Abstract
Cognitive control, which has been localized to the right inferior frontal gyrus (rIFG) based on functional imaging and brain lesion studies, is impaired in patients with ADHD. The present study aims to investigate whether transcranial direct current stimulation (tDCS) over the rIFG might improve cognitive control in ADHD subjects. We hypothesized poorer performance in a cognitive control task, but not in a control language task, in the ADHD subjects. Crucially, following tDCS, we expected the ADHD group to improve their cognitive control. In a double-blind randomized control trial, 42 participants performed the stop signal task (SST) to index their cognitive control level and the language task. Half of them were randomly assigned to the anodal stimulation condition and half to the sham stimulation. The anodal or sham stimulation was applied over the right IFG. Following the stimulation, the participants reset the two tasks to see whether stimulation improved the (predicted) weaker performance in the ADHD group. Stimulation significantly enhanced cognitive control for both groups, with or without ADHD, in the SST task, but no significant stimulation effects were found for the control task. tDCS seems as a promising tool to improve cognitive control in the general population.
Similar content being viewed by others
Data availability
The data are available from the corresponding author upon reasonable request.
References
Adler LA, Spencer TJ, Levine LR et al (2008) Functional outcomes in the treatment of adults with ADHD. J Atten Disord 11(6):720–727. https://doi.org/10.1177/1087054708323006
Albonico A, Furubacke A, Barton JJS et al (2018) Perceptual efficiency and the inversion effect for faces, words and houses. Vision Res 153:91–97. https://doi.org/10.1016/j.visres.2018.09.006
Alvarez JA, Emory E (2006) Executive function and the frontal lobes: a meta-analytic review. Neuropsychol Rev 16:17–42. https://doi.org/10.1007/s11065-007-9024-z
Aron AR, Fletcher PC, Bullmore EdT et al (2003) Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat Neurosci 6(2):115–116. https://doi.org/10.1038/nn1003-115
Bandeira ID, Guimarães RS, Quadros J, Gabriel J et al (2016) Transcranial direct current stimulation in children and adolescents with attention-deficit/hyperactivity disorder (ADHD) a pilot study. J Child Neurol 31(7):918–924. https://doi.org/10.1177/0883073816648306
Barkley RA (1997) Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol Bull 121(1):65. https://doi.org/10.1037/0033-2909.121.1.65
Barkley RA (2012) Executive functions: What they are, how they work, and why they evolved. Guilford Press, New York
Barkley RA, Fischer M, Smallish L et al (2002) The persistence of attention-deficit/hyperactivity disorder into young adulthood as a function of reporting source and definition of disorder. J Abnorm Psychol 111(2):279. https://doi.org/10.1037//0021-843x.111.2.279
Biran M, Friedmann N (2004) SHEMESH: Naming a hundred objects. Tel Aviv University, Tel Aviv
Biran M, Friedmann N (2005) From phonological paraphasias to the structure of the phonological output lexicon. Lang Cognit Process 20(4):589–616. https://doi.org/10.1080/01690960444000162
Bonham MD, Shanley DC, Waters AM et al (2021) Inhibitory control deficits in children with oppositional defiant disorder and conduct disorder compared to attention deficit/hyperactivity disorder: a systematic review and meta-analysis. Res Child Adolesc Psychopathol 49:39–62. https://doi.org/10.1007/s10802-020-00737-2
Brown TE (2013) A new understanding of ADHD in children and adults: executive function impairments. Routledge, Abingdon. https://doi.org/10.4324/9780203724967
Bruce B, Thernlund G, Nettelbladt U (2006) ADHD and language impairment: a study of the parent questionnaire FTF (five to fifteen). Eur Child Et Al. Adolesc Psychiatr 15:52–60. https://doi.org/10.1007/s00787-005-0511-3
Brunoni AR, Nitsche MA, Bolognini N et al (2012) Clinical research with transcranial direct current stimulation (tDCS): challenges and future directions. Brain Stimul 5(3):175–195. https://doi.org/10.1016/j.brs.2012.02.005
Buchanan DM, D’Angiulli A, Samson A et al (2022) Acceptability of transcranial direct current stimulation in children and adolescents with ADHD: The point of view of parents. J Health Psychol 27(1):36–46. https://doi.org/10.1177/1359105320962404
Carlén M (2017) What constitutes the prefrontal cortex? Science 358(6362):478–482. https://doi.org/10.1126/science.aan8862
Castellanos FX, Proal E (2012) Large-scale brain systems in ADHD: beyond the prefrontal–striatal model. Trends Cogn Sci 16(1):17–26. https://doi.org/10.1016/j.tics.2011.11.006
Castellanos FX, Sonuga-Barke EJS, Milham MP et al (2006) Executive function: is there a central executive? Trends Cogn Sci 3(10):117–123. https://doi.org/10.1016/j.tics.2006.01.004
Castells X, Cunill R, Capellà D (2013) Treatment discontinuation with methylphenidate in adults with attention deficit hyperactivity disorder: a meta-analysis of randomized clinical trials. Eur J Clin Pharmacol 69:347–356. https://doi.org/10.1007/s00228-012-1358-0
Chamberlain SR, Robbins TW, Winder-Rhodes S et al (2011) Translational approaches to frontostriatal dysfunction in attention-deficit/hyperactivity disorder using a computerized neuropsychological battery. Biol Psychiat 69(12):1192–1203. https://doi.org/10.1016/j.biopsych.2010.08.019
Chambers CD, Bellgrove MA, Gould IC et al (2007) Dissociable mechanisms of cognitive control in prefrontal and premotor cortex. J Neurophysiol 98(6):3638–3647. https://doi.org/10.1152/jn.00685.2007
Chan RCK, Shum D, Toulopoulou T et al (2008) Assessment of executive functions: review of instruments and identification of critical issues. Arch Clin Neuropsychol 23(2):201–216. https://doi.org/10.1016/j.acn.2007.08.010
Childress AC, Sallee FR (2014) Attention-deficit/hyperactivity disorder with inadequate response to stimulants: approaches to management. CNS Drugs 28:121–129. https://doi.org/10.1007/s40263-014-0144-0
Clavenna A, Bonati M (2014) Safety of medicines used for ADHD in children: a review of published prospective clinical trials. Arch Dis Child 99(9):866–872. https://doi.org/10.1136/archdischild-2013-304456
Coffman BA, Clark VP, Parasuraman R (2014) Battery powered thought: enhancement of attention, learning, and memory in healthy adults using transcranial direct current stimulation. Neuroimage 85:895–908. https://doi.org/10.1016/j.neuroimage.2013.07.083
Coolidge FL, Wynn T (2001) Executive functions of the frontal lobes and the evolutionary ascendancy of Homo sapiens. Camb Archaeol J 11(2):255–260. https://doi.org/10.1017/S095977430100014X
Cortese S, Kelly C, Chabernaud C et al (2012) Toward systems neuroscience of ADHD: a meta-analysis of 55 fMRI studies. Am J Psychiatr 169(10):1038–1055. https://doi.org/10.1176/appi.ajp.2012.11101521
Cosmo C, Ferreira C, Miranda JG, Vivas, et al (2015) Spreading effect of tDCS in individuals with attention-deficit/hyperactivity disorder as shown by functional cortical networks: a randomized, double-blind, sham-controlled trial. Front Psych 6:111. https://doi.org/10.3389/fpsyt.2015.00111
Craig SG, Davies G, Schibuk L et al (2015) Long-term effects of stimulant treatment for ADHD: What can we tell our patients? Curr Dev Disord Rep 2:1–9. https://doi.org/10.1007/s40474-014-0031-2
Diamond A (2013) Executive functions. Annu Rev Psychol 64:135–168. https://doi.org/10.1146/annurev-psych-113011-143750
Dubreuil-Vall L, Gomez-Bernal F, Villegas AC et al (2021) Transcranial direct current stimulation to the left dorsolateral prefrontal cortex improves cognitive control in patients with attention-deficit/hyperactivity disorder: a randomized behavioral and neurophysiological study. Biol Psychiatr 6(4):439–448. https://doi.org/10.1016/j.bpsc.2020.11.016
Duncan J (1986) Disorganisation of behaviour after frontal lobe damage. Cogn Neuropsychol 3(3):271–290. https://doi.org/10.1080/02643298608252856
Ek A, Isaksson G (2013) How adults with ADHD get engaged in and perform everyday activities. Scand J Occup Ther 20(4):282–291. https://doi.org/10.3109/11038128.2013.774137
Ellioit R (2003) Executive functions and their disorders: Imaging in clinical neuroscience. Br Med Bull 65(1):49–59. https://doi.org/10.1093/bmb/65.1.49
Fayyad J, De Graaf R, Kessler R et al (2007) Cross-national prevalence and correlates of adult attention-deficit hyperactivity disorder. British J Psychiatr 190(5):402–409. https://doi.org/10.1192/bjp.bp.106.034389
Fecteau S, Knoch D, Fregni F et al (2007) Diminishing risk-taking behavior by modulating activity in the prefrontal cortex: a direct current stimulation study. J Neurosci 27(46):12500–12505. https://doi.org/10.1523/JNEUROSCI.3283-07.2007
Feeser M, Prehn K, Kazzer P et al (2014) Transcranial direct current stimulation enhances cognitive control during emotion regulation. Brain Stimul 7(1):105–112. https://doi.org/10.1016/j.brs.2013.09.008
Feldman HM, Reiff MI (2014) Attention deficit–hyperactivity disorder in children and adolescents. N Engl J Med 370(9):838–846. https://doi.org/10.1056/NEJMra1110792
Goel V, Vartanian O, Bartolo A et al (2013) Lesions to right prefrontal cortex impair real-world planning through prematurecommitments. Neuropsychologia 51(4):713–724. https://doi.org/10.1016/j.neuropsychologia.2012.12.020
Iyer MB, Mattu U, Grafman J et al (2005) Safety and cognitive effect of frontal DC brain polarization in healthy individuals. Neurology 64(5):872–875. https://doi.org/10.1212/01.WNL.0000152986.07469.E9
Jacobson L, Javitt DC, Lavidor M (2011) Activation of inhibition: diminishing impulsive behavior by direct current stimulation over the inferior frontal gyrus. J Cogn Neurosci 23(11):3380–3387. https://doi.org/10.1162/jocn_a_00012
Jacobson L, Koslowsky M, Lavidor M (2012) tDCS polarity effects in motor and cognitive domains: a meta-analytical review. Exp Brain Res 216:1–10. https://doi.org/10.1007/s00221-011-2891-9
Johnston C, Mash EJ, Miller N et al (2012) Parenting in adults with attention-deficit/hyperactivity disorder (ADHD). Clin Psychol Rev 32(4):215–228. https://doi.org/10.1016/j.cpr.2012.02.008
Keeser D, Meindl T, Bor J et al (2011) Prefrontal transcranial direct current stimulation changes connectivity of resting-state networks during fMRI. J Neurosci 31(43):15284–15293. https://doi.org/10.1523/JNEUROSCI.0542-11.2011
Kessler RC, Adler L, Ames M et al (2005) The world health organization adult ADHD self-report scale (ASRS): a short screening scale for use in the general population. Psychol Med 35(2):245–256. https://doi.org/10.1017/S0033291704002892
Klomjai W, Siripornpanich V, Aneksan B et al (2022) Effects of cathodal transcranial direct current stimulation on inhibitory and attention control in children and adolescents with attention-deficit hyperactivity disorder: a pilot randomized sham-controlled crossover study. J Psychiatr Res 150:130–141. https://doi.org/10.1016/j.jpsychires.2021.12.043
Krain AL, Castellanos FX (2006) Brain development and ADHD. Clin Psychol Rev 26(4):433–444. https://doi.org/10.1016/j.cpr.2006.01.005
Kuo MF, Paulus W, Nitsche MA (2014) Therapeutic effects of non-invasive brain stimulation with direct currents (tDCS) in neuropsychiatric diseases. Neuroimage 85(3):948–960. https://doi.org/10.1016/j.neuroimage.2013.05.117
Lefaucheur J-P, Antal A, Ayache SS et al (2017) Evidence-based guidelines on the therapeutic use of transcranial direct current stimulation (tDCS). Clin Neurophysiol 128(1):56–92. https://doi.org/10.1016/j.clinph.2016.10.087
Leffa DT, Grevet EH, Bau CHD et al (2022) Transcranial direct current stimulation vs sham for the treatment of inattention in adults with attention-deficit/hyperactivity disorder: the TUNED randomized clinical trial. JAMA Psychiatr 79(9):847–856. https://doi.org/10.1001/jamapsychiatry.2022.0567
Li P, Sepanski S, Zhao X (2006) Language history questionnaire: a web-based interface for bilingual research. Behav Res Methods 38(2):202–210
Li C-sR et al (2008) Neural correlates of post-error slowing during a stop signal task: a functional magnetic resonance imaging study. J Cogn Neurosci 20(6):1021–1029. https://doi.org/10.1162/jocn.2008.20071
Lijffijt M, Kenemans JL, Verbaten MN et al (2005) A meta-analytic review of stopping performance in attention-deficit/hyperactivity disorder: deficient inhibitory motor control? J Abnorm Psychol 114(2):216. https://doi.org/10.1037/0021-843X.114.2.216
Lipszyc J, Schachar R (2010) Inhibitory control and psychopathology: a meta-analysis of studies using the stop signal task. J Int Neuropsychol Soc 16(6):1064–1076. https://doi.org/10.1017/S1355617710001101
Logan GD, Schachar RJ, Tannock R (1997) Impulsivity and inhibitory control. Psychol Sci 8(1):60–64. https://doi.org/10.1111/j.1467-9280.1997.tb00545.x
Mannarelli D, Pauletti C, Lucia De, Maria C et al (2016) Effects of cerebellar transcranial direct current stimulation on attentional processing of the stimulus: evidence from an event-related potentials study. Neuropsychologia 84:127–135. https://doi.org/10.1016/j.neuropsychologia.2016.01.016
Mannuzza S, Klein RG, Moulton III, John L (2003) Persistence of attention-deficit/hyperactivity disorder into adulthood: what have we learned from the prospective follow-up studies? J Atten Disord 7(2):93–100. https://doi.org/10.1177/108705470300700202
Matzke D, Verbruggen F, Logan G (2018) The stop-signal paradigm. Stevens Handbook Exp Psychol Cogn Neurosci 5:383–427
Mayse JD et al (2014) Proactive and reactive inhibitory control in rats. Front Neurosci 8:104. https://doi.org/10.3389/fnins.2014.00104
Miniussi C, Ruzzoli M (2013) Transcranial stimulation and cognition. Handb Clin Neurol 116:739–750. https://doi.org/10.1016/B978-0-444-53497-2.00056-5
Miyake A, Friedman NP, Emerson MJ et al (2000) The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: a latent variable analysis. Cogn Psychol 41(1):49–100. https://doi.org/10.1006/cogp.1999.0734
Monti A, Cogiamanian F, Marceglia S et al (2008) Improved naming after transcranial direct current stimulation in aphasia. J Neurol Neurosurg Psychiatr 79(4):451–453. https://doi.org/10.1136/jnnp.2007.135277
Nejati V, Khorrami AS, Nitsche MA (2021) Transcranial direct current stimulation improves reward processing in children with ADHD. J Atten Disord 25(11):1623–1631. https://doi.org/10.1177/1087054720916997
Nelson J, McKinley RA, Golob EJ et al (2014) Modulating the prefrontal cortex during sustained attention with transcranial direct current stimulation. Neuroimage 85(10):909–917. https://doi.org/10.1016/j.neuroimage.2013.07.061
Nitsche MA, Paulus W (2001) Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57(10):1899–1901. https://doi.org/10.1212/WNL.57.10.1899
Nitsche MA, Schauenburg A, Lang N et al (2003) Facilitation of implicit motor learning by weak transcranial direct current stimulation of the primary motor cortex in the human. J Cogn Neurosci 15(4):619–626. https://doi.org/10.1162/089892903321662994
Nitsche MA, Cohen LG, Wassermann EM et al (2008) Transcranial direct current stimulation: state of the art 2008. Brain Stimul 1(3):206–223. https://doi.org/10.1016/j.brs.2008.06.004
Oosterlaan J, Logan GD, Sergeant JA (1998) Response inhibition in AD/HD, CD, comorbid AD/HD+ CD, anxious, and control children: a meta-analysis of studies with the stop task. J Child Psychol Psychiat Allied Discip 39(3):411–425. https://doi.org/10.1017/S0021963097002446
Peirce J, Hirst R, MacAskill M (2022) Building experiments in PsychoPy. Sage, Thousand Oaks
Pennington BF, Ozonoff S (1996) Executive functions and developmental psychopathology. J Child Psychol Psychiatr 37(1):51–87. https://doi.org/10.1111/j.1469-7610.1996.tb01380.x
Psychiatric, American and Association. 2013. DSM-V: Diagnostic and Statistical Manual of Mental Disorders (Reprint)
Reteig LC, Talsma LJ, Van Schouwenburg MR et al (2017) Transcranial electrical stimulation as a tool to enhance attention. J Cogn Enhanc 1:10–25. https://doi.org/10.1007/s41465-016-0009-6
Reuter M, Kirsch P, Hennig J (2006) Inferring candidate genes for attention deficit hyperactivity disorder (ADHD) assessed by the world health organization adult ADHD self-report scale (ASRS). J Neural Transm 113:929–938. https://doi.org/10.1007/s00702-005-0349-4
Sagvolden T, Sergeant JA (1998) Attention deficit/hyperactivity disorder–from brain dysfunctions to behaviour. Behav Brain Res. 94(1):1–10
Salehinejad MA, Wischnewski M, Nejati V et al (2019) Transcranial direct current stimulation in attention-deficit hyperactivity disorder: a meta-analysis of neuropsychological deficits. PloS one. https://doi.org/10.1371/journal.pone.0215095
Salehinejad MA, Vosough Y, Nejati V (2022) The impact of bilateral anodal tDCS over left and right DLPFC on executive functions in children with ADHD. Brain Sci 12(8):1098. https://doi.org/10.3390/brainsci12081098
Schneider MF, Krick CM, Retz W et al (2010) Impairment of fronto-striatal and parietal cerebral networks correlates with attention deficit hyperactivity disorder (ADHD) psychopathology in adults—a functional magnetic resonance imaging (fMRI) study. Psychiatr Res 183(1):75–84. https://doi.org/10.1016/j.pscychresns.2010.03.005
Schroeder PA, Schwippel T, Wolz I et al (2020) Meta-analysis of the effects of transcranial direct current stimulation on inhibitory control. Brain Stimul 13(5):1159–1167. https://doi.org/10.1016/j.brs.2020.05.006
Senderecka M, Grabowska A, Szewczyk J et al (2012) Response inhibition of children with ADHD in the stop-signal task: an event-related potential study. Int J Psychophysiol 85(1):93–105. https://doi.org/10.1016/j.ijpsycho.2011.11.012
Shaw M, Hodgkins P, Caci H et al (2012) A systematic review and analysis of long-term outcomes in attention deficit hyperactivity disorder: effects of treatment and non-treatment. BMC Med 10:1–15. https://doi.org/10.1186/1741-7015-10-99
Snowball A, Tachtsidis I, Popescu T et al (2013) Long-term enhancement of brain function and cognition using cognitive training and brain stimulation. Curr Biol 23(11):987–992. https://doi.org/10.1016/j.cub.2013.04.045
Soff C, Sotnikova A, Christiansen H et al (2017) Transcranial direct current stimulation improves clinical symptoms in adolescents with attention deficit hyperactivity disorder. J Neural Transm 124:133–144. https://doi.org/10.1007/s00702-016-1636-7
Soltaninejad Z, Nejati V, Ekhtiari H (2019) Effect of anodal and cathodal transcranial direct current stimulation on DLPFC on modulation of inhibitory control in ADHD. J Attention Disorders 23(4):325–332. https://doi.org/10.1177/1087054717753908
Swick D, Ashley V (2008) Left inferior frontal gyrus is critical for response inhibition. BMC Neurosci 9(1):1–11. https://doi.org/10.1186/1471-2202-9-102
Thorell LB, Wåhlstedt C (2006) Executive functioning deficits in relation to symptoms of ADHD and/or ODD in preschool children. Infant Child Dev 15(5):503–518. https://doi.org/10.1002/icd.463
Tomé D, Barbosa F, Nowak K et al (2015) The development of the N1 and N2 components in auditory oddball paradigms: a systematic review with narrative analysis and suggested normative values. J Neural Transm 122:375–391. https://doi.org/10.1007/s00702-014-1296-8
Väisänen R, Loukusa S, Moilanen I et al (2014) Language and pragmatic profile in children with ADHD measured by children’s communication checklist. Logopedics Phoniatrics Vocol 39(4):179–187. https://doi.org/10.3109/14015439.2014.882013
Verbruggen F, Logan GD (2008) Response inhibition in the stop-signal paradigm. Trends Cogn Sci 12(11):418–424
Weller S, Nitsche MA, Plewnia C (2020) Enhancing cognitive control training with transcranial direct current stimulation: a systematic parameter study. Brain Stimul 13(5):1358–1369
Westwood SJ, Radua J, Rubia K (2021) Noninvasive brain stimulation in children and adults with attention-deficit/hyperactivity disorder: a systematic review and meta-analysis. J Psychiatr Neurosci 461(2021):E14–E33. https://doi.org/10.1503/jpn.190179
Willcutt EG, Doyle AE, Nigg JT et al (2005) Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review. Biol Psychiatr 57(11):1336–1346
Acknowledgements
The authors would like to thank Yuval Levy for programming the experimental tasks.
Funding
The authors have no relevant financial or non-financial interests to disclose.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no competing interests to declare that are relevant to the content of this article. All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this manuscript. The authors have no financial or proprietary interests in any material discussed in this article.
Ethical approval
This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Bar Ilan University (Date-17.08.2022, No-2022/21).
Additional information
Communicated by Ian Greenhouse.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Weinberg, H., Baruch, Y., Tzameret, H. et al. Cognitive control enhancement in attention deficit hyperactivity disorder (ADHD) and neurotypical individuals. Exp Brain Res 241, 2381–2392 (2023). https://doi.org/10.1007/s00221-023-06695-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-023-06695-6