Abstract
The purpose of the current study was to evaluate whether error monitoring difficulties persist in adults with attention deficit hyperactivity disorder (ADHD) using the event-related potential (ERP) methodology. Adults with ADHD and age-matched healthy controls executed a visual Go/No-Go task with 25% No-Go trials. Performance and ERP correlates of error monitoring were compared between groups. At the performance level no difference was noted between groups. However, exploring the error-related potentials revealed that the error-related negativity (ERN) was the same for both groups, but that adults with ADHD showed a smaller error positivity (Pe). Based on these findings, we conclude that adults with ADHD are normal in early automatic error detection, but are deviant in later conscious evaluation of the error. The findings add to the increasing evidence supporting disturbances in error monitoring in ADHD and show that these problems may persist in adulthood ADHD.
Similar content being viewed by others
References
Achenbach TM, Rescorla LA (2003) Manual for the ASEBA adult forms and profiles. University of Vermont, research center for children, youth, and families, Burlington
Albrecht B, Brandeis D, Uebel H, Heinrich H, Mueller UC, Hasselhorn M, Steinhausen HC, Rothenberger A, Banaschewski T (2008) Action monitoring in boys with attention-deficit/hyperactivity disorder, their nonaffected siblings, and normal control subjects: evidence for an endophenotype. Biol Psychiatry 64:615–625
American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders. 4th edn (text revision). Washington, DC
Ardila A, Pineda D, Rosselli M (2000) Correlation between intelligence test scores and executive function measures. Arch Clin Neuropsychol 15:31–36
Barkley RA (1997) Behavioral inhibition, sustained attention and executive functions: constructing a unifying theory of ADHD. Psychol Bull 121:65–94
Boonstra AM, Oosterlaan J, Sergeant JA, Buitelaar JK (2005) Executive functioning in adult ADHD: a meta-analytic review. Psychol Med 35:1097–1108
Burgio-Murphy A, Klorman R, Shaywitz SE, Fletcher JM, Marchione KE, Holahan J, Stuebing KK, Thatcher JE, Shaywitz BA (2007) Error-related event-related potentials in children with attention-deficit hyperactivity disorder, oppositional defiant disorder, reading disorder, and math disorder. Biol Psychol 75:75–86
Bush G, Frazier JA, Rauch SL, Seidman LJ, Whalen PJ, Jenike MA, Rosen BR, Biederman J (1999) Anterior cingulate cortex dysfunction in attention-deficit/hyperactivity disorder revealed by fMRI and the counting stroop. Biol Psychiatry 45:1542–1552
Bush G, Vogt BA, Holmes J, Dale AM, Greve D, Jenike MA, Rosen BR (2002) Dorsal anterior cingulate cortex: a role in reward-based decision making. Proc Natl Acad Sci USA 99:523–528
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 280:747–749
Castellanos FX, Margulies DS, Kelly C, Uddin LQ, Ghaffari M, Kirsch A, Shaw D, Shehzad Z, Di Martino A, Biswal B, Sonuga-Barke EJS, Rotrosen J, Adler LA, Milham MP (2008) Cingulate–precuneus interactions: a new locus of dysfunction in adult attention-deficit/hyperactivity disorder. Biol Psychiatry 63:332–337
Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum, New York
Coles MGH, Scheffers MK, Holroyd CB (2001) Why is there an ERN/Ne on correct trials? Response representations, stimulus components, and the theory of error processing. Biol Psychol 56:173–189
Critchley HD, Mathias CJ, Josephs O, O’Doherty J, Zanini S, Dewar BK, Cipolotti L, Shallice T, Dolan RJ (2003) Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. Brain 126:2139–2152
Falkenstein M (2004) ERP correlates of erroneous performance. In: Ullsperger M, Falkenstein M (eds) Errors, conflicts, and the brain. Current opinions on performance monitoring (MPI special issue in human cognitive and brain sciences 1). Max-Planck-Institut für Kognitions- und Neurowissenschaften, Leipzig, pp 5–14
Falkenstein M, Hohnsbein J, Hoormann J, Blanke L (1990) Effects of errors in choice reaction tasks on the ERP under focused and divided attention. In: Brunia CHM, Gaillard AWK, Kok A (eds) Psychophysiological brain research. University Press, Tilburg, pp 192–195
Falkenstein M, Hohnsbein J, Hoormann J (1995) Event-related potential correlates of errors in reaction tasks. In: Karmos G, Molnar M, Scepe V, Czigler I, Desmedt JE (eds) Perspectives of event-related potentials research. Elsevier, Amsterdam, pp 287–296
Falkenstein M, Hoormann J, Christ S, Hohnsbein J (2000) ERP components on reaction errors and their functional significance: a tutorial. Biol Psychol 51:87–107
Fassbender C, Schweitzer JB (2006) Is there evidence for neural compensation in attention deficit hyperactivity disorder? A review of the functional neuroimaging literature. Clin Psychol Rev 26:445–465
Gehring WJ, Fencsik DE (2001) Functions of the medial frontal cortex in the processing of conflict and errors. J Neurosci 21:9430–9437
Gehring WJ, Coles MGH, Meyer DE, Donchin E (1990) The error-related negativity: an event-related brain potential accompanying errors (abstract). Psychophysiology 27:S34
Gehring WJ, Goss B, Coles MGH, Meyer DE, Donchin E (1993) A neural system for error detection and compensation. Psychol Sci 4:385–390
Gratton G, Coles MGH, Donchin E (1983) A new method for off-line removal of ocular artifact. Electroencephalogr Clin Neurophysiol 55:468–484
Groen Y, Wijers AA, Mulder LJM, Waggeveld B, Minderaa RB, Althaus M (2008) Error and feedback processing in children with ADHD and children with autistic spectrum disorder: an EEG event-related potential study. Clin Neurophys 119:2476–2493
Henderson H, Schwartz C, Mundy P, Burnette C, Sutton S, Zahka N, Pradella A (2006) Response monitoring, the error-related negativity, and differences in social behavior in autism. Brain Cogn 61:96–109
Hermann MJ, Rommler J, Ehlis AC, Heidrich A, Fallgatter AJ (2004) Source localization (LORETA) of the error-related-negativity (ERN/Ne) and positivity (Pe). Cogn Brain Res 20:294–299
Hogan AM, Vargha-Khadem F, Kirkham FJ, Baldeweg T (2005) Maturation of action monitoring from adolescence to adulthood: an ERP study. Dev Sci 8:525–534
Holroyd CB, Nieuwenhuis S, Yeung N, Nystrom LE, Mars RB, Coles MGH, Cohen JD (2004) Dorsal anterior cingulate cortex shows fMRI response to internal and external error signals. Nature Neurosci 7:497–498
Jonkman LM, van Melis JM, Kemner C, Markus CR (2007) Methylphenidate improves deficient error evaluation in children with ADHD: an event-related brain potential study. Biol Psychol 76:1–29
Krusch DA, Klorman R, Brumaghim JT, Fitzpatrick PA, Borgstedt AD, Strauss J (1996) Methylphenidate slows reactions of children with attention deficit disorder during and after an error. J Abnorm Child Psychol 24:633–650
Liotti M, Pliszka SR, Perez R, Kothmann D, Woldorff MG (2005) Abnormal brain activity related to performance monitoring and error detection in children with ADHD. Cortex 41:377–388
Makris N, Biederman J, Valera EM, Bush G, Kaiser J, Kennedy DN, Caviness VS, Faraone SV, Seidman LJ (2007) Cortical thinning of the attention and executive function networks in adults with attention-deficit/hyperactivity disorder. Cerebr Cortex 17:1364–1375
Nieuwenhuis S, Ridderinkhof K, Blom J, Band GPH, Kok A (2001) Error-related brain potentials are differentially related to awareness of response errors: evidence from an antisaccade task. Psychophysiology 38:752–760
O’Connell RG, Dockree PM, Bellgrove MA, Kelly SP, Hester R, Garavan H, Robertson IH, Foxe JJ (2007) The role of cingulate cortex in the detection of errors with and without awareness: a high-density electrical mapping study. Eur J NeuroSci 25:2571–2579
Overbeek TJM, Nieuewenhuis S, Ridderinkhof R (2005) Dissociable components of error processing—on the functional significance of the Pe Vis-à-vis the ERN/Ne. J Psychophysiol 19:319–329
Overtoom CCE, Kenemans JL, Verbaten MN, Kemner C, van der Molen MW, van Engeland H, Buitelaar JK, Koelega HS (2002) Inhibition in children with attention-deficit/hyperactivity disorder: a psychophysiological study of the stop task. Biol Psychiatry 51:668–676
Polanczyk G, de Lima MS, Horta BL, Biederman J, Rohde LA (2007) The worldwide prevalence of ADHD: a systematic review and metaregression analysis. Am J Psychiatry 164:942–948
Quay HC (1997) Inhibition and attention deficit hyperactivity disorder. J Abnorm Child Psychol 25:7–13
Rabbitt PMA (1966) Errors and error correction in choice reaction tasks. J Exp Psychol 71:264–272
Rubia K, Overmeyer S, Taylor E, Brammer M, Williams SCR, Simmons A, Bullmore ET (1999) Hypofrontality in attention deficit hyperactivity disorder during higher-order motor control: a study with functional MRI. Am J Psychiatry 156:891–896
Ryan JJ, Ward LC (1999) Validity, reliability, and standard errors of measurement for two-seven-subtest short forms of the Wechsler adult intelligence scale-III. Psychol Assess 11:207–211
Schachar RJ, Chen S, Logan GD, Crosbie J, Ickowicz A, Pakulak A (2004) Evidence for an error monitoring deficit in attention deficit hyperactivity disorder. J Abnorm Child Psychol 32:285–293
Schulz KP, Fan J, Tang CY, Newcorn JH, Buchsbaum MS, Cheung AM, Halperin JM (2004) Response inhibition in adolescents diagnosed with attention deficit hyperactivity disorder during childhood: an event-related fMRI study. Am J Psychiatry 161:1650–1657
Sergeant JA, van der Meere JJ (1988) What happens after a hyperactive commits an error? Psychiatr Res 24:157–164
Sergeant JA, Geurts H, Huijbregts S, Scheres A, Oosterlaan J (2003) The top and the bottom of ADHD: a neuropsychological perspective. Neurosci Biobehav Rev 27:583–592
Sonuga-Barke EJS (2002) The dual pathway model of AD/HD: an elaboration of neurodevelopmental characteristics. Neurosci Biobehav Rev 27:593–604
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 14:1387–1401
Van Meel CS, Heslenfeld DJ, Oosterlaan J, Sergeant JA (2007) Adaptive control deficits in attention-deficit/hyperactivity disorder (ADHD): the role of error processing. Psychiatry Res 151:211–220
Vidal F, Hasbroucq T, Grapperon J, Bonnet M (2000) Is the ‘error negativity’ specific of errors? Biol Psychol 51:109–128
Ward MF, Wender PH, Reimherr FW (1993) The Wender Utah rating scale: an aid in the retrospective diagnosis of childhood attention deficit hyperactivity disorder. Am J Psychiatry 50:885–890
Wender PH, Wolf LE, Wasserstein J (2001) Adults with ADHD: an overview. Ann NY Acad Sci 931:1–16
Wiersema JR, van der Meere JJ, Roeyers H (2005) ERP correlates of impaired error monitoring in children with ADHD. J Neur Transm 112:1417–1430
Wiersema JR, van der Meere JJ, Antrop I, Roeyers H (2006a) State regulation in adult ADHD: an event-related potential study. J Clin Exp Neuropsychol 28:1113–1126
Wiersema JR, van der Meere JJ, Roeyers H, Van Coster R, Baeyens D (2006b) Event rate and event-related potentials in ADHD. J Child Psychol Psychiatry 47:560–567
Wiersema JR, van der Meere JJ, Roeyers H (2007) Developmental changes in error monitoring: an event-related potential study. Neuropsychologia 45:1649–1657
Acknowledgments
This study was supported by grants from the Ghent University Research Fund and was carried out at the Ghent University, Department of Experimental-Clinical and Health Psychology. We would like to thank all adults, who participated in this study.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wiersema, J.R., van der Meere, J.J. & Roeyers, H. ERP correlates of error monitoring in adult ADHD. J Neural Transm 116, 371–379 (2009). https://doi.org/10.1007/s00702-008-0165-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00702-008-0165-x