Experimental Brain Research

, Volume 219, Issue 3, pp 363–368 | Cite as

Modulating behavioral inhibition by tDCS combined with cognitive training

  • Thomas Ditye
  • Liron Jacobson
  • Vincent Walsh
  • Michal Lavidor
Research Article

Abstract

Cognitive training is an effective tool to improve a variety of cognitive functions, and a small number of studies have now shown that brain stimulation accompanying these training protocols can enhance their effects. In the domain of behavioral inhibition, little is known about how training can affect this skill. As for transcranial direct current stimulation (tDCS), it was previously found that stimulation over the right inferior frontal gyrus (rIFG) facilitates behavioral inhibition performance and modulates its electrophysiological correlates. This study aimed to investigate this behavioral facilitation in the context of a learning paradigm by giving tDCS over rIFG repetitively over four consecutive days of training on a behavioral inhibition task (stop signal task (SST)). Twenty-two participants took part; ten participants were assigned to receive anodal tDCS (1.5 mA, 15 min), 12 were assigned to receive training but not active stimulation. There was a significant effect of training on learning and performance in the SST, and the integration of the training and rIFG–tDCS produced a more linear learning slope. Better performance was also found in the active stimulation group. Our findings show that tDCS-combined cognitive training is an effective tool for improving the ability to inhibit responses. The current study could constitute a step toward the use of tDCS and cognitive training as a therapeutic tool for cognitive control impairments in conditions such as attention-deficit hyperactivity disorder (ADHD) or schizophrenia.

Keywords

tDCS Cognitive training Behavioral inhibition rIFG Stop signal task 

References

  1. Aron AR, Poldrack RA (2005) The cognitive neuroscience of response inhibition: relevance for genetic research in attention-deficit/hyperactivity disorder. Biol Psychiatry 57:1285–1292PubMedCrossRefGoogle Scholar
  2. Aron AR, Fletcher PC, Bullmore ET, Sahakian BJ, Robbins TW (2003) Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat Neurosci 6:115–116PubMedCrossRefGoogle Scholar
  3. Baribeau J, Ethier M, Braun C (1989) A neurophysiological assessment of selective attention before and after cognitive remediation in patients with severe closed head injury. J Neurol Rehabil 3:71–92Google Scholar
  4. Barkley RA (1997) Behavioral inhibition, sustained attention, and executive functions constructing a unifying theory of ADHD. Psychol Bull 121:65–94PubMedCrossRefGoogle Scholar
  5. Beeli G, Casutt G, Baumgartner T, Jancke L (2008) Modulating presence and impulsiveness by external stimulation of the brain. Behav Brain Funct 4:33PubMedCrossRefGoogle Scholar
  6. Ben-Yishay Y, Piasetsky EB, Rattock J (1987) A systematic method for ameliorating disorders in basic attention. In: Meyer MJ, Benton AL, Diller L (eds) Neuropsychological rehabilitation. Churchill, Edinburgh, pp 165–181Google Scholar
  7. Cohen JR, Poldrack RA (2008) Automaticity in motor sequence learning does not impair response inhibition. Psychon Bull Rev 15:108–115PubMedCrossRefGoogle Scholar
  8. Cohen-Kadosh R, Soskic S, Iuculano T, Kanai R, Walsh V (2010) Modulating neuronal activity produces specific and long-lasting changes in numerical competence. Curr Biol 20:2016–2020PubMedCrossRefGoogle Scholar
  9. Eagle DM, Baunez C, Hutcheson DM, Lehmann O, Shah AP, Robbins TW (2008) Stop-signal reaction-time task performance: role of prefrontal cortex and subthalamic nucleus cereb. Cortex 18:178–188Google Scholar
  10. Ethier M, Braun CMJ, Baribeau JMC (1989) Computer-dispensed cognitive–perceptual training of closed head injury patients after spontaneous recovery. Study 1: speeded tasks. Can J Rehabil 2:223–233Google Scholar
  11. Gray JM, Robertson I, Pentland B, Anderson S (1992) Microcomputer-based attentional retraining after brain damage: a randomised group controlled trial. Neuropsychol Rehabil 2:97–115CrossRefGoogle Scholar
  12. Hoptman MJ, Ardekani BA, Butler PD, Nierenberg J, Javitt DC, Lim KO (2004) DTI and impulsivity in schizophrenia: a first voxelwise correlational analysis. NeuroReport 15:2467–2470PubMedCrossRefGoogle Scholar
  13. Hsu TU, Tseng LY, Yu JX, Kuo WJ, Hung DL, Tzeng OJL, Walsh V, Mugletton NG, Jian CH (2011) Modulating inhibitory control with direct current stimulation of the superior medial frontal cortex. Neuroimage 56:2249–2257PubMedCrossRefGoogle Scholar
  14. Iyer MB, Mattu U, Grafman J, Lomarev M, Sato S, Wassermann EM (2005) Safety and cognitive effect of frontal DC brain polarization in healthy individuals. Neurology 64:872–875PubMedCrossRefGoogle Scholar
  15. 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 23:3380–3387PubMedCrossRefGoogle Scholar
  16. Jacobson L, Ezra A, Berger U, Lavidor M (2012) Modulating oscillatory brain activity correlates of behavioral inhibition using transcranial direct current stimulation. Clin Neurophysiol 123:979–984Google Scholar
  17. Kerns KA, Eso K, Thomson J (1999) Investigation of a direct intervention for improving attention in young children with ADHD. Dev Neuropsychol 16:273–295CrossRefGoogle Scholar
  18. Kiehl KA, Smith AM, Hare RD, Liddle PF (2000) An event-related potential (ERP) investigation of response inhibition in schizophrenia and psychopathy. Biol Psychiatry 48:210–221PubMedCrossRefGoogle Scholar
  19. Klingberg T, Forssberg H, Westerberg H (2002) Training of working memory in children with ADHD. J Clin Exp Neuropsychol 24:781–791PubMedCrossRefGoogle Scholar
  20. Klingberg T, Fernell E, Olesen PJ, Johnson M, Gustaffson P, Dahlstrom K, Gillberg CG, Forssberg H, Weserberg H (2005) Computerized training of working memory in children with ADHDa randomized, controlled trial. Child Adolesc Psychiatry 44:177–186CrossRefGoogle Scholar
  21. Li CSR, Huang C, Constable RT, Sinha R (2006) Imaging response inhibition in a stop signal task: neural correlates independent of signal monitoring and post-response processing. J Neurosci 26:186–192PubMedCrossRefGoogle Scholar
  22. Li CSR, Huang C, Yan P, Paliwal P, Constable RT, Sinha R (2008) Neural correlates of post-error slowing during a stop signal task: a functional magnetic resonance imaging study. J Cogn Neurosci 20:1021–1029PubMedCrossRefGoogle Scholar
  23. Logan GD, Burkell J (1986) Dependence and independence in responding to double stimulation: a comparison of stop, change, and dual-task paradigms. J Exp Psychol 12:549–563Google Scholar
  24. Logan GD, Cowan WB (1984) On the ability to inhibit thought and action: a theory of an act of control. Psychol Rev 91:295–327CrossRefGoogle Scholar
  25. Mateer CA, Sohlberg MM (1988) A paradigm shift in memory rehabilitation. In: Whitaker H (ed) Neuropsychological studies of nonfocal brain injury: dementia and closed head injury. Springer, New York, pp 202–225CrossRefGoogle Scholar
  26. Mateer CA, Sohlberg MM, Yougman P (1990) The management of acquired attention and memory disorders following mild closed head injury. In: Wood R (ed) Cognitive rehabilitation in perspective. Taylor & Francis, London, pp 68–95Google Scholar
  27. Monti A, Cogiamanian F, Marceglia S, Ferrucci R, Mrakic-Sposta S, Vergari M, Zago S, Priori A (2008) Improved naming after transcranial direct current stimulation in aphasia. J Neurol Neurosurg Psychiatry 79:451–453PubMedCrossRefGoogle Scholar
  28. Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527:633–639PubMedCrossRefGoogle Scholar
  29. Posner MI, Rothbart MK (2005) Influencing brain networks: implications for education. Trends Cogn Sci 9:99–103PubMedCrossRefGoogle Scholar
  30. Raskin S (1998) Investigation of P300 as a measure of efficacy of cognitive rehabilitation. Paper presented at the 26th Annual International Neuropsychological Society Conference, Honolulu, HawaiiGoogle Scholar
  31. Raskin S, Mateer CA (1993) Cognitive rehabilitation of the functional reading deficits following traumatic brain injury. Paper presented at the meeting of the American college of Rehabilitation Medicine, Denver, COGoogle Scholar
  32. Reis J, Schambra HM, Cohen LG, Bush ER, Fritsch B, Zarahn E, Celnick PA, Krakauer JW (2009) Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. PNAS 106:1590–1595PubMedCrossRefGoogle Scholar
  33. 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 113:929–938PubMedCrossRefGoogle Scholar
  34. Rosenberg D, Dick EL, O’Heam KM, Sweeney JA (1997) Response inhibition deficits in obsessive-compulsive disorder: an indicator of dysfunction in frontostriatal circuits. J Psychiatry Neurosci 22:29–38PubMedGoogle Scholar
  35. Rubia K, Russell T, Overmeyer S, Brammer MJ, Bullmore ET, Sharma T, Simmons A, Williams SCR, Giampietro V, Andrew CM, Taylor E (2001) Mapping motor inhibition: conjunctive brain activations across different versions of Go/No-Go and stop tasks. NeuroImage 13:250–261PubMedCrossRefGoogle Scholar
  36. Shalev L, Tsal Y, Mevorac C (2007) Computerized progressive attentional training (CPAT) program: effective direct intervention for children with ADHD. Child Neuropsychol 13:382–388PubMedCrossRefGoogle Scholar
  37. Sivak M, Hill CS, Henson DL, Butler BP, Silber SM, Olson PL (1984) Improved driving performance following perceptual training in persons with brain damage. Arch Physic Med Rehabil 65:163–167Google Scholar
  38. Sohlberg MM, Mateer CA (1987) Effectiveness of an attention training program. J Clin Exp Neuropsychol 19:117–130CrossRefGoogle Scholar
  39. Sturm W, Willmes K, Orgass B, Hartje W (1997) Do specific attention deficits need specific training? Neuropsychol Rehabil 7:81–106CrossRefGoogle Scholar
  40. Verbruggen F, Logan GD, Stevens M (2008) STOP-IT: windows executable software for the stop-signal paradigm. Behav Res Methods 40:479–483PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Thomas Ditye
    • 1
  • Liron Jacobson
    • 2
  • Vincent Walsh
    • 1
  • Michal Lavidor
    • 2
    • 3
    • 4
  1. 1.Institute of Cognitive NeuroscienceUniversity College LondonLondonUK
  2. 2.The Gonda Multidisciplinary Brain Research CenterBar-Ilan UniversityRamat GanIsrael
  3. 3.Department of PsychologyBar-Ilan UniversityRamat-GanIsrael
  4. 4.Department of PsychologyUniversity of HullHullUK

Personalised recommendations