#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Transcranial magnetic stimulation induced early silent period and rebound activity re-examined


Autoři: Mustafa Görkem Özyurt aff001;  Heidi Haavik aff002;  Rasmus Wiberg Nedergaard aff002;  Betilay Topkara aff001;  Beatrice Selen Şenocak aff003;  Mehmet Berke Göztepe aff004;  Imran Khan Niazi aff002;  Kemal Sitki Türker aff001
Působiště autorů: School of Medicine, Koç University, Istanbul, Turkey aff001;  Centre for Chiropractic Research, New Zealand College of Chiropractic, Auckland, New Zealand aff002;  Frank H. Netter MD School of Medicine, Quinnipiac University, North Haven, CT, United States of America aff003;  School of Medicine, Akdeniz University, Antalya, Turkey aff004
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0225535

Souhrn

Despite being widely studied, the underlying mechanisms of transcranial magnetic brain stimulation (TMS) induced motor evoked potential (MEP), early cortical silent period (CSP) and rebound activity are not fully understood. Our aim is to better characterize these phenomena by combining various analysis tools on firing motor units. Responses of 29 tibialis anterior (TA) and 8 abductor pollicis brevis (APB) motor units to TMS pulses were studied using discharge rate and probability-based tools to illustrate the profile of the synaptic potentials as they develop on motoneurons in 24 healthy volunteers. According to probability-based methods, TMS pulse produces a short-latency MEP which is immediately followed by CSP that terminates at rebound activity. Discharge rate analysis, however, revealed not three, but just two events with distinct time courses; a long-lasting excitatory period (71.2 ± 9.0 ms for TA and 42.1 ± 11.2 ms for APB) and a long-latency inhibitory period with duration of 57.9 ± 9.5 ms for TA and 67.3 ± 13.8 ms for APB. We propose that part of the CSP may relate to the falling phase of net excitatory postsynaptic potential induced by TMS. Rebound activity, on the other hand, may represent tendon organ inhibition induced by MEP activated soleus contraction and/or long-latency intracortical inhibition. Due to generation of field potentials when high intensity TMS is used, this study is limited to investigate the events evoked by low intensity TMS only and does not provide information about later parts of much longer CSPs induced by high intensity TMS. Adding discharge rate analysis contributes to obtain a more accurate picture about the characteristics of TMS-induced events. These results have implications for interpreting motor responses following TMS for diagnosis and overseeing recovery from various neurological conditions.

Klíčová slova:

Action potentials – Electrodes – Electromyography – Muscle contraction – Transcranial magnetic stimulation – Excitatory postsynaptic potentials – Synaptic potential – Motor cortex


Zdroje

1. Polson MJ, Barker AT, Freeston IL. Stimulation of nerve trunks with time-varying magnetic fields. Med Biol Eng Comput. 1982;20: 243–244. doi: 10.1007/bf02441362 7098583

2. Barker AT, Jalinous R, Freeston IL. Non-invasive magnetic stimulation of human motor cortex. Lancet. 1985;1: 1106–1107. doi: 10.1016/s0140-6736(85)92413-4 2860322

3. Wu L, Goto Y, Taniwaki T, Kinukawa N, Tobimatsu S. Different patterns of excitation and inhibition of the small hand and forearm muscles from magnetic brain stimulation in humans. Clin Neurophysiol. 2002;113: 1286–1294. doi: 10.1016/s1388-2457(02)00160-8 12140009

4. Orth M, Rothwell JC. The cortical silent period: intrinsic variability and relation to the waveform of the transcranial magnetic stimulation pulse. Clin Neurophysiol. 2004;115: 1076–1082. doi: 10.1016/j.clinph.2003.12.025 15066533

5. Taylor JL, Allen GM, Butler JE, Gandevia SC. Supraspinal fatigue during intermittent maximal voluntary contractions of the human elbow flexors. J Appl Physiol. 2000;89: 305–313. doi: 10.1152/jappl.2000.89.1.305 10904066

6. Fuhr P, Agostino R, Hallett M. Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalogr Clin Neurophysiol. 1991;81: 257–262. doi: 10.1016/0168-5597(91)90011-l 1714819

7. Inghilleri M, Berardelli A, Cruccu G, Manfredi M. Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol. 1993;466: 521–534. 8410704

8. Ziemann U. TMS and drugs. Clin Neurophysiol. 2004;115: 1717–1729. doi: 10.1016/j.clinph.2004.03.006 15261850

9. Priori A, Berardelli A, Inghilleri M, Accornero N, Manfredi M. Motor cortical inhibition and the dopaminergic system. Pharmacological changes in the silent period after transcranial brain stimulation in normal subjects, patients with Parkinson's disease and drug-induced parkinsonism. Brain. 1994;117: 317–323. doi: 10.1093/brain/117.2.317 8186958

10. Kimiskidis VK, Papagiannopoulos S, Kazis DA, Sotirakoglou K, Vasiliadis G, et al. Lorazepam-induced effects on silent period and corticomotor excitability. Exp Brain Res. 2006;173: 603–611. doi: 10.1007/s00221-006-0402-1 16525803

11. Devanne H, Lavoie BA, Capaday C. Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res. 1997;114: 329–338. doi: 10.1007/pl00005641 9166922

12. Ziemann U, Iliać TV, Pauli C, Meintzschel F, Ruge D. Learning Modifies Subsequent Induction of Long-Term Potentiation-Like and Long-Term Depression-Like Plasticity in Human Motor Cortex. J Neurosci. 2004;24: 1666–1672. doi: 10.1523/JNEUROSCI.5016-03.2004 14973238

13. Lee JC, Croarkin PE, Ameis SH, Sun Y, Blumberger DM, et al. Paired-Associative Stimulation-Induced Long-term Potentiation-Like Motor Cortex Plasticity in Healthy Adolescents. Front Psychiatry. 2017;8: 95. doi: 10.3389/fpsyt.2017.00095 28611693

14. Guekht A, Selikhova M, Serkin G, Gusev E. Implementation of the TMS in the early stages of Parkinson's disease. Electromyogr Clin Neurophysiol. 2005;45: 291–297. 16218197

15. Ahonen JP, Jehkonen M, Dastidar P, Molnar G, Hakkinen V. Cortical silent period evoked by transcranial magnetic stimulation in ischemic stroke. Electroencephalogr Clin Neurophysiol. 1998;109: 224–229. doi: 10.1016/s0924-980x(98)00014-9 9741788

16. Schmied A, Attarian S. Enhancement of single motor unit inhibitory responses to transcranial magnetic stimulation in amyotrophic lateral sclerosis. Exp Brain Res. 2008;189: 229–242. doi: 10.1007/s00221-008-1420-y 18496679

17. Rossini P, Burke D, Chen R, Cohen LG, Daskalakis Z, et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: Basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol. 2015;89.

18. Pearce SL, Miles TS, Thompson PD, Nordstrom MA. Responses of single motor units in human masseter to transcranial magnetic stimulation of either hemisphere. J Physiol. 2003;549: 583–596. doi: 10.1113/jphysiol.2002.035352 12692177

19. Türker KS, Powers RK. Black box revisited: a technique for estimating postsynaptic potentials in neurons. Trends Neurosci. 2005;28: 379–386. doi: 10.1016/j.tins.2005.05.007 15927277

20. Moore GP, Segundo JP, Perkel DH, Levitan H. Statistical signs of synaptic interaction in neurons. Biophys J. 1970;10: 876–900. doi: 10.1016/S0006-3495(70)86341-X 4322240

21. Türker KS, Powers RK. Estimation of postsynaptic potentials in rat hypoglossal motoneurones: insights for human work. J Physiol. 2003;551: 419–431. doi: 10.1113/jphysiol.2003.044982 12872008

22. Todd G, Rogasch NC, Türker KS. Transcranial magnetic stimulation and peristimulus frequencygram. Clin Neurophysiol. 2012;123: 1002–1009. doi: 10.1016/j.clinph.2011.09.019 22019353

23. Haavik H, Niazi IK, Jochumsen M, Ugincius P, Sebik O, et al. Chiropractic spinal manipulation alters TMS induced I-wave excitability and shortens the cortical silent period. J Electromyogr Kinesiol. 2018;42: 24–35. doi: 10.1016/j.jelekin.2018.06.010 29936314

24. Mueller JK, Grigsby EM, Prevosto V, Petraglia FW 3rd, Rao H, et al. Simultaneous transcranial magnetic stimulation and single-neuron recording in alert non-human primates. Nat Neurosci. 2014;17: 1130–1136. doi: 10.1038/nn.3751 24974797

25. Moliadze V, Zhao Y, Eysel U, Funke K. Effect of transcranial magnetic stimulation on single-unit activity in the cat primary visual cortex. J Physiol. 2003;553: 665–679. doi: 10.1113/jphysiol.2003.050153 12963791

26. Tucker KJ, Türker KS. A new method to estimate signal cancellation in the human maximal M-wave. J Neurosci Methods. 2005;149: 31–41. doi: 10.1016/j.jneumeth.2005.05.010 16024088

27. Türker KS, Miles TS, Le HT. The lip-clip: a simple, low-impedance ground electrode for use in human electrophysiology. Brain Res Bull. 1988;21: 139–141. doi: 10.1016/0361-9230(88)90130-x 3219597

28. Homan RW, Herman J, Purdy P. Cerebral location of international 10–20 system electrode placement. Electroencephalogr Clin Neurophysiol. 1987;66: 376–382. doi: 10.1016/0013-4694(87)90206-9 2435517

29. Türker KS, Cheng HB. Motor-unit firing frequency can be used for the estimation of synaptic potentials in human motoneurones. J Neurosci Methods. 1994;53: 225–234. doi: 10.1016/0165-0270(94)90181-3 7823625

30. Ellaway PH. Cumulative sum technique and its application to the analysis of peristimulus time histograms. Electroencephalogr Clin Neurophysiol. 1978;45: 302–304. doi: 10.1016/0013-4694(78)90017-2 78843

31. Türker KS, Yang J, Brodin P. Conditions for excitatory or inhibitory masseteric reflexes elicited by tooth pressure in man. Arch Oral Biol. 1997;42: 121–128. doi: 10.1016/s0003-9969(96)00112-4 9134124

32. Brinkworth RS, Türker KS. A method for quantifying reflex responses from intra-muscular and surface electromyogram. J Neurosci Methods. 2003;122: 179–193. doi: 10.1016/s0165-0270(02)00321-7 12573477

33. Miles TS, Türker KS, Le TH. Ia reflexes and EPSPs in human soleus motor neurones. Exp Brain Res. 1989;77: 628–636. doi: 10.1007/bf00249616 2806452

34. Powers RK, Türker KS. Estimates of EPSP amplitude based on changes in motoneuron discharge rate and probability. Exp Brain Res. 2010;206: 427–440. doi: 10.1007/s00221-010-2423-z 20862458

35. Kudina LP. Reflex effects of muscle afferents on antagonist studied on single firing motor units in man. Electroencephalogr Clin Neurophysiol. 1980;50: 214–221. doi: 10.1016/0013-4694(80)90148-0 6160962

36. Kojima S, Onishi H, Sugawara K, Kirimoto H, Suzuki M, et al. Modulation of the cortical silent period elicited by single- and paired-pulse transcranial magnetic stimulation. BMC Neurosci. 2013;14: 43. doi: 10.1186/1471-2202-14-43 23547559

37. Saisanen L, Pirinen E, Teitti S, Kononen M, Julkunen P, et al. Factors influencing cortical silent period: optimized stimulus location, intensity and muscle contraction. J Neurosci Methods. 2008;169: 231–238. doi: 10.1016/j.jneumeth.2007.12.005 18243329

38. Julkunen P, Säisänen L, Danner N, Niskanen E, Hukkanen T, et al. Comparison of navigated and non-navigated transcranial magnetic stimulation for motor cortex mapping, motor threshold and motor evoked potentials. NeuroImage. 2009;44: 790–795. doi: 10.1016/j.neuroimage.2008.09.040 18976714

39. McNulty PA, Lin G, Doust CG. Single motor unit firing rate after stroke is higher on the less-affected side during stable low-level voluntary contractions. Front Hum Neurosci. 2014;8: 518. doi: 10.3389/fnhum.2014.00518 25100969

40. van Kuijk AAA, Bakker CD, Hendriks JCM, Geurts ACH, Stegeman DF, et al. Definition dependent properties of the cortical silent period in upper-extremity muscles, a methodological study. J Neuroeng Rehabil. 2014;11: 1. doi: 10.1186/1743-0003-11-1 24393611

41. Tataroglu C, Ozkiziltan S, Baklan B. Motor cortical thresholds and cortical silent periods in epilepsy. Seizure. 2004;13: 481–485. doi: 10.1016/j.seizure.2003.11.003 15324826

42. Poston B, Kukke SN, Paine RW, Francis S, Hallett M. Cortical silent period duration and its implications for surround inhibition of a hand muscle. J Neurosci. 2012;36: 2964–2971.

43. Powers RK, Türker KS. Deciphering the contribution of intrinsic and synaptic currents to the effects of transient synaptic inputs on human motor unit discharge. Clin Neurophysiol. 2010;121: 1643–1654. doi: 10.1016/j.clinph.2009.10.041 20427230

44. Kernell D. Functional properties of spinal motoneurons and gradation of muscle force. Adv Neurol. 1983;39: 213–226. 6318530

45. Inghilleri M, Berardelli A, Cruccu G, Manfredi M. Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol. 1993;466: 521–534. 8410704

46. Chen R, Lozano AM, Ashby P. Mechanism of the silent period following transcranial magnetic stimulation: Evidence from epidural recordings. Exp Brain Res. 1999;128: 539–542. doi: 10.1007/s002210050878 10541749

47. Pierantozzi M, Marciani MG, Palmieri MG, Brusa L, Galati S, et al. Effect of Vigabatrin on motor responses to transcranial magnetic stimulation: an effective tool to investigate in vivo GABAergic cortical inhibition in humans. Brain Res. 2004;1028: 1–8. doi: 10.1016/j.brainres.2004.06.009 15518635

48. Brasil-Neto JP, Cammarota A, Valls-Sole J, Pascual-Leone A, Hallett M, et al. Role of intracortical mechanisms in the late part of the silent period to transcranial stimulation of the human motor cortex. Acta Neurol Scand. 1995;92: 383–386. doi: 10.1111/j.1600-0404.1995.tb00151.x 8610491

49. Tergau F, Wanschura V, Canelo M, Wischer S, Wassermann EM, et al. Complete suppression of voluntary motor drive during the silent period after transcranial magnetic stimulation. Exp Brain Res. 1999;124: 447–454. doi: 10.1007/s002210050640 10090656

50. Siebner HR, Dressnandt J, Auer C, Conrad B. Continuous intrathecal baclofen infusions induced a marked increase of the transcranially evoked silent period in a patient with generalized dystonia. Muscle Nerve. 1998;21: 1209–1212. doi: 10.1002/(sici)1097-4598(199809)21:9<1209::aid-mus15>3.0.co;2-m 9703450

51. Werhahn KJ, Kunesch E, Noachtar S, Benecke R, Classen J. Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol. 1999;517: 591–597. doi: 10.1111/j.1469-7793.1999.0591t.x 10332104

52. McDonnell MN, Orekhov Y, Ziemann U. The role of GABA(B) receptors in intracortical inhibition in the human motor cortex. Exp Brain Res. 2006;173: 86–93. doi: 10.1007/s00221-006-0365-2 16489434

53. Bowery NG. GABAB receptor: a site of therapeutic benefit. Curr Opin Pharmacol. 2006;6: 37–43. doi: 10.1016/j.coph.2005.10.002 16361115

54. Özyurt MG, Piotrkiewicz M, Topkara B, Weisskircher HW, Türker KS. Motor units as tools to evaluate profile of human Renshaw inhibition. J Physiol. 2019;597: 2185–2199. doi: 10.1113/JP277129 30673125

55. Cantello R, Gianelli M, Civardi C, Mutani R. Magnetic brain stimulation: the silent period after the motor evoked potential. Neurology. 1992;42: 1951–1959. doi: 10.1212/wnl.42.10.1951 1407578

56. Burne JA, Lippold OC. Reflex inhibition following electrical stimulation over muscle tendons in man. Brain. 1996;119 (Pt 4): 1107–1114.

57. Roick H, von Giesen HJ, Benecke R. On the origin of the postexcitatory inhibition seen after transcranial magnetic brain stimulation in awake human subjects. Exp Brain Res. 1993;94: 489–498. doi: 10.1007/bf00230207 8359263


Článek vyšel v časopise

PLOS One


2019 Číslo 12
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#