Abstract
Advanced ERP topographic mapping techniques were used to study error monitoring functions in human adult participants, and test whether proactive attentional effects during the pre-response time period could later influence early error detection mechanisms (as measured by the ERN component) or not. Participants performed a speeded go/nogo task, and made a substantial number of false alarms that did not differ from correct hits as a function of behavioral speed or actual motor response. While errors clearly elicited an ERN component generated within the dACC following the onset of these incorrect responses, I also found that correct hits were associated with a different sequence of topographic events during the pre-response baseline time-period, relative to errors. A main topographic transition from occipital to posterior parietal regions (including primarily the precuneus) was evidenced for correct hits ~170–150 ms before the response, whereas this topographic change was markedly reduced for errors. The same topographic transition was found for correct hits that were eventually performed slower than either errors or fast (correct) hits, confirming the involvement of this distinctive posterior parietal activity in top-down attentional control rather than motor preparation. Control analyses further ensured that this pre-response topographic effect was not related to differences in stimulus processing. Furthermore, I found a reliable association between the magnitude of the ERN following errors and the duration of this differential precuneus activity during the pre-response baseline, suggesting a functional link between an anticipatory attentional control component subserved by the precuneus and early error detection mechanisms within the dACC. These results suggest reciprocal links between proactive attention control and decision making processes during error monitoring.
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References
Allain S, Carbonnell L, Falkenstein M, Burle B, Vidal F (2004) The modulation of the Ne-like wave on correct responses foreshadows errors. Neurosci Lett 372(1–2):161–166
Astafiev SV, Shulman GL, Stanley CM, Snyder AZ, Van Essen DC, Corbetta M (2003) Functional organization of human intraparietal and frontal cortex for attending, looking, and pointing. J Neurosci 23(11):4689–4699
Barber AD, Carter CS (2005) Cognitive control involved in overcoming prepotent response tendencies and switching between tasks. Cereb Cortex 15(7):899–912
Botvinick MM, Braver TS, Barch DM, Carter CS, Cohen JD (2001) Conflict monitoring and cognitive control. Psychol Rev 108(3):624–652
Braver TS, Gray JR, Burgess GC (2007) Explaining the many varieties of working memory variation: Dual mechanisms of cognitive control. In: Conway ARA, Jarrold C, Kane MJ, Miyake A, Towse JN (eds) Variation in working memory. Oxford University Press, Oxford, pp 76–106
Braver TS, Paxton JL, Locke HS, Barch DM (2009) Flexible neural mechanisms of cognitive control within human prefrontal cortex. Proc Natl Acad Sci U S A 106(18):7351–7356
Bunge SA, Hazeltine E, Scanlon MD, Rosen AC, Gabrieli JD (2002) Dissociable contributions of prefrontal and parietal cortices to response selection. Neuroimage 17(3):1562–1571
Bush G, Luu P, Posner MI (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 4(6):215–222
Carter CS, Braver TS, Barch DM, Botvinick MM, Noll D, Cohen JD (1998) Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280(5364):747–749
Carter CS, Botvinick MM, Cohen JD (1999) The contribution of the anterior cingulate cortex to executive processes in cognition. Rev Neurosci 10(1):49–57
Cohen JD, Perlstein WM, Braver TS, Nystrom LE, Noll DC, Jonides J et al (1997) Temporal dynamics of brain activation during a working memory task. Nature 386(6625):604–608
Coles MG, Gratton G, Donchin E (1988) Detecting early communication: using measures of movement-related potentials to illuminate human information processing. Biol Psychol 26(1–3):69–89
Coles MG, Scheffers MK, Holroyd CB (2001) Why is there an ERN/Ne on correct trials? Response representations, stimulus-related components, and the theory of error-processing. Biol Psychol 56(3):173–189
Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215
Debener S, Ullsperger M, Siegel M, Fiehler K, von Cramon DY, Engel AK (2005) Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring. J Neurosci 25(50):11730–11737
Dehaene S, Posner MI, Tucker DM (1994) Localization of a neural system for error detection and compensation. Psychol Sci 5(5):303–305
Dempster FN, Corkill AJ (1999) Interference and inhibition in cognition and behavior: unifying themes for educational psychology. Educ Psychol Rev 11(1):1–88
Desimone R, Duncan J (1995) Neural mechanisms of selective visual attention. Annu Rev Neurosci 18:193–222
Dreher JC, Berman KF (2002) Fractionating the neural substrate of cognitive control processes. Proc Natl Acad Sci U S A 99(22):14595–14600
Eichele T, Debener S, Calhoun VD, Specht K, Engel AK, Hugdahl K et al (2008) Prediction of human errors by maladaptive changes in event-related brain networks. Proc Natl Acad Sci U S A 105(16):6173–6178
Falkenstein M, Hohnsbein J, Hoormann J, Blanke L (1991) Effects of crossmodal divided attention on late ERP components. II. Error processing in choice reaction tasks. Electroencephalogr Clin Neurophysiol 78(6):447–455
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
Friedman NP, Miyake A (2004) The relations among inhibition and interference control functions: a latent-variable analysis. J Exp Psychol Gen 133(1):101–135
Fuchs M, Kastner J, Wagner M, Hawes S, Ebersole JS (2002) A standardized boundary element method volume conductor model. Clin Neurophysiol 113:702–712
Gevins AS, Morgan NH, Bressler SL, Cutillo BA, White RM, Illes J et al (1987) Human neuroelectric patterns predict performance accuracy. Science 235(4788):580–585
Gratton G, Coles MGH, Donchin E (1983) A new method for off-line removal of ocular artifact. Electroencephalogr Clin Neurophysiol 55(4):468–484
Gratton G, Coles MG, Sirevaag EJ, Eriksen CW, Donchin E (1988) Pre- and poststimulus activation of response channels: a psychophysiological analysis. J Exp Psychol Hum Percept Perform 14(3):331–344
Hajcak G, Nieuwenhuis S, Ridderinkhof KR, Simons RF (2005) Error-preceding brain activity: robustness, temporal dynamics, and boundary conditions. Biol Psychol 70(2):67–78
Herrmann MJ, Rommler J, Ehlis AC, Heidrich A, Fallgatter AJ (2004) Source localization (LORETA) of the error-related-negativity (ERN/Ne) and positivity (Pe). Brain Res Cogn Brain Res 20(2):294–299
Holroyd CB, Coles MG (2002) The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. Psychol Rev 109(4):679–709
Jurcak V, Tsuzuki D, Dan I (2007) 0/20, 10/10, and 10/5 systems revisited: their validity as relative head-surface-based positioning systems. Neuroimage 34:1600–1611
Kastner S, Ungerleider LG (2000) Mechanisms of visual attention in the human cortex. Annu Rev Neurosci 23:315–341
Kastner S, Pinsk MA, De Weerd P, Desimone R, Ungerleider LG (1999) Increased activity in human visual cortex during directed attention in the absence of visual stimulation. Neuron 22(4):751–761
Koenig T, Melie-Garcia L (2010) A Method to Determine the Presence of Averaged Event-Related Fields Using Randomization Tests. Brain topography 23(3):233–242
Kok A (1986) Effects of degradation of visual stimulation on components of the event-related potential (ERP) in go/nogo reaction tasks. Biol Psychol 23(1):21–38
Kondakor I, Pascual-Marqui RD, Michel CM, Lehmann D (1995) Event-related potential map differences depend on the prestimulus microstates. J Med Eng Technol 19(2–3):66–69
Lavie N (2005) Distracted and confused?: selective attention under load. Trends Cogn Sci 9(2):75–82
Lehmann D (1987) Principles of spatial analysis. In: Gevins AS, Remond D (eds) Handbook of electroencephalography and clinical neurophysiology. Methods of analysis of brain electrical and magnetic signals. Elsevier, Amsterdam, pp 309–354
Lehmann D, Skrandies W (1980) Reference-free identification of components of checkerboard-evoked multichannel potential fields. Electroencephalogr Clin Neurophysiol 48(6):609–621
Levy R, Goldman-Rakic PS (1999) Association of storage and processing functions in the dorsolateral prefrontal cortex of the nonhuman primate. J Neurosci 19(12):5149–5158
Li CS, Yan P, Bergquist KL, Sinha R (2007) Greater activation of the “default” brain regions predicts stop signal errors. Neuroimage 38(3):640–648
Li CS, Yan P, Chao HH, Sinha R, Paliwal P, Constable RT et al (2008) Error-specific medial cortical and subcortical activity during the stop signal task: a functional magnetic resonance imaging study. Neuroscience 155(4):1142–1151
Luu P, Tucker DM, Makeig S (2004) Frontal midline theta and the error-related negativity: neurophysiological mechanisms of action regulation. Clin Neurophysiol 115(8):1821–1835
MacDonald AW, Cohen JD, Stenger VA, Carter CS (2000) Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 288(5472):1835–1838
Manly BF (1991) Randomization and Monte Carlo methods in biology. Chapman & Hall, London
Margulies DS, Kelly AM, Uddin LQ, Biswal BB, Castellanos FX, Milham MP (2007) Mapping the functional connectivity of anterior cingulate cortex. Neuroimage 37(2):579–588
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
Mazziotta J, Toga A, Fox P, Lancaster J, Zilles K, Woods R et al (2001) A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos Trans R Soc Lond B Biol Sci 356:1293–1322
Michel CM, Seeck M, Landis T (1999) Spatiotemporal dynamics of human cognition. News Physiol Sci 14:206–214
Michel CM, Thut G, Morand S, Khateb A, Pegna AJ, Grave de Peralta R et al (2001) Electric source imaging of human brain functions. Brain Res Brain Res Rev 36(2–3):108–118
Murray MM, Brunet D, Michel CM (2008) Topographic ERP analyses: a step-by-step tutorial review. Brain Topogr 20(4):249–264
Nieuwenhuis S, Ridderinkhof KR, Blom J, Band GP, Kok A (2001) Error-related brain potentials are differentially related to awareness of response errors: evidence from an antisaccade task. Psychophysiology 38(5):752–760
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
Nieuwenhuis S, Holroyd CB, Mol N, Coles MG (2004) Reinforcement-related brain potentials from medial frontal cortex: origins and functional significance. Neurosci Biobehav Rev 28(4):441–448
O’Connell RG, Dockree PM, Bellgrove MA, Kelly SP, Hester R, Garavan H et al (2007) The role of cingulate cortex in the detection of errors with and without awareness: a high-density electrical mapping study. Eur J Neurosci 25(8):2571–2579
Orr JM, Weissman DH (2009) Anterior cingulate cortex makes 2 contributions to minimizing distraction. Cereb Cortex 19(3):703–711
Padilla ML, Wood RA, Hale LA, Knight RT (2006) Lapses in a prefrontal-extrastriate preparatory attention network predict mistakes. J Cogn Neurosci 18(9):1477–1487
Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24D:5–12
Pascual-Marqui RD, Michel CM, Lehmann D (1995) Segmentation of brain electrical activity into microstates: model estimation and validation. IEEE Trans Biomed Eng 42:658–665
Picton TW, Bentin S, Berg P, Donchin E, Hillyard SA, Johnson R et al (2000) Guidelines for using human event-related potentials to study cognition: recording standards and publication criteria. Psychophysiology 37(2):127–152
Pizzagalli DA, Peccoralo LA, Davidson RJ, Cohen JD (2006) Resting anterior cingulate activity and abnormal responses to errors in subjects with elevated depressive symptoms: a 128-channel EEG study. Hum Brain Mapp 27(3):185–201
Pourtois G, Dan ES, Grandjean D, Sander D, Vuilleumier P (2005a) Enhanced extrastriate visual response to bandpass spatial frequency filtered fearful faces: time course and topographic evoked-potentials mapping. Hum Brain Mapp 26(1):65–79
Pourtois G, Thut G, Grave de Peralta R, Michel C, Vuilleumier P (2005b) Two electrophysiological stages of spatial orienting towards fearful faces: early temporo-parietal activation preceding gain control in extrastriate visual cortex. Neuroimage 26(1):149–163
Pourtois G, De Pretto M, Hauert CA, Vuilleumier P (2006) Time course of brain activity during change blindness and change awareness: performance is predicted by neural events before change onset. J Cogn Neurosci 18(12):2108–2129
Pourtois G, Peelen MV, Spinelli L, Seeck M, Vuilleumier P (2007) Direct intracranial recording of body-selective responses in human extrastriate visual cortex. Neuropsychologia 45(11):2621–2625
Pourtois G, Delplanque S, Michel C, Vuilleumier P (2008) Beyond conventional event-related brain potential (ERP): exploring the time-course of visual emotion processing using topographic and principal component analyses. Brain Topogr 20(4):265–277
Pourtois G, Vocat R, N’Diaye K, Spinelli L, Seeck M, Vuilleumier P (2010) Errors recruit both cognitive and emotional monitoring systems: simultaneous intracranial recordings in the dorsal anterior cingulate gyrus and amygdala combined with fMRI. Neuropsychologia 48(4):1144–1159
Ridderinkhof KR, Nieuwenhuis S, Bashore TR (2003) Errors are foreshadowed in brain potentials associated with action monitoring in cingulate cortex in humans. Neurosci Lett 348(1):1–4
Ridderinkhof KR, Ullsperger M, Crone EA, Nieuwenhuis S (2004) The role of the medial frontal cortex in cognitive control. Science 306(5695):443–447
Ridderinkhof KR, Nieuwenhuis S, Braver TS (2007) Medial frontal cortex function: an introduction and overview. Cogn Affect Behav Neurosci 7(4):261–265
Robbins TW (2007) Shifting and stopping: fronto-striatal substrates, neurochemical modulation and clinical implications. Philos Trans R Soc Lond B Biol Sci 362(1481):917–932
Rowe JB, Toni I, Josephs O, Frackowiak RS, Passingham RE (2000) The prefrontal cortex: response selection or maintenance within working memory? Science 288(5471):1656–1660
Rushworth MF, Taylor PC (2006) TMS in the parietal cortex: updating representations for attention and action. Neuropsychologia 44(13):2700–2716
Rushworth MF, Paus T, Sipila PK (2001) Attention systems and the organization of the human parietal cortex. J Neurosci 21(14):5262–5271
Scheffers MK, Coles MG, Bernstein P, Gehring WJ, Donchin E (1996) Event-related brain potentials and error-related processing: an analysis of incorrect responses to go and no-go stimuli. Psychophysiology 33(1):42–53
Sekihara K, Sahani M, Nagarajan SS (2005) Localization bias and spatial resolution of adaptive and non-adaptive spatial filters for MEG source reconstruction. Neuroimage 25(4):1056–1067
Silva L, Amitai Y, Connors B (1991) Intrinsic oscillations of neocortex generated by layer 5 pyrimidal neurons. Science 251:432–435
Super H, van der Togt C, Spekreijse H, Lamme VA (2003) Internal state of monkey primary visual cortex (V1) predicts figure-ground perception. J Neurosci 23(8):3407–3414
Tibshirani R, Walther G, Hastie T (2001) Estimating the number of clusters in a data set via the gap statistic. J R Stat Soc Series B Stat Methodol 63:411–423
Ullsperger M, von Cramon DY (2001) Subprocesses of performance monitoring: a dissociation of error processing and response competition revealed by event-related fMRI and ERPs. Neuroimage 14(6):1387–1401
van Veen V, Carter CS (2006) Error detection, correction, and prevention in the brain: a brief review of data and theories. Clin EEG Neurosci 37(4):330–335
van Veen V, Cohen JD, Botvinick MM, Stenger VA, Carter CS (2001) Anterior cingulate cortex, conflict monitoring, and levels of processing. Neuroimage 14(6):1302–1308
Vocat R, Pourtois G, Vuilleumier P (2008) Unavoidable errors: a spatio-temporal analysis of time-course and neural sources of evoked potentials associated with error processing in a speeded task. Neuropsychologia 46(10):2545–2555
Weissman DH, Roberts KC, Visscher KM, Woldorff MG (2006) The neural bases of momentary lapses in attention. Nat Neurosci 9(7):971–978
Woldorff MG, Hazlett CJ, Fichtenholtz HM, Weissman DH, Dale AM, Song AW (2004) Functional parcellation of attentional control regions of the brain. J Cogn Neurosci 16(1):149–165
Yeung N, Cohen JD, Botvinick MM (2004) The neural basis of error detection: conflict monitoring and the error-related negativity. Psychol Rev 111(4):931–959
Acknowledgments
This work is supported by grants from the European Research Council (Starting Grant #200758) and Ghent University (BOF Grant #05Z01708). Thanks to Dr. Roland Vocat for earlier discussions on error detection brain mechanisms, and to Dr. Monica Dhar for her comments on an earlier draft of this manuscript.
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Supplementary Fig. 1
a A control analysis was carried out to assess whether the occurrence of errors (i.e. false alarms) varied with the delay/SOA (between the black arrow/cue and the changing arrow/target) or not. This SOA varied randomly between 1,000 and 2,000 ms (with steps of 100 ms) on a trial by trial basis. This analysis clearly confirmed a lack of systematic relationship between the cue-target interval and the prevalence of errors. Errors were distributed evenly across the different (and randomized) SOAs used. b An additional control analysis was also performed to look at the RT distribution for errors, relative to fast hits, and eventually ascertain a reasonable overlap between these two RT distributions. The RT distribution for errors was found to tightly overlap with that obtained for fast hits, confirming that errors were comparable to fast hits. (TIFF 125 kb)
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Pourtois, G. Early Error Detection Predicted by Reduced Pre-response Control Process: An ERP Topographic Mapping Study. Brain Topogr 23, 403–422 (2011). https://doi.org/10.1007/s10548-010-0159-5
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DOI: https://doi.org/10.1007/s10548-010-0159-5