Advertisement

Experimental Brain Research

, Volume 234, Issue 6, pp 1525–1535 | Cite as

Event-related fields evoked by vocal response inhibition: a comparison of younger and older adults

  • Leidy J. Castro-Meneses
  • Blake W. Johnson
  • Paul F. Sowman
Research Article
  • 253 Downloads

Abstract

The current study examined event-related fields (ERFs) evoked by vocal response inhibition in a stimulus-selective stop-signal task. We compared inhibition-related ERFs across a younger and an older group of adults. Behavioural results revealed that stop-signal reaction times (RTs), go-RTs, ignore-stop RTs and failed stop RTs were longer in the older, relative to the younger group by 38, 123, 149 and 116 ms, respectively. The amplitude of the ERF M2 peak (approximately 200 ms after the stop signal) evoked on successful stop trials was larger compared to that evoked on both failed stop and ignore-stop trials. The M4 peak (approximately 450 ms after stop signal) was of larger amplitude in both successful and failed stops compared to ignore-stop trials. In the older group, the M2, M3 and M4 peaks were smaller in amplitude and peaked later in time (by 24, 50 and 76 ms, respectively). We demonstrate that vocal response inhibition-related ERFs exhibit a similar temporal evolution to those previously described for manual response inhibition: an early peak at 200 ms (i.e. M2) that differentiates successful from failed stopping, and a later peak (i.e. M4) that is consistent with a neural marker of response checking and error processing. Across groups, our data support a more general decline of stimulus processing speed with age.

Keywords

Response inhibition Speech Magnetoencephalography Event-related fields Ageing and stop-signal task 

Notes

Acknowledgments

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).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

221_2016_4555_MOESM1_ESM.docx (43 kb)
Supplementary material 1 (DOCX 43 kb)

References

  1. Aron AR (2011) From reactive to proactive and selective control: developing a richer model for stopping inappropriate responses. Biol Psychiatry 69(12):e55–e68. doi: 10.1016/j.biopsych.2010.07.024 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bedard A-C, Nichols S, Barbosa JA, Schachar R, Logan GD, Tannock R (2002) The development of selective inhibitory control across the life span. Dev Neuropsychol 21(1):93–111. doi: 10.1207/S15326942DN2101_5 CrossRefPubMedGoogle Scholar
  3. Bissett PG, Logan GD (2014) Selective stopping? Maybe not. J Exp Psychol Gen 143(1):455–472. doi: 10.1037/a0032122 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Boehler CN, Munte TF, Krebs RM, Heinze HJ, Schoenfeld MA, Hopf JM (2009) Sensory MEG responses predict successful and failed inhibition in a stop-signal task. Cereb Cortex 19(1):134–145. doi: 10.1093/cercor/bhn063 CrossRefPubMedGoogle Scholar
  5. 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 CrossRefPubMedGoogle Scholar
  6. Boulinguez P, Ballanger B, Granjon L, Benraiss A (2009) The paradoxical effect of warning on reaction time: demonstrating proactive response inhibition with event-related potentials. Clin Neurophysiol 120(4):730–737. doi: 10.1016/j.clinph.2009.02.167 CrossRefPubMedGoogle Scholar
  7. Brown WS, Marsh JT, LaRue A (1983) Exponential electrophysiological aging: P3 latency. Electroencephalogr Clin Neurophysiol 55(3):277–285. doi: 10.1016/0013-4694(83)90205-5 CrossRefPubMedGoogle Scholar
  8. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Castro-Meneses LJ, Johnson BW, Sowman PF (2015a) 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. doi: 10.3389/fnhum.2015.00529 PubMedPubMedCentralGoogle Scholar
  10. Castro-Meneses LJ, Johnson BW, Sowman PF (2015b) Vocal response inhibition is enhanced by anodal tDCS over the right prefrontal cortex. Exp Brain Res. doi: 10.1007/s00221-015-4452-0 PubMedGoogle Scholar
  11. Coxon JP, Goble DJ, Leunissen I, Van Impe A, Wenderoth N, Swinnen SP (2014) Functional brain activation associated with inhibitory control deficits in older adults. Cerebral Cortex. doi: 10.1093/cercor/bhu165 Google Scholar
  12. 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 CrossRefPubMedGoogle Scholar
  13. Dimoska A, Johnstone SJ (2008) Effects of varying stop-signal probability on ERPs in the stop-signal task: do they reflect variations in inhibitory processing or simply novelty effects? Biol Psychol 77(3):324–336. doi: 10.1016/j.biopsycho.2007.11.005 CrossRefPubMedGoogle Scholar
  14. Dimoska A, Johnstone SJ, Barry RJ, Clarke AR (2003) Inhibitory motor control in children with attention-deficit/hyperactivity disorder: event-related potentials in the stop-signal paradigm. Biol Psychiatry 54(12):1345–1354. doi: 10.1016/S0006-3223(03)00703-0 CrossRefPubMedGoogle Scholar
  15. Dustman RE, Emmerson RY, Ruhling RO, Shearer DE, Steinhaus LA, Johnson SC, Shigeoka JW (1990) Age and fitness effects on EEG, ERPs, visual sensitivity, and cognition. Neurobiol Aging 11(3):193–200. doi: 10.1016/0197-4580(90)90545-B CrossRefPubMedGoogle Scholar
  16. 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 CrossRefPubMedGoogle Scholar
  17. Falkenstein M, Hoormann J, Hohnsbein J (1999) ERP components in Go/Nogo tasks and their relation to inhibition. Acta Psychol 101(2–3):267–291. doi: 10.1016/S0001-6918(99)00008-6 CrossRefGoogle Scholar
  18. Falkenstein M, Hoormann J, Christ S, Hohnsbein J (2000) ERP components on reaction errors and their functional significance: a tutorial. Biol Psychol 51(2–3):87–107. doi: 10.1016/S0301-0511(99)00031-9 CrossRefPubMedGoogle Scholar
  19. Gläscher J, Gitelman D (2008) Contrast weights in flexible factorial design with multiple groups of subjects. http://www.jiscmail.ac.uk/cgi-bin/webadmin?A2=ind0803&L=SPM&P=R16629
  20. Greenhouse I, Wessel JR (2013) EEG signatures associated with stopping are sensitive to preparation. Psychophysiology 50(9):900–908. doi: 10.1111/psyp.12070 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hartsuiker RJ, Bastiaanse R, Postma A, Wijnen F (2005) Phonological encoding and monitoring in normal and pathological speech. Psychology Press, LondonGoogle Scholar
  22. Hege MA, Preissl H, Stingl KT (2014) Magnetoencephalographic signatures of right prefrontal cortex involvement in response inhibition. Hum Brain Mapp 35(10):5236–5248. doi: 10.1002/hbm.22546 CrossRefPubMedGoogle Scholar
  23. Hughes LE, Rittman T, Regenthal R, Robbins TW, Rowe JB (2015) Improving response inhibition systems in frontotemporal dementia with citalopram. Brain. doi: 10.1093/brain/awv133 PubMedCentralGoogle Scholar
  24. Huster RJ, Enriquez-Geppert S, Lavallee CF, Falkenstein M, Herrmann CS (2013) Electroencephalography of response inhibition tasks: functional networks and cognitive contributions. Int J Psychophysiol 87(3):217–233. doi: 10.1016/j.ijpsycho.2012.08.001 CrossRefPubMedGoogle Scholar
  25. Kado H, Higuchi M, Shimogawara M, Haruta Y, Adachi Y, Kawai J, Uehara G (1999) Magnetoencephalogram systems developed at KIT. IEEE Trans Appl Supercond 9(2):4057–4062CrossRefGoogle Scholar
  26. Knösche TR (2002) Transformation of whole-head MEG recordings between different sensor positions. Biomed Eng 47(3):59–62CrossRefGoogle Scholar
  27. Kok A, Ramautar JR, De Ruiter MB, Band GPH, Ridderinkhof KR (2004) ERP components associated with successful and unsuccessful stopping in a stop-signal task. Psychophysiology 41(1):9–20. doi: 10.1046/j.1469-8986.2003.00127.x CrossRefPubMedGoogle Scholar
  28. Kramer AF, Humphrey DG, Larish JF, Logan GD (1994) Aging and inhibition: beyond a unitary view of inhibitory processing in attention. Psychol Aging 9(4):491–512. doi: 10.1037/0882-7974.9.4.491 CrossRefPubMedGoogle Scholar
  29. Lansbergen MM, Böcker KBE, Bekker EM, Kenemans JL (2007) Neural correlates of stopping and self-reported impulsivity. Clin Neurophysiol 118(9):2089–2103. doi: 10.1016/j.clinph.2007.06.011 CrossRefPubMedGoogle Scholar
  30. Lavallee CF, Herrmann CS, Weerda R, Huster RJ (2014) Stimulus-response mappings shape inhibition processes: a combined EEG-fMRI study of contextual stopping. PLoS One 9(4):e96159. doi: 10.1371/journal.pone.0096159 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Liotti M, Pliszka SR, Higgins K, Perez Iii R, Semrud-Clikeman M (2010) Evidence for specificity of ERP abnormalities during response inhibition in ADHD children: a comparison with reading disorder children without ADHD. Brain Cogn 72(2):228–237. doi: 10.1016/j.bandc.2009.09.007 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 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 189–239Google Scholar
  33. 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 CrossRefGoogle Scholar
  34. Luck SJ (2005) An introduction to the event-related potential technique, 1st edn. MIT Press, MassachussetsGoogle Scholar
  35. Mazaheri A, Nieuwenhuis IL, van Dijk H, Jensen O (2009) Prestimulus alpha and mu activity predicts failure to inhibit motor responses. Hum Brain Mapp 30(6):1791–1800. doi: 10.1002/hbm.20763 CrossRefPubMedGoogle Scholar
  36. McLaren, D. (2014). Re: flexible factorial desgins (SPM mailing list archive). http://www.jiscmail.ac.uk/cgi-bin/webadmin?A2=ind1401&L=spm&P=R36001&1=spm&9=A&J=on&d=No+Match%3BMatch%3BMatches&z=4
  37. Mullis RJ, Holcomb PJ, Diner BC, Dykman RA (1985) The effects of aging on the P3 component of the visual event-related potential. Electroencephalogr Clin Neurophysiol 62(2):141–149. doi: 10.1016/0168-5597(85)90026-7 CrossRefPubMedGoogle Scholar
  38. Nakata H, Inui K, Wasaka T, Akatsuka K, Kakigi R (2005) Somato-motor inhibitory processing in humans: a study with MEG and ERP. Eur J Neurosci 22(7):1784–1792. doi: 10.1111/j.1460-9568.2005.04368.x CrossRefPubMedGoogle Scholar
  39. Nakata H, Sakamoto K, Otsuka A, Yumoto M, Kakigi R (2013) Cortical rhythm of No-go processing in humans: an MEG study. Clin Neurophysiol 124(2):273–282. doi: 10.1016/j.clinph.2012.06.019 CrossRefPubMedGoogle Scholar
  40. Nieuwenhuis S, Yeung N, van den Wildenberg W, Ridderinkhof KR (2003) Electrophysiological correlates of anterior cingulate function in a go/no-go task: effects of response conflict and trial type frequency. Cogn Affect Behav Neurosci 3(1):17–26. doi: 10.3758/CABN.3.1.17 CrossRefPubMedGoogle Scholar
  41. Pfefferbaum A, Ford JM, Wenegrat BG, Roth WT, Kopell BS (1984) Clinical application of the P3 component of event-related potentials. I. Normal aging. Electroencephalogr Clin Neurophysiol 59(2):85–103. doi: 10.1016/0168-5597(84)90026-1 CrossRefPubMedGoogle Scholar
  42. Podlesny JA, Dustman RE, Shearer DE (1984) Aging and respond-withhold tasks: effects on sustained potentials, P3 responses and late activity. Electroencephalogr Clin Neurophysiol 58(2):130–139. doi: 10.1016/0013-4694(84)90026-9 CrossRefPubMedGoogle Scholar
  43. Ramautar JR, Kok A, Ridderinkhof KR (2004) Effects of stop-signal probability in the stop-signal paradigm: the N2/P3 complex further validated. Brain Cogn 56(2):234–252. doi: 10.1016/j.bandc.2004.07.002 CrossRefPubMedGoogle Scholar
  44. Salmelin R, Schnitzler A, Schmitz F, Freund HJ (2000) Single word reading in developmental stutterers and fluent speakers. Brain 123(Pt 6):1184–1202CrossRefPubMedGoogle Scholar
  45. Schmajuk M, Liotti M, Busse L, Woldorff MG (2006) Electrophysiological activity underlying inhibitory control processes in normal adults. Neuropsychologia 44(3):384–395. doi: 10.1016/j.neuropsychologia.2005.06.005 CrossRefPubMedGoogle Scholar
  46. Sörös P, Cornelissen K, Laine M, Salmelin R (2003) Naming actions and objects: cortical dynamics in healthy adults and in an anomic patient with a dissociation in action/object naming. NeuroImage 19(4):1787–1801. doi: 10.1016/S1053-8119(03)00217-9 CrossRefPubMedGoogle Scholar
  47. Squires NK, Squires KC, Hillyard SA (1975) Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man. Electroencephalogr Clin Neurophysiol 38(4):387–401. doi: 10.1016/0013-4694(75)90263-1 CrossRefPubMedGoogle Scholar
  48. Teplan M (2002) Fundamentals of EEG measurement. Measurement science review 2(2):1–11Google Scholar
  49. Uehara G, Adachi Y, Kawai J, Shimogawara M, Higuchi M, Haruta Y, Hisashi K (2003) Multi-channel SQUID systems for biomagnetic measurement. IEICE Trans Electron 86(1):43–54Google Scholar
  50. Uusitalo MA, Ilmoniemi RJ (1997) Signal-space projection method for separating MEG or EEG into components. Med Biol Eng Comput 35(2):135–140CrossRefPubMedGoogle Scholar
  51. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Vidal J, Mills T, Pang EW, Taylor MJ (2012) Response inhibition in adults and teenagers: spatiotemporal differences in the prefrontal cortex. Brain Cogn 79(1):49–59. doi: 10.1016/j.bandc.2011.12.011 CrossRefPubMedGoogle Scholar
  54. Vihla M, Laine M, Salmelin R (2006) Cortical dynamics of visual/semantic vs. phonological analysis in picture confrontation. NeuroImage 33(2):732–738. doi: 10.1016/j.neuroimage.2006.06.040 CrossRefPubMedGoogle Scholar
  55. Wessel JR, Aron AR (2013) Unexpected events induce motor slowing via a brain mechanism for action-stopping with global suppressive effects. J Neurosci 33(47):18481–18491CrossRefPubMedPubMedCentralGoogle Scholar
  56. 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. Psychophysiology 52(4):472–480. doi: 10.1111/psyp.12374 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Williams BR, Ponesse JS, Schachar RJ, Logan GD, Tannock R (1999) Development of inhibitory control across the life span. Dev Psychol 35(1):205–213. doi: 10.1037/0012-1649.35.1.205 CrossRefPubMedGoogle Scholar
  58. 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 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Leidy J. Castro-Meneses
    • 1
    • 2
  • Blake W. Johnson
    • 1
  • Paul F. Sowman
    • 1
    • 2
  1. 1.Department of Cognitive Science, Australian Research Council Centre of Excellence in Cognition and its Disorders (CCD)Macquarie UniversitySydneyAustralia
  2. 2.Department of Cognitive Science, Perception in Action Research Centre (PARC)Macquarie UniversitySydneyAustralia

Personalised recommendations