#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Effects of Transcranial Direct Current Stimulation on GABA and Glx in Children: A pilot study


Autoři: Chidera Nwaroh aff001;  Adrianna Giuffre aff002;  Lauran Cole aff002;  Tiffany Bell aff001;  Helen L. Carlson aff002;  Frank P. MacMaster aff002;  Adam Kirton aff002;  Ashley D. Harris aff001
Působiště autorů: Department of Radiology, University of Calgary, Calgary AB, Canada aff001;  Alberta Children’s Hospital (ACHRI), Calgary, AB, Canada aff002;  Hotchkiss Brain Institute, Calgary, AB, Canada aff003;  Child and Adolescent Imaging Research (CAIR) Program, Calgary, AB, Canada aff004;  Department of Neuroscience, University of Calgary, Calgary, AB, Canada aff005;  Department of Pediatrics, University of Calgary, Calgary, AB, Canada aff006;  Department of Psychiatry, University of Calgary, Calgary, AB, Canada aff007;  The Mathison Centre for Mental Health Research and Education, University of Calgary, Calgary, AB, Canada aff008;  Addictions and Mental Health Strategic Clinical Network, Calgary, AB, Canada aff009
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222620

Souhrn

Transcranial direct current stimulation (tDCS) is a form of non-invasive brain stimulation that safely modulates brain excitability and has therapeutic potential for many conditions. Several studies have shown that anodal tDCS of the primary motor cortex (M1) facilitates motor learning and plasticity, but there is little information about the underlying mechanisms. Using magnetic resonance spectroscopy (MRS), it has been shown that tDCS can affect local levels of γ-aminobutyric acid (GABA) and Glx (a measure of glutamate and glutamine combined) in adults, both of which are known to be associated with skill acquisition and plasticity; however this has yet to be studied in children and adolescents. This study examined GABA and Glx in response to conventional anodal tDCS (a-tDCS) and high definition tDCS (HD-tDCS) targeting the M1 in a pediatric population. Twenty-four typically developing, right-handed children ages 12–18 years participated in five consecutive days of tDCS intervention (sham, a-tDCS or HD-tDCS) targeting the right M1 while training in a fine motor task (Purdue Pegboard Task) with their left hand. Glx and GABA were measured before and after the protocol (at day 5 and 6 weeks) using a PRESS and GABA-edited MEGA-PRESS MRS sequence in the sensorimotor cortices. Glx measured in the left sensorimotor cortex was higher in the HD-tDCS group compared to a-tDCS and sham at 6 weeks (p = 0.001). No changes in GABA were observed in either sensorimotor cortex at any time. These results suggest that neither a-tDCS or HD-tDCS locally affect GABA and Glx in the developing brain and therefore it may demonstrate different responses in adults.

Klíčová slova:

Pediatrics – Functional electrical stimulation – Transcranial magnetic stimulation – Glutamate – Metabolites – Transcranial direct-current stimulation – Gamma-aminobutyric acid – Magnetic resonance spectroscopy


Zdroje

1. Reis J, Fritsch B. Modulation of motor performance and motor learning by transcranial direct current stimulation. Curr Opin Neurol. 2011;24(6):590–6. doi: 10.1097/WCO.0b013e32834c3db0 21968548

2. Nitsche MA, Paulus WJ. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology. 2001;57(10):1899–901. doi: 10.1212/wnl.57.10.1899 11723286

3. Nitsche MA, Schauenburg A, Lang N, Liebetanz D, Exner C, Paulus WJ, et al. Facilitation of implicit motor learning by weak transcranial direct current stimulation of the primary motor cortex in the human. J Cogn Neurosci. 2003;15(4):619–26. doi: 10.1162/089892903321662994 12803972

4. Stagg CJ, Best JG, Stephenson MC, O’Shea J, Wylezinska M, Kincses ZT, et al. Polarity-Sensitive Modulation of Cortical Neurotransmitters by Transcranial Stimulation. J Neurosci. 2009;29(16):5202–6. doi: 10.1523/JNEUROSCI.4432-08.2009 19386916

5. Zhao H, Qiao L, Fan D, Zhang S, Turel O, Li Y. Modulation of Brain Activity with Noninvasive Transcranial Direct Current Stimulation (tDCS): Clinical Applications and Safety Concerns. 2017;8(May). doi: 10.3389/fpsyg.2017.00685 28539894

6. Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, et al. Transcranial direct current stimulation: State of the art 2008. Brain Stimul. 2008;1(3):206–23. doi: 10.1016/j.brs.2008.06.004 20633386

7. Antal A, Lang N, Boros K, Nitsche MA, Siebner HR, Paulus W. Homeostatic metaplasticity of the motor cortex is altered during headache-free intervals in migraine with aura. Cereb Cortex. 2008;18(11):2701–5. doi: 10.1093/cercor/bhn032 18372292

8. Boggio PS, Nunes A, Rigonatti SP, Nitsche MA, Pascual-Leone A, Fregni F. Repeated sessions of noninvasive brain DC stimulation is associated with motor function improvement in stroke patients. Restor Neurol Neurosci. 2007;25(2):123–9. 17726271

9. Fregni F, Boggio PS, Santos MC, Lima MC, Vieira AL, Rigonatti SP, et al. Noninvasive cortical stimulation with transcranial direct current stimulation in Parkinson’s disease. Mov Disord. 2006;21(10):1693–702. doi: 10.1002/mds.21012 16817194

10. Fregni F, Boggio PS, Lima MC, Ferreira MJ., Wagner T, Rigonatti SP, et al. A sham-controlled, phase II trial of transcranial direct current stimulation for the treatment of central pain in traumatic spinal cord injury. Pain. 2006;122(1):197–209.

11. Harris AD, Wang Z, Ficek B, Webster K, Edden RA, Tsapkini K. Reductions in GABA following a tDCS-Language Intervention for Primary Progressive Aphasia. Neurobiol Aging. 2019;79:75–82. doi: 10.1016/j.neurobiolaging.2019.03.011 31029018

12. Fregni F, Boggio PS, Nitsche MA, Marcolin MA, Rigonatti SP, Pascual-Leone A. Treatment of major depression with transcranial direct current stimulation. Bipolar Disord. 2006;8:203–4. doi: 10.1111/j.1399-5618.2006.00291.x 16542193

13. Dmochowski JP, Datta A, Bikson M, Su Y, Parra LC. Optimized multi-electrode stimulation increases focality and intensity at target. J Neural Eng. 2011;8(4).

14. Datta A, Bansal V, Diaz J, Patel J, Reato D, Bikson M. Gyri–precise head model of transcranial DC stimulation. NIH Public Access. 2010;2(4):201–7.

15. Villamar MF, Volz MS, Bikson M, Datta A, DaSilva AF, Fregni F. Technique and Considerations in the Use of 4x1 Ring High-definition Transcranial Direct Current Stimulation (HD-tDCS). J Vis Exp. 2013;(77).

16. Kuo HI, Bikson M, Datta A, Minhas P, Paulus W, Kuo MF, et al. Comparing cortical plasticity induced by conventional and high-definition 4 × 1 ring tDCS: A neurophysiological study. Brain Stimul. 2013;6(4):644–8. doi: 10.1016/j.brs.2012.09.010 23149292

17. Borckardt JJ, Bikson M, Frohman H, Reeves ST, Datta A, Bansal V, et al. A pilot study of the tolerability and effects of high-definition transcranial direct current stimulation (HD-tDCS) on pain perception. J Pain. 2012;13(2):112–20. doi: 10.1016/j.jpain.2011.07.001 22104190

18. Cole L, Giuffre A, Ciechanski P, Carlson HL, Zewdie E, Kuo H-C, et al. Effects of High-Definition and Conventional Transcranial Direct-Current Stimulation on Motor Learning in Children. 2018;12:1–12.

19. Woods AJ, Antal A, Bikson M, Boggio PS, Brunoni AR, Celnik PA, et al. A technical guide to tDCS, and related non-invasive brain stimulation tools. Clin Neurophysiol. 2016;127(2):1031–48. doi: 10.1016/j.clinph.2015.11.012 26652115

20. Bikson M, Grossman P, Thomas C, Zannou AL, Jiang J, Adnan T, et al. Safety of Transcranial Direct Current Stimulation: Evidence Based Update 2016. Brain Stimul. 2016;9(5):641–61. doi: 10.1016/j.brs.2016.06.004 27372845

21. Rajapakse T, Kirton A. Non-invasive brain stimulation in children: Applications and future directions. Transl Neurosci. 2013;4(2):217–33.

22. Kessler SK, Minhas P, Woods AJ, Rosen A, Gorman C, Bikson M. Dosage Considerations for Transcranial Direct Current Stimulation in Children: A Computational Modeling Study. PLoS One. 2013;8(9):1–15.

23. Davis NJ. Transcranial stimulation of the developing brain: A plea for extreme caution. Front Hum Neurosci. 2014;8(AUG):8–11.

24. Hameed MQ, Dhamne SC, Gersner R, Kaye HL, Oberman LM, Pascual-Leone A, et al. Transcranial Magnetic and Direct Current Stimulation in Children. Curr Neurol Neurosci Rep. 2017;17(2).

25. Kirton A, Ciechanski P, Zewdie E, Andersen J, Nettel-Aguirre A, Carlson H, et al. Transcranial direct current stimulation for children with perinatal stroke and hemiparesis. Neurology. 2016;88(3):259–67. doi: 10.1212/WNL.0000000000003518 27927938

26. Ciechanski P, Kirton A. Transcranial Direct-Current Stimulation Can Enhance Motor Learning in Children. Cereb Cortex. 2017;27(5):2758–67. doi: 10.1093/cercor/bhw114 27166171

27. Kirton A. Modeling developmental plasticity after perinatal stroke: Defining central therapeutic targets in cerebral palsy. Vol. 48, Pediatric Neurology. 2013. p. 81–94. doi: 10.1016/j.pediatrneurol.2012.08.001 23337000

28. Stagg CJ, Bachtiar V, Johansen-Berg H. The role of GABA in human motor learning. Curr Biol. 2011;21(6):480–4. doi: 10.1016/j.cub.2011.01.069 21376596

29. Kim S, Stephenson MC, Morris PG, Jackson SR. TDCS-induced alterations in GABA concentration within primary motor cortex predict motor learning and motor memory: A 7T magnetic resonance spectroscopy study. Neuroimage. 2014;99:237–43. doi: 10.1016/j.neuroimage.2014.05.070 24904994

30. Clark VP, Coffman BA, Trumbo MC, Gasparovic C. Transcranial direct current stimulation (tDCS) produces localized and specific alterations in neurochemistry: A 1H magnetic resonance spectroscopy study. Neurosci Lett. 2011;500(1):67–71. doi: 10.1016/j.neulet.2011.05.244 21683766

31. Froc DJ, Chapman A, Trepel C, Racine RJ. Long-Term Depression and Depotentiation in the Sensorimotor Cortex of the Freely Moving Rat. J Neurosci. 2000;20(1):438–45. doi: 10.1523/JNEUROSCI.20-01-00438.2000 10627619

32. Lüscher C, Malenka RC. NMDA Receptor-Dependent Long-Term Potentiation and Long-Term Depression (LTP / LTD). 2012;1–15.

33. Carlson HL, Ciechanski P, Harris AD, MacMaster FP, Kirton A. Changes in spectroscopic biomarkers after transcranial direct current stimulation in children with perinatal stroke. Brain Stimul. 2018;11(1):94–103. doi: 10.1016/j.brs.2017.09.007 28958737

34. Harris AD, Saleh MG, Edden R. Edited 1 H magnetic resonance spectroscopy in vivo: Methods and metabolites. Magn Reson Med. 2017;77(4):1377–89. doi: 10.1002/mrm.26619 28150876

35. Mullins P, McGonigle DJ, O’Gorman RL, Puts N, Vidyasagar R, Evans J, et al. Current practice in the use of MEGA-PRESS spectroscopy for the detection of GABA. Neuroimage. 2014;86:43–52. doi: 10.1016/j.neuroimage.2012.12.004 23246994

36. Oldfield RC. The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia. 1971;

37. Reis J, Schambra HM, Cohen LG, Buch ER, Fritsch B, Zarahn E, et al. Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc Natl Acad Sci. 2009;106(5):1590–5. doi: 10.1073/pnas.0805413106 19164589

38. Kolasinski J, Hinson EL, Divanbeighi Zand AP, Rizov A, Emir UE, Stagg CJ. The dynamics of cortical GABA in human motor learning. J Physiol. 2019;597(1):271–82. doi: 10.1113/JP276626 30300446

39. Caparelli-Daquer EM, Zimmermann TJ, Mooshagian E, Parra LC, Rice JK, Datta A, et al. A Pilot Study on Effects of 4×1 High-Definition tDCS on Motor Cortex Excitability. 2017;20(1):48–55.

40. Richardson J, Datta A, Dmochowski JP, Parra LC, Fridriksson J. Feasibility of using high-definition transcranial direct current stimulation (HD-tDCS) to enhance treatment outcomes in persons with aphasia. NeuroRehabilitation. 2015;36(1):115–26. doi: 10.3233/NRE-141199 25547776

41. Fregni F, Boggio PS, Nitsche M, Bermpohl F, Antal A, Feredoes E, et al. Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory. Exp Brain Res. 2005;166(1):23–30. doi: 10.1007/s00221-005-2334-6 15999258

42. Ciechanski P, Carlson HL, Yu SS, Kirton A. Modeling Transcranial Direct-Current Stimulation-Induced Electric Fields in Children and Adults. Front Hum Neurosci. 2018;12(July):1–14. doi: 10.3389/fnhum.2018.00001

43. Ambrus GG, Al-Moyed H, Chaieb L, Sarp L, Antal A, Paulus W. Brain Stimulation The fade-in e Short stimulation e Fade out approach to sham tDCS e Reliable at 1 mA for naïve and experienced subjects, but not investigators. Brain Stimul.

44. Tiffin J, Asher EJ. The Purdue Pegboard: norms and studies of reliability and validity. J Appl Psychol. 1948;32(3):234–47. doi: 10.1037/h0061266 18867059

45. Yousry TA, Schmid UD, Alkadhi H, Schmidt D, Peraud A, Buettner A, et al. Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. Brain. 1997;120(1):141–57.

46. Edden R, Puts N, Harris AD, Barker PB, Evans J. Gannet: A batch-processing tool for the quantitative analysis of gamma-aminobutyric acid-edited MR spectroscopy spectra. J Magn Reson Imaging. 2014;40(6):1445–52. doi: 10.1002/jmri.24478 25548816

47. Harris AD, Puts N, Edden R. Tissue correction for GABA-edited MRS: Considerations of voxel composition, tissue segmentation, and tissue relaxations. J Magn Reson Imaging. 2015;42(5):1431–40. doi: 10.1002/jmri.24903 26172043

48. Gasparovic C, Song T, Devier D, Bockholt HJ, Caprihan A, Mullins PG, et al. Use of tissue water as a concentration reference for proton spectroscopic imaging. Magn Reson Med. 2006;55(6):1219–26. doi: 10.1002/mrm.20901 16688703

49. Harris AD, Gilbert DL, Horn P, Crocetti D, Cecil KM, Edden RA, et al. Anomalous relationship between sensorimotor GABA levels and task-dependent cortical excitability in children with Attention-deficit/hyperactivity disorder. Brain Stimul. 2019;

50. Near J, Edden R, Evans J, Paquin R, Harris AD, Jezzard P. Frequency and phase drift correction of magnetic resonance spectroscopy data by spectral registration in the time domain. Magn Reson Med. 2015;73(1):44–50. doi: 10.1002/mrm.25094 24436292

51. Provencher SW. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med. 1993;30(6):672–9. doi: 10.1002/mrm.1910300604 8139448

52. Boggio PS, Castro LO, Savagim EA, Braite R, Cruz VC, Rocha RR, et al. Enhancement of non-dominant hand motor function by anodal transcranial direct current stimulation. Neurosci Lett. 2006;404(1–2):232–6. doi: 10.1016/j.neulet.2006.05.051 16808997

53. Vines BW, Cerruti C, Schlaug G. Dual-hemisphere tDCS facilitates greater improvements for healthy subjects’ non-dominant hand compared to uni-hemisphere stimulation. BMC Neurosci. 2008;9:1–7. doi: 10.1186/1471-2202-9-1

54. Prichard G, Weiller C, Fritsch B, Reis J. Effects of different electrical brain stimulation protocols on subcomponents of motor skill learning. Brain Stimul. 2014;7(4):532–40. doi: 10.1016/j.brs.2014.04.005 24810956

55. Floyer-Lea A. Rapid Modulation of GABA Concentration in Human Sensorimotor Cortex During Motor Learning. J Neurophysiol. 2006;95(3):1639–44. doi: 10.1152/jn.00346.2005 16221751

56. Hunter MA, Coffman BA, Gasparovic C, Calhoun VD, Trumbo MC, Clark VP. Baseline effects of transcranial direct current stimulation on glutamatergic neurotransmission and large-scale network connectivity. Brain Res. 2015;1594:92–107. doi: 10.1016/j.brainres.2014.09.066 25312829

57. Cohen-Kadosh K, Krause B, King AJ, Near J, Cohen-Kadosh R. Linking GABA and glutamate levels to cognitive skill acquisition during development. Hum Brain Mapp. 2015;36(11):4334–45. doi: 10.1002/hbm.22921 26350618

58. Bachtiar V, Near J, Johansen-Berg H, Stagg CJ. Modulation of GABA and resting state functional connectivity by transcranial direct current stimulation. Elife. 2015;4(September 2015):1–9.

59. Turrigiano GG, Nelson SB. Hebb and homeostasis in neuronal plasticity. Curr Opin Neurobiol. 2000;10(3):358–64. doi: 10.1016/s0959-4388(00)00091-x 10851171

60. Krause B, Márquez-Ruiz J, Cohen Kadosh R. The effect of transcranial direct current stimulation: a role for cortical excitation/inhibition balance? Front Hum Neurosci. 2013;7(September):1–4.

61. Lebel C, Walker L, Leemans A, Phillips L, Beaulieu C. Microstructural maturation of the human brain from childhood to adulthood. Neuroimage. 2008;40(3):1044–55. doi: 10.1016/j.neuroimage.2007.12.053 18295509

62. Ciechanski P, Zewdie E, Kirton A. Developmental profile of motor cortex transcallosal inhibition in children and adolescents. J Neurophysiol. 2017;118(1):140–8. doi: 10.1152/jn.00076.2017 28381485

63. Schambra HM, Abe M, Luckenbaugh DA, Reis J, Krakauer JW, Cohen LG. Probing for hemispheric specialization for motor skill learning: a transcranial direct current stimulation study. J Neurophysiol. 2011;106(2):652–61. doi: 10.1152/jn.00210.2011 21613597

64. Kirton A, deVeber G, Gunraj C, Chen R. Cortical excitability and interhemispheric inhibition after subcortical pediatric stroke: Plastic organization and effects of rTMS. Clin Neurophysiol. 2010;121(11):1922–9. doi: 10.1016/j.clinph.2010.04.021 20537584

65. Patel HJ, Romanzetti S, Pellicano A, Nitsche MA, Reetz K, Binkofski F. Proton Magnetic Resonance Spectroscopy of the motor cortex reveals long term GABA change following anodal Transcranial Direct Current Stimulation. Sci Rep. 2019;9(1):2807. doi: 10.1038/s41598-019-39262-7 30808895

66. Hone-Blanchet A, Edden R, Fecteau S. Online Effects of Transcranial Direct Current Stimulation in Real Time on Human Prefrontal and Striatal Metabolites. Biol Psychiatry. 2016;80(6):432–8. doi: 10.1016/j.biopsych.2015.11.008 26774968

67. Ryan K, Wawrzyn K, Gati JS, Chronik BA, Wong D, Duggal N, et al. 1H MR spectroscopy of the motor cortex immediately following transcranial direct current stimulation at 7 Tesla. PLoS One. 2018;13(8):1–14.

68. Dwyer GE, Craven AR, Hirnstein M, Kompus K, Assmus J, Ersland L, et al. No Effects of Anodal tDCS on Local GABA and Glx Levels in the Left Posterior Superior Temporal Gyrus. Front Neurol. 2019;9(January):1–10.

69. Auvichayapat P, Aree-uea B, Auvichayapat N, Phuttharak W, Janyacharoen T, Tunkamnerdthai O, et al. Transient Changes in Brain Metabolites after Transcranial Direct Current Stimulation in Spastic Cerebral Palsy: A Pilot Study. Front Neurol. 2017;8(July):1–9. doi: 10.3389/fneur.2017.00001

70. Foerster BR, Nascimento TD, DeBoer M, Bender MA, Rice IC, Truong DQ, et al. Brief report: Excitatory and inhibitory brain metabolites as targets of motor cortex transcranial direct current stimulation therapy and predictors of its efficacy in fibromyalgia. Arthritis Rheumatol. 2015;67(2):576–81. doi: 10.1002/art.38945 25371383

71. Boissy P, Bourbonnais D, Kaegi C, Gravel D, Arsenault BA. Characterization of global synkineses during hand grip in hemiparetic patients. Arch Phys Med Rehabil. 1997;78(10):1117–24. doi: 10.1016/s0003-9993(97)90138-6 9339163

72. Nitsche MA, Paulus WJ. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol. 2000;527(3):633–9.

73. Antal A, Kincses TZ, Nitsche MA, Paulus WJ. Manipulation of phosphene thresholds by transcranial direct current stimulation in man. Exp Brain Res. 2003;150(3):375–8. doi: 10.1007/s00221-003-1459-8 12698316

74. Anguera JA, Russell CA, Noll DC, Seidler RD. Neural correlates associated with intermanual transfer of sensorimotor adaptation. Brain Res. 2007;1185(1):136–51.

75. Lee M, Hinder MR, Gandevia SC, Carroll TJ. The ipsilateral motor cortex contributes to cross-limb transfer of performance gains after ballistic motor practice. J Physiol. 2010;588(1):201–12.


Článok vyšiel v časopise

PLOS One


2020 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#