Abstract
Many situations in our everyday life call for a mechanism deputed to outright stop an ongoing course of action. This behavioral inhibition ability, known as response stopping, is often impaired in psychiatric conditions characterized by impulsivity and poor inhibitory control. Transcranial direct current stimulation (tDCS) has recently been proposed as a tool for modulating response stopping in such clinical populations, and previous studies in healthy humans have already shown that this noninvasive brain stimulation technique is effectively able to improve response stopping, as measured in a stop-signal task (SST) administered immediately after the stimulation. So far, the right inferior frontal gyrus (rIFG) has been the main focus of these attempts to modulate response stopping by the means of noninvasive brain stimulation. However, other cortical areas such as the right dorsolateral prefrontal cortex (rDLPFC) have been implicated in inhibitory control with other paradigms. In order to provide new insight about the involvement of these areas in response stopping, in the present study, tDCS was delivered to 115 healthy subjects, using five stimulation setups that differed in terms of target area (rIFG or rDLPFC) and polarity of stimulation (anodal, cathodal, or sham). The SST was performed 15 min after the offset of the stimulation. Consistently with previous studies, only anodal stimulation over rIFG induced a reliable, although weak, improvement in the SST, which was specific for response stopping, as it was not mirrored in more general reaction time measures.
Similar content being viewed by others
References
Anderson MC (2003) Rethinking interference theory: executive control and the mechanisms of forgetting. J Mem Lang 49:415–445
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
Aron AR, Behrens TE, Smith S, Frank MJ, Poldrack RA (2007) Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI. J Neurosci 27:3743–3752
Aron AR, Robbins T, Poldrack RA (2014) Inhibition and the right inferior frontal cortex: one decade on. Trends Cogn Sci 18:177–185
Banich MT, Depue B (2015) Recent advances in understanding neural systems that support inhibitory control. Curr Opin Behav Sci 1:17–22
Batsikadze G, Moliadze V, Paulus W, Kuo M-F, Nitsche MA (2013) Partially non-linear stimulation intensity-dependent effects of direct current stimulation on motor cortex excitability in humans. J Physiol 591:1987–2000
Beeli G, Casutt G, Baumgartner T, Jäncke L (2008) Modulating presence and impulsiveness by external stimulation of the brain. Behav Brain Funct 4:33
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57:289–300
Bermpohl F, Fregni F, Boggio PS, Thut G, Northoff G, Otachi PTM, Rigonatti SP, Marcolin MA, Pascual-Leone A (2006) Effect of low-frequency transcranial magnetic stimulation on an affective go/no-go task in patients with major depression: role of stimulation site and depression severity. Psychiatry Res 141:1–13
Berryhill ME, Peterson DJ, Jones KT, Stephens JA (2014) Hits and misses: leveraging tDCS to advance cognitive research. Front Psychol 5:800. doi:10.3389/fpsyg.2014.00800
Betta E, Galfano G, Turatto M (2007) Microsaccadic response during inhibition of return in a target-target paradigm. Vision Res 47:428–436
Bikson M, Datta A, Elwassif M (2009) Establishing safety limits for transcranial direct current stimulation. Clin Neurophysiol 120:1033–1034
Boisseau CL, Thompson-Brenner H, Caldwell-Harris C, Pratt E, Farchione T, Harrison Barlow D (2012) Behavioral and cognitive impulsivity in obsessive–compulsive disorder and eating disorders. Psychiatry Res 200:1062–1066
Brunoni AR, Shiozawa P, Truong D, Javitt DC, Elkis H, Fregni F, Bikson M (2014) Understanding tDCS effects in schizophrenia: a systematic review of clinical data and an integrated computation modeling analysis. Expert Rev Med Devices 11:383–394
Chambers CD, Bellgrove MA, Stokes MG, Henderson TR, Garavan H, Robertson IH, Morris AP, Mattingley JB (2006) Executive “brake failure” following deactivation of human frontal lobe. J Cogn Neurosci 18:444–455
Chevrier AD, Noseworthy MD, Schachar R (2007) Dissociation of response inhibition and performance monitoring in the stop signal task using event-related fMRI. Hum Brain Mapp 28:1347–1358
Chikazoe J, Jimura K, Hirose S, Yamashita K, Miyashita Y, Konishi S (2009) Preparation to inhibit a response complements response inhibition during performance of a stop-signal task. J Neurosci 29:15870–15877
Cunillera T, Fuentemilla L, Brignani D, Cucurell D, Miniussi C (2014) A simultaneous modulation of reactive and proactive inhibition processes by anodal tDCS on the right inferior frontal cortex. PLoS ONE 9:e113537. doi:10.1371/journal.pone.0113537
Depue BE, Burgess EG, Willcutt L, Ruzic MT, Banich MT (2010) Inhibitory control of memory retrieval and motor processing associated with the right lateral prefrontal cortex: evidence from deficits in individuals with ADHD. Neuropsychologia 48:3909–3917
Ditye T, Jacobson L, Walsh V, Lavidor M (2012) Modulating behavioral inhibition by tDCS combined with cognitive training. Exp Brain Res 219:363–368
Enticott PG, Ogloff JRP, Bradshaw JL (2008) Response inhibition and impulsivity in schizophrenia. Psychiatry Res 157:251–254
Falcone B, Coffman B, Clark VP, Parasuraman R (2012) Transcranial direct current stimulation augments sensitivity and 24-hour retention in a complex threat detection task. PLoS ONE 7:e34993. doi:10.1371/journal.pone.0034993
Feil J, Zangen A (2010) Brain stimulation in the study and treatment of addiction. Neurosci Biobehav Rev 34:559–574
Fertonani A, Rosini S, Cotelli M, Rossini PM, Miniussi C (2010) Naming facilitation induced by transcranial direct current stimulation. Behav Brain Res 208:311–318
Fillmore MT, Rush CR (2002) Impaired inhibitory control of behavior in chronic cocaine users. Drug Alcohol Depend 66:265–273
Galfano G, Betta E, Turatto M (2004) Inhibition of return in microsaccades. Exp Brain Res 159:400–404
Hsu T-Y, Tseng L-Y, Yu J-X, Kuo W-J, Hung DL, Tzeng OJL, Walsh V, Muggleton NG, Juan Juan C-H (2011) Modulating inhibitory control with direct current stimulation of the superior medial frontal cortex. Neuroimage 56:2249–2257
Hughes ME, Budd TW, Fulham WR, Lancaster S, Woods W, Rossell SL, Michie PT (2014) Sustained brain activation supporting stop-signal task performance. Eur J Neurosci 39:1363–1369
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
Jacobson L, Ezra A, Berger U, Lavidor M (2012a) Modulating oscillatory brain activity correlates of behavioral inhibition using transcranial direct current stimulation. Clin Neurophysiol 123:979–984
Jacobson L, Koslowsky M, Lavidor M (2012b) tDCS polarity effects in motor and cognitive domains: a meta-analytical review. Exp Brain Res 216:1–10
Jasper H (1958) The ten-twenty system of the International Federation. Electroencephalogr Clin Neurophysiol 10:371–375
Juan C-H, Muggleton NG (2012) Brain stimulation and inhibitory control. Brain Stimul 5:63–69
Jung Y-J, Kim J-H, Im C-H (2013) COMETS: A MATLAB toolbox for simulating local electric fields generated by transcranial Direct Current Stimulation (tDCS). Biomed Eng Lett 3:39–46
Krause B, Cohen Kadosh R (2013) Can transcranial electrical stimulation improve learning difficulties in atypical brain development? A future possibility for cognitive training. Dev Cogn Neurosci 6:176–194
Kuhl BA, Dudukovic NM, Kahn I, Wagner A (2007) Decreased demands on cognitive control reveal the neural processing benefits of forgetting. Nat Neurosci 10:908–914
Li CSR, Huang C, Constable RT, Sinha R (2006) Imaging response inhibition in a stop-signal task: neural correlates of signal monitoring and post-response processing. J Neurosci 26:186–192
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
Metuki N, Sela T, Lavidor M (2012) Enhancing cognitive control components of insight problem solving by anodal tDCS of the left dorsolateral prefrontal cortex. Brain Stimul 5:110–115
Nitsche MA, Liebetanz D, Lang N, Antal A, Tergau F, Paulus W (2003) Safety criteria for transcranial direct current stimulation (tDCS) in humans. Clin Neurophysiol 114:220–222
Nitsche MA, Doemkes S, Karakose T, Antal A, Liebetanz D, Lang N, Tergau F, Paulus W (2007) Shaping the effects of transcranial direct current stimulation of the human motor cortex. J Neurophysiol 97:3109–3117
Osman A, Kornblum S, Meyer DE (1986) The point of no return in choice reaction time: controlled and ballistic stages of response preparation. J Exp Psychol Hum Percept Perform 12:243–258
Pastore M, Nucci M, Galfano G (2008) Comparing different methods for multiple testing in reaction time data. J Mod App Stat Meth 7:120–139
Penolazzi B, Di Domenico A, Marzoli D, Mammarella N, Fairfield B, Franciotti R, Brancucci A, Tommasi L (2010) Effects of transcranial direct current stimulation on episodic memory related to emotional visual stimuli. PLoS ONE 5:e10623. doi:10.1371/journal.pone.0010623
Penolazzi B, Pastore M, Mondini S (2013) Electrode montage dependent effects of transcranial direct current stimulation on semantic fluency. Behav Brain Res 248:129–135
Penolazzi B, Stramaccia DF, Braga M, Mondini S, Galfano G (2014) Human memory retrieval and inhibitory control in the brain: beyond correlational evidence. J Neurosci 34:6606–6610
Schall JD, Godlove DC (2012) Current advances and pressing problems in studies of stopping. Curr Opin Neurobiol 22:1012–1021
Stefan K, Cohen LG, Duque J, Mazzocchio R, Celnik P, Sawaki L, Ungerleider L, Classen J (2005) Formation of a motor memory by action observation. J Neurosci 25:9339–9346
Swick D, Chatham CH (2014) Ten years of inhibition revisited. Front Hum Neurosci 8:329. doi:10.3389/fnhum.2014.00329
Swick D, Ashley V, Turken U (2011) Are the neural correlates of stopping and not going identical? Quantitative meta-analysis of two response inhibition tasks. Neuroimage 56:1655–1665
Vannorsdall TD, Schretlen DJ, Andrejczuk M, Ledoux K, Bosley LV, Weaver JR, Skolasky RL, Gordon B (2012) Altering automatic verbal processes with transcranial direct current stimulation. Front Psychiatry 3:73
Verbruggen F, Logan GD, Stevens MA (2008) STOP-IT: windows executable software for the stop-signal paradigm. Behav Res Methods 40:479–483
Wu M, Giel KE, Skunde M, Schag K, Rudofsky G, de Zwaan M, Zipfel S, Herzog W, Friederich HC (2013) Inhibitory control and decision making under risk in bulimia nervosa and binge-eating disorder. Int J Eat Disord 46:721–728
Acknowledgments
Part of this research was funded by grants awarded from the University of Padua to G.G., B.P., and S.M.
Conflict of interest
None of the authors have potential conflicts of interest to be disclosed.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Stramaccia, D.F., Penolazzi, B., Sartori, G. et al. Assessing the effects of tDCS over a delayed response inhibition task by targeting the right inferior frontal gyrus and right dorsolateral prefrontal cortex. Exp Brain Res 233, 2283–2290 (2015). https://doi.org/10.1007/s00221-015-4297-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-015-4297-6