:104-112. CrossRef Medline
15. Chokroverty S, Shah S, Chokroverty M, Deutsch A, Belsh J (1995) Percutaneous magnetic coil stimulation of the phrenic nerve roots and trunk. Electroencephalogr Clin Neurophysiol 97:369-374. CrossRef Medline
16. Cogiamanian F, Vergari M, Pulecchi F, Marceglia S, Priori A (2008) Effect of spinal transcutaneous direct current stimulation on somatosensory evoked potentials in humans. Clin Neurophysiol 119:2636-2640. CrossRef Medline
17. Cogiamanian F, Vergari M, Schiaffi E, Marceglia S, Ardolino G, Barbieri S, Priori A (2011) Transcutaneous spinal cord direct current stimulation inhibits the lower limb nociceptive flexion reflex in human beings. Pain 152:370-375. CrossRef Medline
18. Cooke SF, Bliss TV (2006) Plasticity in the human central nervous system. Brain 129:1659-1673. CrossRef Medline
19. Dale-Nagle EA, Hoffman MS, MacFarlane PM, Satriotomo L, Lovett-Barr MR, Vinit S, Mitchell GS (2010) Spinal plasticity following intermittent hypoxia: implications for spinal injury. Ann N Y Acad Sci 1198:252–259. CrossRef Medline
20. Davey NJ, Murphy K, Maskill DW, Guz A, Ellaway PH (1996) Site of facilitation of diaphragm EMG to corticospinal stimulation during inspiration. Respir Physiol 106:127–135. CrossRef Medline
21. Del Negro CA, Morgado-Valle C, Feldman JL (2002) Respiratory rhythm: an emergent network property? Neuron 34:821-830. CrossRef Medline
22. Demoule A, Verin E, Le Locher C, Derenne JP, Similowski T (2003a) Validation of surface recordings of the diaphragm response to transcranial magnetic stimulation in humans. J Appl Physiol 94:453-461. CrossRef Medline
23. Demoule A, Verin E, Ross E, Moxham J, Derenne JP, Polkey MI, Similowski T (2003b) Intracortical inhibition and facilitation of the response of the diaphragm to transcranial magnetic stimulation. J Clin Neurophysiol 20: 59–64. CrossRef Medline
24. Demoule A, Verin E, Montcel ST, Similowski T (2008) Short-term trainingdependent plasticity of the corticospinal diaphragm control in normal humans. Respir Physiol Neurobiol 160:172–180. CrossRef Medline
25. Di Lazzaro V, Oliviero A, Profice P, Saturno E, Pilato F, Insola A, Mazzone P, Tonali P, Rothwell JC (1998) Comparison of descending volleys evoked by transcranial magnetic and electric stimulation in conscious humans. Electroencephalogr Clin Neurophysiol 109:397-401. CrossRef Medline
26. Duffin J, Tian GF, Peever JH (2000) Functional synaptic connections among respiratory neurons. Respir Physiol 122:237–246. CrossRef Medline
27. Fedorko L, Merrill EG, Lipski J (1983) Two descending medullary inspiratory pathways to phrenic motoneurones. Neurosci Lett 43:285–291. CrossRef Medline
28. Fiamma MN, Samara Z, Baconnier P, Similowski T, Straus C (2007) Respiratory inductive plethysmography to assess respiratory variability and complexity in humans. Respir Physiol Neurobiol 156:234-239. CrossRef Medline
29. Fuller DD, Bach KB, Baker TL, Kinkead R, Mitchell GS (2000) Long term facilitation of phrenic motor output. Respir Physiol 121:135–146. CrossRef Medline
30. Fuortes MG (1954) Direct current stimulation of motoneurones. J Physiol 126:494-506. Medline
31. Golder FJ (2009) SpinalNMDAreceptor activation is necessary for de novo, but not the maintenance of, A2a receptor-mediated phrenic motor facilitation. J Appl Physiol 107:217–223. CrossRef Medline
32. Henneman E, Somjen G, Carpente DO (1965) Functional significance of cell size in spinal motoneurons. J Neurophysiol 28:560-580. Medline
33. Hess A, Yu L, Klein I, De Mazancourt M, Jebrak G, Mal H, Brugie`re O, Fournier M, Courbage M, Dauriat G, Schouman-Clayes E, Clerici C, Mangin L (2013) Neural mechanisms underlying breathing complexity. PLoS One 8:e75740. CrossRef Medline
34. Johnson RA, Mitchell GS (2013) Common mechanisms of compensatory respiratory plasticity in spinal neurological disorders. Respir Physiol Neurobiol 189:419–428. CrossRef Medline
35. Kong FJ, Berger AJ (1986) Firing properties and hypercapnic responses of single phrenic motor axons in the rat. J Appl Physiol 61:1999-2004. Medline
36. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, Wroe S, Asselman P, Marsden CD (1993) Corticocortical inhibition in human motor cortex. J Physiol 471:501–519. Medline
37. Lamy JC, Ho C, Badel A, Arrigo RT, Boakye M (2012) Modulation of soleus H reflex by spinal DC stimulation in humans. J Neurophysiol 108:906–914. CrossRef Medline
38. Laviolette L, Niérat MC, Hudson AL, Raux M, Allard E, Similowski T (2013) The supplementary motor area exerts a tonic excitatory influence on corticospinal projections to phrenic motoneurons in awake humans. PLoS One 8:e62258. CrossRef Medline
39. Lee KZ, Fuller DD (2011) Neural control of phrenic motoneuron discharge. Respir Physiol Neurobiol 179:71–79. CrossRef Medline
40. Lee KZ, Reier PJ, Fuller DD (2009) Phrenic motoneuron discharge patterns during hypoxia-induced short-term potentiation in rats. J Neurophysiol 102:2184-2193. CrossRef Medline
41. Liebetanz D, Nitsche MA, Tergau F, Paulus W (2002) Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced aftereffects of human motor cortex excitability. Brain 125:2238-2247. CrossRef Medline
42. Lim CY, Shin HI (2011) Noninvasive DC stimulation on neck changes MEP. Neuroreport 22:819–823. CrossRef Medline
43. Mangin L, Fiamma MN, Straus C, Derenne JP, Zelter M, Clerici C, Similowski T (2008) Source of human ventilatory chaos: lessons from switching controlled mechanical ventilation to inspiratory pressure support in critically ill patients. Respir Physiol Neurobiol 161:189-196. CrossRef Medline
44. Mateika JH, Syed Z (2013) Intermittent hypoxia, respiratory plasticity and sleep apnea in humans: present knowledge and future investigations. Respir Physiol Neurobiol 188:289-300. CrossRef Medline
45. Matsumoto H, Hanajima R, Terao Y, Ugawa Y (2013) Magnetic-motorroot stimulation: review. Clin Neurophysiol 124:1055–1067. CrossRef Medline
46. Matsumoto L, Hanajima R, Matsumoto H, Ohminami S, Terao Y, Tsuji S, Ugawa Y (2010) Supramaximal responses can be elicited in hand muscles by magnetic stimulation of the cervical motor roots. Brain Stimul 3:153–160. CrossRef Medline
47. McCrimmon DR, Smith JC, Feldman JL (1989) Involvement of excitatory amino-acids in neurotransmission of inspiratory drive to spinal respiratory motoneurons. J Neurosci 9:1910-1921. Medline
48. McGuire M, Liu C, Cao Y, Ling L (2008) Formation and maintenance of ventilatory long-term facilitation require NMDA but not non-NMDA receptors in awake rats. J Appl Physiol 105:942–950. CrossRef Medline
49. Mehiri S, Straus C, Arnulf I, Attali V, Zelter M, Derenne JP, Similowski T (2006) Responses of the diaphragm to transcranial magnetic stimulation during wake and sleep in humans. Respir Physiol Neurobiol 154:406–418. CrossRef Medline
50. Merrill EG, Fedorko L (1984) Mono-synaptic inhibition of phrenic motoneurons - a long descending projection from Botzinger neurons. J Neurosci 4:2350-2353. Medline
51. Mitchell GS, Baker TL, Nanda SA, Fuller DD, Zabka AG, Hodgeman BA, Bavis RW, Mack KJ, Olson EB (2001) Invited review: Intermittent hypoxia and respiratory plasticity. J Appl Physiol 90:2466-2475. Medline
52. Mitchell GS, Johnson SM (2003) Plasticity in respiratory motor control-invited review: neuroplasticity in respiratory motor control. J Appl Physiol 94:358-374. Medline
53. Mitchell GS, Terada J (2011) Should we standardize protocols and preparations used to study respiratory plasticity? Respir Physiol Neurobiol 177: 93–97. CrossRef Medline
54. Murphy K, Mier A, Adams L, Guz A (1990) Putative cerebral cortical involvement in the ventilatory response to inhaled co2 in conscious man. J Physiol 420:1–18. Medline
55. Nitsche MA, Fricke K, Henschke U, Schlitterlau A, Liebetanz D, Lang N, Henning S, Tergau F, Paulus W (2003) Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J Physiol 553:293–301. CrossRef Medline
56. Parazzini M, Rossi E, Ferrucci R, Liorni I, Priori A, Ravazzani P (2014) Modelling the electric field and the current density generated by cerebellar transcranial DC stimulation in humans. Clin Neurophysiol 125:577–584. CrossRef Medline
57. Poon CS, Barahona M (2001) Titration of chaos with added noise. Proc Natl Acad Sci U S A 98:7107–7112. CrossRef Medline
58. Priori A, Ciocca M, Parazzini M, Vergari M, Ferrucci R (2014) Transcranial cerebellar direct current stimulation and transcutaneous spinal cord direct current stimulation as innovative tools for neuroscientists. J Physiol 592:3345–3369. CrossRef Medline
59. Raux M, Xie H, Similowski T, Koski L (2010) Facilitatory conditioning of the supplementary motor area in humans enhances the corticophrenic responsiveness to transcranial magnetic stimulation. J Appl Physiol 108: 39–46. CrossRef Medline
60. Rekling JC, Funk GD, Bayliss DA, Dong XW, Feldman JL (2000) Synaptic central of motoneuronal excitability. Physiol Rev 80:767-852. Medline
61. Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, Dimitrijeviæ MR, Hallett M, Katayama Y, Lücking CH, Maertens de Noordhout AL, Marsden CD, Murray NMF, Rothwell JC, Swash M, Tomberg C (1994) Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 91:79-92. CrossRef Medline
62. Rothwell JC, Day BL, Thompson PD, Kujirai T (2009) Short latency intracortical inhibition: one of the most popular tools in human motor neurophysiology. J Physiol 587:11–12. CrossRef Medline
63. Roulin E, Freitas US, Letellier C (2011) Working conditions for safe detection of nonlinearity and noise titration. Phys Rev E Stat Nonlin Soft Matter Phys. 83:046225. CrossRef Medline
64. Saboisky J, Gorman RB, De Troyer A, Gandevia SC, Butler JE (2007) Differential activation among five human inspiratory motoneuron pools during tidal breathing. J Appl Physiol 102:772–780. CrossRef Medline
65. Schmid UD, Walker G, Hess CW, Schmid J (1990) Magnetic and electrical stimulation of cervical motor roots: technique, site and mechanisms of excitation. J Neurol Neurosurg Psychiatry 53:770-777. CrossRef Medline
66. Schmidt M, Demoule A, Cracco C, Gharbi A, Fiamma MN, Straus C, Duguet A, Gottfried SB, Similowski T (2010) Neurally adjusted ventilatory assist increases respiratory variability and complexity in acute respiratory failure. Anesthesiology 112:670–681. CrossRef Medline
67. Sharshar T, Hopkinson NS, Jonville S, Prigent H, Carlier R, Dayer MJ, Swallow EB, Lofaso F, Moxham J, Polkey MI (2004) Demonstration of a second rapidly conducting cortico-diaphragmatic pathway in humans. J Physiol 560:897–908. CrossRef Medline
68. Similowski T, Fleury B, Launois S, Cathala HP, Bouche P, Derenne JP (1989) Cervical magnetic stimulation: a new painless method for bilateral phrenic nerve stimulation in conscious humans. J Appl Physiol 67:1311–1318. Medline
69. Similowski T, Mehiri S, Duguet A, Attali V, Straus C, Derenne JP (1997) Comparison of magnetic and electrical phrenic nerve stimulation in assessment of phrenic nerve conduction time. J Appl Physiol 82:1190-1199. Medline
70. Stagg CJ, Nitsche MA (2011) Physiological basis of transcranial direct current stimulation. Neuroscientist 17:37–53. CrossRef Medline
71. Stein PK, Domitrovich PP, Huikuri HV, Kleiger RE (2005) Traditional and nonlinear heart rate variability are each independently associated with mortality after myocardial infarction. J Cardiovasc Electrophysiol 16:13–20. CrossRef Medline
72. Stinear CM, Byblow WD (2004) Elevated threshold for intracortical inhibition in focal hand dystonia. Mov Disord 19:1312–1317. CrossRef Medline
73. Straus C, Locher C, Zelter M, Derenne JP, Similowski T (2004) Facilitation of the diaphragm response to transcranial magnetic stimulation by increases in human respiratory drive. J Appl Physiol 97:902–912. CrossRef Medline
74. Straus C, Samara Z, Fiamma MN, Bautin N, Ranohavimparany A, Le Coz P, Golmard JL, Darré P, Zelter M, Poon CS, Similowski T (2011) Effects of maturation and acidosis on the chaos-like complexity of the neural respiratory output in the isolated brainstem of the tadpole, Rana esculenta. Am J Physiol Regul Integr Comp Physiol 300:R1163–R1174. CrossRef Medline
75. Syed Z, Lin HS, Mateika JH (2013) The impact of arousal state, sex, and sleep apnea on the magnitude of progressive augmentation and ventilatory long-term facilitation. J Appl Physiol 114:52-65. CrossRef Medline
76. Toshev PK, Guleyupoglu B, Bikson M (2014) Informing dose design by modeling transcutaneous spinal direct current stimulation Clin Neurophysiol. Advance online publication. Retrieved April 4, 2014. doi: 10.1016/j.clinph.2014.03.022. CrossRef.
77. Truini A, Vergari M, Biasiotta A, La Cesa S, Gabriele M, Di Stefano G, Cambieri C, Cruccu G, Inghilleri M, Priori A (2011) Transcutaneous spinal direct current stimulation inhibits nociceptive spinal pathway conduction and increases pain tolerance in humans. Eur J Pain 15:1023–1027. CrossRef Medline
78. Ugawa Y, Rothwell JC, Day BL, Thompson PD, Marsden CD (1989) Magnetic stimulation over the spinal enlargements. J Neurol Neurosurg Psychiatry 52:1025–1032. CrossRef Medline
79. Verin E, Marie JP, Similowski T (2011) Cartography of human diaphragmatic innervation: preliminary data. Respir Physiol Neurobiol 176:68–71. CrossRef Medline
80. Winkler T, Hering P, Straube A (2010) Spinal DC stimulation in humans modulates post-activation depression of the H-reflex depending on current polarity. Clin Neurophysiol 121:957–961. CrossRef Medline
81. Wolpaw JR, Carp JS (2006) Plasticity from muscle to brain. Prog Neurobiol 78:233–263. CrossRef Medline
82. Wysocki M, Fiamma MN, Straus C, Poon CS, Similowski T (2006) Chaotic dynamics of resting ventilatory flow in humans assessed through noise titration. Respir Physiol Neurobiol 153:54–65. CrossRef Medline