Vocal response inhibition is enhanced by anodal tDCS over the right prefrontal cortex

Abstract

Stopping outright (reactive inhibition) and slowing down (proactive inhibition) are types of response inhibition which have mainly been investigated in the manual effector system. This study compared reactive inhibition across manual and vocal effector systems, examined the effects of excitatory anodal transcranial direct current stimulation (anodal tDCS) over the right prefrontal cortex (right-PFC) and looked at the relationship between reactive and proactive inhibition. We hypothesised (1) that vocal reactive inhibition would be less effective than manual reactive inhibition as evidenced by longer stop signal reaction times; (2) that anodal tDCS would enhance both vocal and manual reactive inhibitions and (3) that proactive and reactive inhibitions would be positively related. We tested 14 participants over two sessions (one session with anodal tDCS and one session with sham stimulation) and applied stimulation protocol in the middle of the session, i.e. only during the second of three phases. We used a stop signal task across two stop conditions: relevant and irrelevant stop conditions in which stopping was required or ignored, respectively. We found that reactive inhibition was faster during and immediately after anodal tDCS relative to sham. We also found that greater level of proactive inhibition enhanced reactive inhibition (indexed by shorter stop signal reaction times). These results support the hypothesis that the right-PFC is part of a core network for reactive inhibition and supports previous contention that proactive inhibition is possibly modulated via preactivating the reactive inhibition network.

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References

  1. Aron AR (2011) From reactive to proactive and selective control: developing a richer model for stopping inappropriate responses. Biol Psychiatr 69(12):e55–e68. doi:10.1016/j.biopsych.2010.07.024

    Article  Google Scholar 

  2. Aron AR, Poldrack RA (2005) The cognitive neuroscience of response inhibition: relevance for genetic research in Attention-Deficit/Hyperactivity Disorder. Biol Psychiatr 57(11):1285–1292. doi:10.1016/j.biopsych.2004.10.026

    Article  Google Scholar 

  3. 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(2):115–116. doi:10.1038/nn1003

    PubMed  CAS  Article  Google Scholar 

  4. Aron AR, Robbins TW, Poldrack RA (2004) Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8(4):170–177. doi:10.1016/j.tics.2004.02.010

    PubMed  Article  Google Scholar 

  5. 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(14):3743–3752. doi:10.1523/jneurosci.0519-07.2007

    PubMed  CAS  Article  Google Scholar 

  6. Barkley RA (1997) Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol Bull 121(1):65–94. doi:10.1037/0033-2909.121.1.65

    PubMed  CAS  Article  Google Scholar 

  7. Beeli G, Casutt G, Baumgartner T, Jäncke L (2008) Modulating presence and impulsiveness by external stimulation of the brain. Behav Brain Funct 4:33. doi:10.1186/1744-9081-4-33

    PubMed  PubMed Central  Article  Google Scholar 

  8. Bissett PG, Logan GD (2014) Selective stopping? Maybe not. J Exp Psychol Gen 143(1):455–472. doi:10.1037/a0032122

    PubMed  PubMed Central  Article  Google Scholar 

  9. Bohne A, Savage CR, Deckersbach T, Keuthen NJ, Wilhelm S (2008) Motor inhibition in trichotillomania and obsessive-compulsive disorder. J Psychiatr Res 42(2):141–150. doi:10.1016/j.jpsychires.2006.11.008

    PubMed  Article  Google Scholar 

  10. Boucher L, Stuphorn V, Logan G, Schall J, Palmeri T (2007) Stopping eye and hand movements: are the processes independent? Percept Psychophys 69(5):785–801. doi:10.3758/BF03193779

    PubMed  Article  Google Scholar 

  11. Cai W, Oldenkamp CL, Aron AR (2012) Stopping speech suppresses the task-irrelevant hand. Brain Lang 120(3):412–415. doi:10.1016/j.bandl.2011.11.006

    PubMed  PubMed Central  Article  Google Scholar 

  12. Castro-Meneses LJ, Johnson BW, Sowman PF (2015) The effects of impulsivity and proactive inhibition on reactive inhibition and the go process: insights from vocal and manual stop signal tasks. Front Hum Neurosci 9. doi:10.3389/fnhum.2015.00529

  13. Chambers CD, Bellgrove MA, Stokes MG, Henderson TR, Garavan H, Robertson IH, Mattingley JB (2006) Executive “Brake Failure” following deactivation of human frontal lobe. J Cogn Neurosci 18(3):444–455. doi:10.1162/089892906775990606

    PubMed  Google Scholar 

  14. Chambers CD, Bellgrove MA, Gould IC, English T, Garavan H, McNaught E, Mattingley JB (2007) Dissociable mechanisms of cognitive control in prefrontal and premotor cortex. J Neurophysiol 98(6):3638–3647. doi:10.1152/jn.00685.2007

    PubMed  Article  Google Scholar 

  15. Chambers CD, Garavan H, Bellgrove MA (2009) Insights into the neural basis of response inhibition from cognitive and clinical neuroscience. Neurosci Biobehav Rev 33(5):631–646. doi:10.1016/j.neubiorev.2008.08.016

    PubMed  Article  Google Scholar 

  16. Chikazoe J, Jimura K, Hirose S, Yamashita K-I, Miyashita Y, Konishi S (2009) Preparation to inhibit a response complements response inhibition during performance of a stop-signal task. J Neurosci 29(50):15870–15877. doi:10.1523/jneurosci.3645-09.2009

    PubMed  CAS  Article  Google Scholar 

  17. Cruccu G, Inghilleri M, Berardelli A, Romaniello A, Manfredi M (1997) Cortical mechanisms mediating the inhibitory period after magnetic stimulation of the facial motor area. Muscle Nerve 20(4):418–424. doi:10.1002/(SICI)1097-4598(199704)20:4<418:AID-MUS3>3.0.CO;2-D

    PubMed  CAS  Article  Google Scholar 

  18. Curtis CE, Cole MW, Rao VY, D’Esposito M (2005) Canceling planned action: an fMRI study of countermanding saccades. Cereb Cortex 15(9):1281–1289. doi:10.1093/cercor/bhi011

    PubMed  Article  Google Scholar 

  19. Ditye T, Jacobson L, Walsh V, Lavidor M (2012) Modulating behavioral inhibition by tDCS combined with cognitive training. Exp Brain Res 219(3):363–368. doi:10.1007/s00221-012-3098-4

    PubMed  Article  Google Scholar 

  20. Eggers K, De Nil LF, Van den Bergh BRH (2013) Inhibitory control in childhood stuttering. J Fluency Disord 38(1):1–13. doi:10.1016/j.jfludis.2012.10.001

    PubMed  Article  Google Scholar 

  21. Enticott PG, Ogloff JRP, Bradshaw JL (2008) Response inhibition and impulsivity in schizophrenia. Psychiatr Res 157(1):251–254. doi:10.1016/j.psychres.2007.04.007

    Article  Google Scholar 

  22. Etchell AC, Sowman PF, Johnson BW (2012) “Shut up!” An electrophysiological study investigating the neural correlates of vocal inhibition. Neuropsychologia 50(1):129–138. doi:10.1016/j.neuropsychologia.2011.11.009

    PubMed  Article  Google Scholar 

  23. Filevich E, Kühn S, Haggard P (2012) Negative motor phenomena in cortical stimulation: implications for inhibitory control of human action. Cortex 48(10):1251–1261. doi:10.1016/j.cortex.2012.04.014

    PubMed  Article  Google Scholar 

  24. Filmer HL, Mattingley JB, Marois R, Dux PE (2013) Disrupting prefrontal cortex prevents performance gains from sensory-motor training. J Neurosci 33(47):18654–18660. doi:10.1523/jneurosci.2019-13.2013

    PubMed  CAS  Article  Google Scholar 

  25. Giglia G, Brighina F, Rizzo S, Puma A, Indovino S, Maccora S, Fierro B (2014) Anodal transcranial direct current stimulation of the right dorsolateral prefrontal cortex enhances memory-guided responses in a visuospatial working memory task. Funct Neurol 29(3):189–193

    PubMed  PubMed Central  Google Scholar 

  26. Glass JM, Williams DA, Fernandez-Sanchez M-L, Kairys A, Barjola P, Heitzeg MM, Schmidt-Wilcke T (2011) Executive function in chronic pain patients and healthy controls: different cortical activation during response inhibition in fibromyalgia. J Pain 12(12):1219–1229. doi:10.1016/j.jpain.2011.06.007

    PubMed  PubMed Central  Article  Google Scholar 

  27. Hsu T-Y, Tseng L-Y, Yu J-X, Kuo W-J, Hung DL, Tzeng OJL, Juan C-H (2011) Modulating inhibitory control with direct current stimulation of the superior medial frontal cortex. NeuroImage 56(4):2249–2257. doi:10.1016/j.neuroimage.2011.03.059

    PubMed  Article  Google Scholar 

  28. Jaberzadeh S, Sakuma S, Zoghi M, Miles TS, Nordstrom MA (2008) Focal transcranial magnetic stimulation of motor cortex evokes bilateral and symmetrical silent periods in human masseter muscles. Clin Neurophysiol 119(3):693–703. doi:10.1016/j.clinph.2007.11.005

    PubMed  Article  Google Scholar 

  29. 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. doi:10.1162/jocn_a_00020

    PubMed  Article  Google Scholar 

  30. Jaffard M, Longcamp M, Velay J-L, Anton J-L, Roth M, Nazarian B, Boulinguez P (2008) Proactive inhibitory control of movement assessed by event-related fMRI. NeuroImage 42(3):1196–1206. doi:10.1016/j.neuroimage.2008.05.041

    PubMed  Article  Google Scholar 

  31. Jahfari S, Stinear CM, Claffey M, Verbruggen F, Aron AR (2010) Responding with restraint: what are the neurocognitive mechanisms? J Cogn Neurosci 22(7):1479–1492. doi:10.1162/jocn.2009.21307

    PubMed  PubMed Central  Article  Google Scholar 

  32. Jasper HH (1958) The ten-twenty electrode system of the International Federation. Electroencephalogr Clin Neurophysiol 10:371–375

    Google Scholar 

  33. Jongsma ML, Postma SA, Souren P, Arns M, Gordon E, Vissers K, van Goor H (2011) Neurodegenerative properties of chronic pain: cognitive decline in patients with chronic pancreatitis. PLoS ONE. doi:10.1371/journal.pone.0023363

    Google Scholar 

  34. Juan C-H, Muggleton NG (2012) Brain stimulation and inhibitory control. Brain Stimul 5(2):63–69. doi:10.1016/j.brs.2012.03.012

    PubMed  Article  Google Scholar 

  35. Kiehl KA, Smith AM, Hare RD, Liddle PF (2000) An event-related potential investigation of response inhibition in schizophrenia and psychopathy. Biol Psychiatr 48(3):210–221. doi:10.1016/S0006-3223(00)00834-9

    CAS  Article  Google Scholar 

  36. Logan GD (1994) On the ability to inhibit thought and action: a users’ guide to the stop signal paradigm. In: Dagenbach D, Carr TH (eds) Inhibitory processes in attention, memory, and language. Academic Press, San Diego, pp 189–239

    Google Scholar 

  37. Logan GD, Cowan WB (1984) On the ability to inhibit thought and action: a theory of an act of control. Psychol Rev 91(3):295–327. doi:10.1037/0033-295x.91.3.295

    Article  Google Scholar 

  38. Logan GD, Irwin DE (2000) Don’t look! Don’t touch! Inhibitory control of eye and hand movements. Psychon Bull Rev 7(1):107–112. doi:10.3758/BF03210728

    PubMed  CAS  Article  Google Scholar 

  39. Logan GD, Schachar RJ, Tannock R (1997) Impulsivity and inhibitory control. Psychol Sci 8(1):60–64. doi:10.1111/j.1467-9280.1997.tb00545.x

    Article  Google Scholar 

  40. Luschei ES, Goldberg LJ (2011) Neural mechanisms of mandibular control: Mastication and voluntary biting. Compr Physiol. John Wiley & Sons, Inc

  41. Menzies L, Achard S, Chamberlain SR, Fineberg N, Chen CH, del Campo N, Bullmore E (2007) Neurocognitive endophenotypes of obsessive-compulsive disorder. Brain 130(Pt 12):3223–3236. doi:10.1093/brain/awm205

    PubMed  Article  Google Scholar 

  42. Ortu E, Deriu F, Suppa A, Giaconi E, Tolu E, Rothwell JC (2008) Intracortical modulation of cortical-bulbar responses for the masseter muscle. J Physiol 586(14):3385–3404. doi:10.1113/jphysiol.2008.153288

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  43. 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 Percep Perform 12(3):243–258. doi:10.1037/0096-1523.12.3.243

    CAS  Article  Google Scholar 

  44. Osman A, Kornblum S, Meyer DE (1990) Does motor programming necessitate response execution? J Exp Psychol Hum Percep Perform 16(1):183–198. doi:10.1037/0096-1523.16.1.183

    CAS  Article  Google Scholar 

  45. Paradiso GO, Cunic DI, Gunraj CA, Chen R (2005) Representation of facial muscles in human motor cortex. J Physiol 567(1):323–336. doi:10.1113/jphysiol.2005.088542

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  46. Penadés R, Catalán R, Rubia K, Andrés S, Salamero M, Gastó C (2007) Impaired response inhibition in obsessive compulsive disorder. Eur Psychiar 22(6):404–410. doi:10.1016/j.eurpsy.2006.05.001

    Article  Google Scholar 

  47. Rubia K, Russell T, Overmeyer S, Brammer MJ, Bullmore ET, Sharma T, Taylor E (2001) Mapping motor inhibition: conjunctive brain activations across different versions of Go/No-Go and stop tasks. NeuroImage 13(2):250–261. doi:10.1006/nimg.2000.0685

    PubMed  CAS  Article  Google Scholar 

  48. Rubia K, Smith AB, Brammer MJ, Taylor E (2003) Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection. NeuroImage 20(1):351–358. doi:10.1016/S1053-8119(03)00275-1

    PubMed  Article  Google Scholar 

  49. Sandler AD (2003) Tics and problem behaviors in schoolchildren: prevalence, characterization, and associations. J Dev Behav Pediatr 24(1):84

    Article  Google Scholar 

  50. Sowman PF, Flavel SC, McShane CL, Miles TS, Nordstrom MA (2008) Transcranial magnetic stimulation reduces masseter motoneuron pool excitability throughout the cortical silent period. Clin Neurophysiol 119(5):1119–1129. doi:10.1016/j.clinph.2007.12.019

    PubMed  Article  Google Scholar 

  51. Stinear CM, Coxon JP, Byblow WD (2009) Primary motor cortex and movement prevention: where Stop meets Go. Neurosci Behav Rev 33(5):662–673. doi:10.1016/j.neubiorev.2008.08.013

    Article  Google Scholar 

  52. van den Wildenberg WPM, Christoffels IK (2010) STOP TALKING! Inhibition of speech is affected by word frequency and dysfunctional impulsivity. Front Psychol 1:145. doi:10.3389/fpsyg.2010.00145

    PubMed  PubMed Central  Article  Google Scholar 

  53. Veldhuijzen DS, Sondaal SF, Oosterman JM (2012) Intact cognitive inhibition in patients with fibromyalgia but evidence of declined processing speed. J Pain 13(5):507–515. doi:10.1016/j.jpain.2012.02.011

    PubMed  Article  Google Scholar 

  54. Verbruggen F, Logan GD (2008) Response inhibition in the stop-signal paradigm. Trends Cogn Sci 12(11):418–424. doi:10.1016/j.tics.2008.07.005

    PubMed  PubMed Central  Article  Google Scholar 

  55. Verbruggen F, Logan GD (2009) Models of response inhibition in the stop-signal and stop-change paradigms. Neurosci Biobehav Rev 33(5):647–661. doi:10.1016/j.neubiorev.2008.08.014

    PubMed  PubMed Central  Article  Google Scholar 

  56. Verbruggen F, Aron AR, Stevens MA, Chambers CD (2010) Theta burst stimulation dissociates attention and action updating in human inferior frontal cortex. Proc Natl Acad Sci USA 107(31):13966–13971. doi:10.1073/pnas.1001957107

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  57. Verbruggen F, Chambers CD, Logan GD (2013) Fictitious inhibitory differences: how skewness and slowing distort the estimation of stopping latencies. Psychol Sci 24(3):352–362. doi:10.1177/0956797612457390

    PubMed  PubMed Central  Article  Google Scholar 

  58. Werhahn KJ, Classen J, Benecke R (1995) The silent period induced by transcranial magnetic stimulation in muscles supplied by cranial nerves: normal data and changes in patients. J Neurol Neurosurg Psychiatry 59(6):586–596. doi:10.1136/jnnp.59.6.586

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  59. Wessel JR, Aron AR (2014) It’s not too late: the onset of the frontocentral P3 indexes successful response inhibition in the stop-signal paradigm. Psychophysiol. doi:10.1111/psyp.12374

    Google Scholar 

  60. Xue G, Aron AR, Poldrack RA (2008) Common neural substrates for inhibition of spoken and manual responses. Cereb Cortex 18(8):1923–1932. doi:10.1093/cercor/bhm220

    PubMed  Article  Google Scholar 

  61. Ziemann U, Paulus W, Rothenberger A (1997) Decreased motor inhibition in Tourette’s disorder: evidence from transcranial magnetic stimulation. Am J Psychiatr 154(9):1277–1284. doi:10.1176/ajp.154.9.1277

    PubMed  CAS  Article  Google Scholar 

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Funding

This research was supported by Macquarie University Research Excellence Scholarships (MQRES), National Health and Medical Research Council, Australia (#1003760), and the Australian Research Council (DE130100868).

Author contributions

LCM and PFS designed the experiments, collected and analysed the data. LCM, PFS and BWJ wrote the manuscript.

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Correspondence to Leidy J. Castro-Meneses.

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The authors declare that they have no conflict of interest.

Additional information

Leidy J Castro-Meneses and Paul F. Sowman have contributed equally to this work.

Appendices

Appendix 1

See Table 1.

Table 1 Go reaction times (go-RTs), stop signal delay (SSD) and stop signal reaction times (SSRTs)

Appendix 2

See Table 2.

Table 2 Non-significant interactions for the 2 × 2 × 3 × 2 ANOVA of go-RTs

Appendix 3

Analyses of Spearman correlations between proactive and reactive inhibition.

See Table 3.

Table 3 Spearman correlations between proactive and reactive inhibition (two-tailed)

Appendix 4

Results for the 2 × 3 × 2 repeated-measures ANOVA for proactive inhibition. This ANOVA was done for the effects of two sessions (session with anodal tDCS and session with sham), three phases (phase-1, phase-2 and phase-3) and two response modalities (manual and vocal). The results showed that session had no effect on proactive inhibition.

See Table 4.

Table 4 2 × 3 × 2 repeated-measures ANOVA for proactive inhibition

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Castro-Meneses, L.J., Johnson, B.W. & Sowman, P.F. Vocal response inhibition is enhanced by anodal tDCS over the right prefrontal cortex. Exp Brain Res 234, 185–195 (2016). https://doi.org/10.1007/s00221-015-4452-0

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Keywords

  • Anodal tDCS
  • Vocal inhibition
  • Stop signal task
  • Response inhibition
  • Reactive inhibition and proactive inhibition