Research Article

Inhibitory function and sustained attention following galvanic vestibular stimulation in children with attention-deficit/hyperactivity disorder


Background and Aim: In recent years, galvanic vestibular stimulation (GVS) has been used as an effective method in rehabilitation and treatment of psychological disorders in children and adults. This study was designed to evaluate the effect of GVS on response inhibition and susta­ined attention in children with attention-deficit/hyperactivity disorder (ADHD).
Methods: Seventeen children with ADHD, within the age range of 9−12 years, participated in this study. All participants were exposed to the go/no-go task. The behavioral outcomes and event-related potentials were recorded at baseline status, in sham condition, and after 20 minutes of exposure to GVS polarities, with an anode on the right mastoid region and a cathode on the left mastoid region.
Results: The results showed that there was a significant difference in reducing the behavioral response of the commission error (p < 0.05). But the reduction in behavioral responses to omission error and reaction time were not significant (p > 0.05). However, regarding ERPs, reduced latencies and increased amplitudes of N2 and P3 waves were observed in GVS intervention, compared to the baseline and sham conditions (p < 0.05).
Conclusion: The present results indicated the potential of GVS in improving of cognition function in children with ADHD and could help us develop a new strategy for rehabilitation of response inhibition disorders in the future.

1. Weiss G, Hechtman LT. Hyperactive children grown up: ADHD in children, adolescents, and adults. 2nd ed. London: Guilford Press; 1993.
2. Pliszka SR, Glahn DC, Semrud-Clikeman M, Franklin C, Perez 3rd R, Xiong J, et al. Neuroimaging of inhibitory control areas in children with attention deficit hyperactivity disorder who were treatment naive or in long-term treatment. Am J Psychiatry. 2006;163(6):1052-60. doi: 10.1176/ajp.2006.163.6.1052
3. Christakou A, Murphy CM, Chantiluke K, Cubillo AI, Smith AB, Giampietro V, et al. Disorder-specific functional abnormalities during sustained attention in youth with attention deficit hyperactivity disorder (ADHD) and with autism. Mol Psychiatry. 2013;18(2):236-44. doi: 10.1038/mp.2011.185
4. Avisar A, Shalev L. Sustained attention and behavioral characteristics associated with ADHD in adults. Appl Neuropsychol. 2011;18(2):107-16. doi: 10.1080/09084282.2010.547777
5. Wingen M, Kuypers KPC, van de Ven V, Formisano E, Ramaekers JG. Sustained attention and serotonin: a pharmaco‐fMRI study. Hum Psychopharmacol. 2008;23(3):221-30. doi: 10.1002/hup.923
6. Cubillo A, Halari R, smith A, Tylor E, Rubia K. A review of fronto-striatal and fronto-cortical brain abnormalities in children and adults with attention deficit hyperactivity disorder (ADHD) and new evidence for dysfunction in adults with ADHD during motivation and attention. Cortex. 2012;48(2):194-215. doi: 10.1016/j.cortex.2011.04.007
7. Blondis TA. Motor disorders and attention-deficit/hyperactivity disorder. Pediatr Clin North Am. 1999;46(5):899-913, vi-vii. doi: 10.1016/s0031-3955(05)70162-0
8. Castellanos FX, Lee PP, Sharp W, Jeffries NO, Greenstein DK, Clasen LS, et al. Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder. JAMA. 2002;288(14):1740-8. doi: 10.1001/jama.288.14.1740
9. Volkow ND, Wang G-J, Fowler JS, Telang F, Maynard L, Logan J, et al. Evidence that methylphenidate enhances the saliency of a mathematical task by increasing dopamine in the human brain. Am J Psychiatry. 2004;161(7):1173-80. doi: 10.1176/appi.ajp.161.7.1173
10. Lobel E, Kleine JF, Bihan DL, Leroy-Willig A, Berthoz A. Functional MRI of galvanic vestibular stimulation. J Neurophysiol. 1998;80(5):2699-709. doi: 10.1152/jn.1998.80.5.2699
11. Miller SM, Ngo TT. Studies of caloric vestibular stimu¬lation: implications for the cognitive neurosciences, the clinical neurosciences and neurophilosophy. Acta Neuropsychiatr. 2007;19(3):183-203. doi: 10.1111/j.1601-5215.2007.00208.x
12. Hitier M, Besnard S, Smith PF. Vestibular pathways involved in cognition. Front Integr Neurosci. 2014;8:59. doi: 10.3389/fnint.2014.00059
13. Spiegel EA, Szekely EG, Gildenberg PL. Vestibular responses in midbrain, thalamus, and basal ganglia. Arch Neurol. 1965;12:258-69. doi: 10.1001/archneur.1965.00460270034005
14. Liu Y, Hanna GL, Hanna BS, Rough HE, Arnold PD, Gehring WJ. Behavioral and electrophysiological correlates of performance monitoring and development in children and adolescents with attention-deficit/hyperactivity disorder. Brain Sci. 2020;10(2):79. doi: 10.3390/brainsci10020079
15. Oja L, Huotilainen M, Nikkanen E, Oksanen-Hennah H, Laasonen M, Voutilainen M, et al. Behavioral and electrophysiological indicators of auditory distractibility in children with ADHD and comorbid ODD. Brain Res. 2016;1632:42-50. doi: 10.1016/j.brainres.2015.12.003
16. Metin B, Roeyers H, Wiersema JR, van der Meere J, Sonuga-Barke E. A meta-analytic study of event rate effects on go/no-go performance in attention-deficit/hyperactivity disorder. Biol Psychiatry. 2012;72(12):990-6. doi: 10.1016/j.biopsych.2012.08.023
17. Marquardt L, Eichele H, Lundervold AJ, Haavik J, Eichele T. Event-related-potential (ERP) correlates of performance monitoring in adults with attention-deficit hyperactivity disorder (ADHD). Front Psychol. 2018;9:485. doi: 10.3389/fpsyg.2018.00485
18. Watter S, Geffen GM, Geffen LB. The n-back as a dual-task: P300 morphology under divided attention. Psychophysiology. 2001;38(6):998-1003. doi: 10.1111/1469-8986.3860998
19. Verleger R, Paehge T, Kolev V, Yordanova J, Jaśkowski P. On the relation of movement-related potentials to the go/no-go effect on P3. Biol Psychol. 2006;73(3):298-313. doi: 10.1016/j.biopsycho.2006.05.005
20. Smith JL, Johnstone SJ, Barry RJ. Inhibitory processing during the go/no-go task: an ERP analysis of children with attention-deficit/hyperactivity disorder. Clin Neurophysiol. 2004;115(6):1320-31. doi: 10.1016/j.clinph.2003.12.027
21. Tajik-Parvinchi D, Wright L, Schachar R. Cognitive rehabilitation for attention deficit/hyperactivity disorder (ADHD): promises and problems. J Can Acad Child Adolesc Psychiatry. 2014;23(3):207-17.
22. Ditye T, Jacobson L, Walsh V, Lavidor M. Modulating behavioral inhibition by tDCS combined with cognitive training. Exp Brain Res. 2012;219(3):363-8. doi: 10.1007/s00221-012-3098-4
23. Nejati V, Salehinejad MA, Nitsche MA, Najian A, Javadi AH. Transcranial direct current stimulation improves executive dysfunctions in ADHD: implications for inhi¬bitory control, interference control, working memory, and cognitive flexibility. J Atten Disord. 2020;24(13):1928-43. doi: 10.1177/1087054717730611
24. Dieterich M, Bense S, Lutz S, Drzezga A, Stephan T, Bartenstein P, et al. Dominance for vestibular cortical function in the non-dominant hemisphere. Cereb Cortex. 2003;13(9):994-1007. doi: 10.1093/cercor/13.9.994
25. Utz KS, Dimova V, Dimova K, Oppenländer K, Kerkhoff G. Electrified minds: transcranial direct current stimulation (tDCS) and galvanic vestibular stimulation (GVS) as methods of non-invasive brain stimulation in neuropsychology--a review of current data and future implications. Neuropsychologia. 2010;48(10):2789-810. doi: 10.1016/j.neuropsychologia.2010.06.002
26. Palm U, Hasan A, Strube W, Padberg F. tDCS for the treatment of depression: a comprehensive review. Eur Arch Psychiatry Clin Neurosci. 2016;266(8):681-94. doi: 10.1007/s00406-016-0674-9
27. Smith RC, Boules S, Mattiuz S, Youssef M, Tobe RH, Sershen H, et al. Effects of transcranial direct current stimulation (tDCS) on cognition, symptoms, and smoking in schizophrenia: a randomized controlled study. Schizophr Res. 2015;168(1-2):260-6. doi: 10.1016/j.schres.2015.06.011
28. Costanzo F, Varuzza C, Rossi S, Sdoia S, Varvara P, Oliveri M, et al. Evidence for reading improvement following tDCS treatment in children and adolescents with dyslexia. Restor Neurol Neurosci. 2016;34(2):215-26. doi: 10.3233/RNN-150561
29. American Psychiatric Association. Diagnostic and statistical manual of mental disorders (DSM-5®). 5th ed. Washington DC; American Psychiatric Association; 2013.
30. Tural Hesapçıoğlu S, Çelik C, Özmen S, Yiğit I. [Analyzing the Wechsler Intelligence Scale for Children-Revised (WISC-R) in children with attention deficit and hyperactivity disorder: predictive value of subtests, Kaufman, and Bannatyne categories]. Turk Psikiyatri Derg. 2016;27(1):31-40. Turkish. doi: 10.5080/u7985
31. Barry RJ, de Blasio FM. Performance and ERP components in the equiprobable go/no‐go task: Inhibition in children. Psychophysiology. 2015;52(9):1228-37. doi: 10.1111/psyp.12447
32. Fonteneau C, Mondino M, Arns M, Baeken C, Bikson M, Brunoni AR, et al. Sham tDCS: A hidden source of variability? Reflections for further blinded, controlled trials. Brain Stimul. 2019;12(3):668-73. doi: 10.1016/j.brs.2018.12.977
33. Homan RW, Herman J, Purdy P. Cerebral location of international 10–20 system electrode placement. Electroencephalogr Clin Neurophysiol. 1987;66(4):376-82. doi: 10.1016/0013-4694(87)90206-9
34. de Freitas Alvarenga K, Bernardez-Braga GRA, Zucki F, Luciene Duarte J, Lopes AC, Ribeiro Feniman M. Correlation analysis of the long latency auditory evoked potential N2 and cognitive P3 with the level of lead poisoning in children. Int Arch Otorhinolaryngol. 2013;17(1):41-6. doi: 10.7162/S1809-97772013000100007
35. O'Connell RG, Dockree PM, Bellgrove MA, Turin A, Ward S, Foxe JJ, et al. Two types of action error: electrophysiological evidence for separable inhibitory and sustained attention neural mechanisms producing error on go/no-go tasks. J Cogn Neurosci. 2009;21(1):93-104. doi: 10.1162/jocn.2009.21008
36. Alderson RM, Patros CHG, Tarle SJ, Hudec KL, Kasper LJ, Lea SE. Working memory and behavioral inhibition in boys with ADHD: An experimental examination of competing models. Child Neuropsychol. 2017;23(3):255-72. doi: 10.1080/09297049.2015.1105207
37. Doucet C, Stelmack RM. The effect of response execution on P3 latency, reaction time, and movement time. Psychophysiology. 1999;36(3):351-63. doi: 10.1017/s0048577299980563
38. Kappenman ES, Farrens LJ, Luck SJ, Proudfit GH. Behavioral and ERP measures of attentional bias to threat in the dot-probe task: Poor reliability and lack of correlation with anxiety. Front Psychol. 2014;5:1368. doi: 10.3389/fpsyg.2014.01368
39. Allen G, McColl R, Barnard H, Ringe WK, Fleckenstein J, Cullum CM. Magnetic resonance imaging of cerebellar–prefrontal and cerebellar–parietal functional connectivity. Neuroimage. 2005;28(1):39-48. doi: 10.1016/j.neuroimage.2005.06.013
40. Yamamoto Y, Struzik ZR, Soma R, Ohashi K, Kwak S. Noisy vestibular stimulation improves autonomic and motor responsiveness in central neurodegenerative disorders. Ann Neurol. 2005;58(2):175-81. doi: 10.1002/ana.20574
41. Phillips-Silver J, Trainor LJ. Vestibular influence on auditory metrical interpretation. Brain Cogn. 2008;67(1):94-102. doi: 10.1016/j.bandc.2007.11.007
42. Castellanos FX, Proal E. Large-scale brain systems in ADHD: beyond the prefrontal–striatal model. Trends Cogn Sci. 2012;16(1):17-26. doi: 10.1016/j.tics.2011.11.007
43. Wijesinghe R, Protti DA, Camp AJ. Vestibular interactions in the thalamus. Front Neural Circuits. 2015;9:79. doi: 10.3389/fncir.2015.00079
44. Chuang CJ, Lin PC, Hung CL, Chang YK, Hung TM. Type of physical exercise and inhibitory function in older adults: an event-related potential study. Psychology of Sport and Exercise. 2014;15(2):205-11. doi: 10.1016/j.psychsport.2013.11.005
45. Angelaki DE, Cullen KE. Vestibular system: the many facets of a multimodal sense. Annu Rev Neurosci. 2008;31:125-50. doi: 10.1146/annurev.neuro.31.060407.125555
46. Smith PF, Darlington CL, Zheng Y. Move it or lose it--is stimulation of the vestibular system necessary for normal spatial memory? Hippocampus. 2010;20(1):36-43. doi: 10.1002/hipo.20588
47. Kotchabhakdi N, Walberg F. Cerebellar afferent pro¬jections from the vestibular nuclei in the cat: an experimental study with the method of retrograde axonal transport of horseradish Exp Brain Res. 1978;31(4):591-604. doi: 10.1007/BF00239814
48. Wilkinson D, Ko P, Kilduff P, McGlinchey R, Milberg W. Improvement of a face perception deficit via subsensory galvanic vestibular stimulation. J Int Neuropsychol Soc. 2005;11(7):925-9. doi: 10.1017/s1355617705051076
49. Wilkinson D, Nicholls S, Pattenden C, Kilduff P, Milberg W. Galvanic vestibular stimulation speeds visual memory recall. Exp Brain Res. 2008;189(2):243-8. doi: 10.1007/s00221-008-1463-0
50. Wilkinson D, Zubko O, Sakel M, Coulton S, Higgins T, Pullicino P. Galvanic vestibular stimulation in hemi-spatial neglect. Front Integr Neurosci. 2014;8:4. doi: 10.3389/fnint.2014.00004
51. Lee S, Kim D, McKeown MJ. Galvanic vestibular stimulation (GVS) effects on impaired interhemispheric connectivity in Parkinson's disease. Annu Int Conf IEEE Eng Med Biol Soc. 2017;2017:2109-13. doi: 10.1109/EMBC.2017.8037270
IssueVol 30 No 3 (2021) QRcode
SectionResearch Article(s)
Galvanic vestibular stimulation attention deficit hyperactivity disorder go no go task event-related potentials motor control

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How to Cite
Hosseinabadi M, Mohammadkhani G, Rostami R, Aalmasi A. Inhibitory function and sustained attention following galvanic vestibular stimulation in children with attention-deficit/hyperactivity disorder. Aud Vestib Res. 2021;30(3):189-199.