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Modulating behavioral inhibition by tDCS combined with cognitive training

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.

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References

  • Aron AR, Poldrack RA (2005) The cognitive neuroscience of response inhibition: relevance for genetic research in attention-deficit/hyperactivity disorder. Biol Psychiatry 57:1285–1292

    PubMed  Article  Google Scholar 

  • 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 6:115–116

    PubMed  Article  CAS  Google Scholar 

  • 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 3:71–92

    Google Scholar 

  • Barkley RA (1997) Behavioral inhibition, sustained attention, and executive functions constructing a unifying theory of ADHD. Psychol Bull 121:65–94

    PubMed  Article  CAS  Google Scholar 

  • Beeli G, Casutt G, Baumgartner T, Jancke L (2008) Modulating presence and impulsiveness by external stimulation of the brain. Behav Brain Funct 4:33

    PubMed  Article  Google Scholar 

  • 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 165–181

    Google Scholar 

  • Cohen JR, Poldrack RA (2008) Automaticity in motor sequence learning does not impair response inhibition. Psychon Bull Rev 15:108–115

    PubMed  Article  Google Scholar 

  • 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 20:2016–2020

    PubMed  Article  CAS  Google Scholar 

  • 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 18:178–188

    Google Scholar 

  • 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 2:223–233

    Google Scholar 

  • Gray JM, Robertson I, Pentland B, Anderson S (1992) Microcomputer-based attentional retraining after brain damage: a randomised group controlled trial. Neuropsychol Rehabil 2:97–115

    Article  Google Scholar 

  • Hoptman MJ, Ardekani BA, Butler PD, Nierenberg J, Javitt DC, Lim KO (2004) DTI and impulsivity in schizophrenia: a first voxelwise correlational analysis. NeuroReport 15:2467–2470

    PubMed  Article  Google Scholar 

  • 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 56:2249–2257

    PubMed  Article  Google Scholar 

  • 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 64:872–875

    PubMed  Article  CAS  Google Scholar 

  • 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 23:3380–3387

    PubMed  Article  Google Scholar 

  • Jacobson L, Ezra A, Berger U, Lavidor M (2012) Modulating oscillatory brain activity correlates of behavioral inhibition using transcranial direct current stimulation. Clin Neurophysiol 123:979–984

    Google Scholar 

  • Kerns KA, Eso K, Thomson J (1999) Investigation of a direct intervention for improving attention in young children with ADHD. Dev Neuropsychol 16:273–295

    Article  Google Scholar 

  • Kiehl KA, Smith AM, Hare RD, Liddle PF (2000) An event-related potential (ERP) investigation of response inhibition in schizophrenia and psychopathy. Biol Psychiatry 48:210–221

    PubMed  Article  CAS  Google Scholar 

  • Klingberg T, Forssberg H, Westerberg H (2002) Training of working memory in children with ADHD. J Clin Exp Neuropsychol 24:781–791

    PubMed  Article  Google Scholar 

  • 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 44:177–186

    Article  Google Scholar 

  • 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 26:186–192

    PubMed  Article  CAS  Google Scholar 

  • 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 20:1021–1029

    PubMed  Article  CAS  Google Scholar 

  • 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 12:549–563

    Google Scholar 

  • Logan GD, Cowan WB (1984) On the ability to inhibit thought and action: a theory of an act of control. Psychol Rev 91:295–327

    Article  Google Scholar 

  • 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 202–225

    Chapter  Google Scholar 

  • 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 68–95

    Google Scholar 

  • 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 79:451–453

    PubMed  Article  CAS  Google Scholar 

  • Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527:633–639

    PubMed  Article  CAS  Google Scholar 

  • Posner MI, Rothbart MK (2005) Influencing brain networks: implications for education. Trends Cogn Sci 9:99–103

    PubMed  Article  Google Scholar 

  • 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, Hawaii

  • 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, CO

  • 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 106:1590–1595

    PubMed  Article  CAS  Google Scholar 

  • 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

    PubMed  Article  CAS  Google Scholar 

  • 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 22:29–38

    PubMed  CAS  Google Scholar 

  • 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 13:250–261

    PubMed  Article  CAS  Google Scholar 

  • Shalev L, Tsal Y, Mevorac C (2007) Computerized progressive attentional training (CPAT) program: effective direct intervention for children with ADHD. Child Neuropsychol 13:382–388

    PubMed  Article  Google Scholar 

  • 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 65:163–167

    CAS  Google Scholar 

  • Sohlberg MM, Mateer CA (1987) Effectiveness of an attention training program. J Clin Exp Neuropsychol 19:117–130

    Article  Google Scholar 

  • Sturm W, Willmes K, Orgass B, Hartje W (1997) Do specific attention deficits need specific training? Neuropsychol Rehabil 7:81–106

    Article  Google Scholar 

  • Verbruggen F, Logan GD, Stevens M (2008) STOP-IT: windows executable software for the stop-signal paradigm. Behav Res Methods 40:479–483

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

TD, VW, and ML are members of the Marie Curie ITN-LAN network funded by the EC. LJ and ML are supported by an ERC start-up grant awarded to ML. VW is supported a Royal Society Industry Fellow.

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Correspondence to Michal Lavidor.

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Thomas Ditye and Liron Jacobson contributed equally to this work.

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Ditye, T., Jacobson, L., Walsh, V. et al. Modulating behavioral inhibition by tDCS combined with cognitive training. Exp Brain Res 219, 363–368 (2012). https://doi.org/10.1007/s00221-012-3098-4

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  • DOI: https://doi.org/10.1007/s00221-012-3098-4

Keywords

  • tDCS
  • Cognitive training
  • Behavioral inhibition
  • rIFG
  • Stop signal task