Abstract
When participants commit errors or receive feedback signaling that they have made an error, a negative brain potential is elicited. According to Holroyd and Coles’s (in press) neurocomputational model of error processing, this error-related negativity (ERN) is elicited when the brain first detects that the consequences of an action are worse than expected. To study age-related changes in error processing, we obtained performance and ERN measures of younger and high-functioning older adults. Experiment 1 demonstrated reduced ERN amplitudes in older adults in the context of otherwise intact brain potentials. This result could not be attributed to uncertainty about the required response in older adults. Experiment 2 revealed impaired performance and reduced response- and feedback-related ERNs of older adults in a probabilistic learning task. These age changes could be simulated by manipulation of a single parameter of the neurocomputational model, this manipulation corresponding to weakened phasic activity of the mesencephalic dopamine system.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Arnsten, A. F. T. (1993). Catecholamine mechanisms in age-related cognitive decline. Neurobiology of Aging, 14, 639–641.
Arnsten, A. F. T., & Goldman-Rakic, P. S. (1985). Alpha 2-adrenergic mechanisms in prefrontal cortex associated with cognitive decline in aged nonhuman primates. Science, 230, 1273–1276.
Backman, L., Ginovart, N., Dixon, R. A., Wahlin, T. B., Wahlin, A., Halldin, C., & Farde L. (2000). Age-related cognitive deficits mediated by changes in the striatal dopamine system. American Journal of Psychiatry, 157, 635–637.
Band, G. P. H., & Kok, A. (2000). Age effects on response monitoring in a mental-rotation task. Biological Psychology, 51, 201–221.
Bernstein, P. S., Scheffers, M. K., & Coles, M. G. H. (1995). “Where did I go wrong?” A psychophysiological analysis of error detection. Journal of Experimental Psychology: Human Perception & Performance, 21, 1312–1322.
Botvinick, M. M., Braver, T. S., Barch, D. M., Carter, C. S., & Cohen, J. D. (2001). Evaluating the demand for control: Anterior cingulate cortex and conflict monitoring. Psychological Review, 108, 624–652.
Braver, T. S., Barch, D. M., Keys, B. A., Carter, C. S., Cohen, J. D., Kaye, J. A., Janowsky, J. S., Taylor, S. F., Yesavage, J. A., Mumenthaler, M. S., Jagust, W. J., & Reed, B. R. (2001). Context processing in older adults: Evidence for a theory relating cognitive control to neurobiology in healthy aging. Journal of Experimental Psychology: General, 130, 746–763.
Braver, T. S., & Cohen, J. D. (2000). On the control of control: The role of dopamine in regulating prefrontal function and working memory. In S. Monsell & J. Driver (Eds.), Attention and performance XVIII: Control of cognitive processes (pp. 713–737). Cambridge, MA: MIT Press.
Carter, C. S., Braver, T. S., Barch, D. M., Botvinick, M. M., Noll, D., & Cohen, J. D. (1998). Anterior cingulate cortex, error detection, and the online monitoring of performance. Science, 280, 747–749.
Coles, M. G. H., Gratton, G., Bashore, T. R., Eriksen, C. W., & Donchin, E. (1985). A psychophysiological investigation of the continuous flow model of human information processing. Journal of Experimental Psychology: Human Perception & Performance, 11, 529–553.
Coles, M. G. H., Scheffers, M. K., & Holroyd, C. B. (1998). Berger’s dream: The error-related negativity and modern cognitive psychophysiology. In H. Witte, U. Zwiener, B. Schack, & A. Doering (Eds.), Quantitative and topological EEG and MEG analysis (pp. 96–102). Jena-Erlangen: Druckhaus Mayer.
Coles, M. G. H., Scheffers, M. K., & Holroyd, C. B. (2001). Why is there an ERN/Ne on correct trials? Response representations, stimulusrelated components, and the theory of error-processing. Biological Psychology, 56, 173–189.
Dehaene, S., Posner, M. I., & Tucker, D. M. (1994). Localization of a neural system for error detection and compensation. Psychological Science, 5, 303–305.
Eriksen, B. A., & Eriksen, C. W. (1974). Effects of noise letters upon the identification of a target letter in a nonsearch task. Perception & Psychophysics, 16, 143–149.
Falkenstein, M., Hielscher, H., Dziobek, I., Schwarzenau, P., Hoormann, J., Sunderman, B., & Hohnsbein, J. (2001). Action monitoring, error detection, and the basal ganglia: An ERP study. Neuro-Report, 12, 157–161.
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. Electroencephalography & Clinical Neurophysiology, 78, 447–455.
Falkenstein, M., Hoormann, J., Christ, S., & Hohnsbein, J. (2000). ERP components on reaction errors and their functional significance: A tutorial. Biological Psychology, 51, 87–107.
Falkenstein, M., Hoormann, & Hohnsbein, J. (2001). Changes of error-related ERPs with age. Experimental Brain Research, 138, 258–262.
Ford, J. M. (1999). Schizophrenia: The broken P300 and beyond. Psychophysiology, 36, 667–682.
Gehring, W. J., Goss, B., Coles, M. G. H., Meyer, D. E., & Donchin, E. (1993). A neural system for error detection and compensation. Psychological Science, 4, 385–390.
Gehring, W. J., Himle, J., & Nisenson, L. G. (2000). Action-monitoring dysfunction in obsessive-compulsive disorder. Psychological Science, 11, 1–6.
Gehring, W. J., & Knight, R. T. (2000). Prefrontal-cingulate interactions in action monitoring. Nature Neuroscience, 3, 516–520.
Goldman-Rakic, P. S., & Brown, R. M. (1981). Regional changes of monoamines in cerebral cortex and subcortical structures of aging rhesus monkeys. Neuroscience, 6, 177–187.
Gratton, G., Coles, M. G. H., Sirevaag, E. J., Eriksen, C. W., & Donchin, E. (1988). Pre- and poststimulus activation of response channels: A psychophysiological analysis. Journal of Experimental Psychology: Human Perception & Performance, 14, 331–344.
Holroyd, C. B., & Coles, M. G. H. (in press). The neural basis of human error processing: Reinforcement learning, dopamine, and the error-related negativity. Psychological Review.
Holroyd, C. B., Dien, J., & Coles, M. G. H. (1998). Error-related scalp potentials elicited by hand and foot movements: Evidence for an outputindependent error-processing system in humans. Neuroscience Letters, 242, 65–68.
Holroyd, C., Praamstra, P., Plat, E., & Coles, M. G. H. (in press). Spared error-related potentials in mild to moderate Parkinson’s disease. Neuropsychologia.
Holroyd, C., Reichler, J., & Coles, M. G. H. (1999, April 10–13). Is the error-related negativity generated by a dopaminergic error signal for reinforcement learning? Hypothesis and model [Abstract]. Cognitive Neuroscience Society 1999 annual meeting, Washington, DC.
Holroyd, C. B., Yeung, N., Coles, M. G. H., & Cohen, J. D. (2002). A computational model of learning and error detection in the Eriksen Flankers Task. Manuscript in preparation.
Kaasinen, V., Vilkman, H., Hietala, J., Nagren, K., Helenius, H., Olsson, H., Farde, L., & Rinne J. (2000). Age-related dopamine D2/D3 receptor loss in extrastriatal regions of the human brain. Neurobiology & Aging, 21, 683–688.
Kiehl, K. A., Liddle, P. F., & Hopfinger, J. B. (2000). Error processing and the rostral anterior cingulate: An event-related fMRI study. Psychophysiology, 37, 216–223.
Kok, A. (2000). Age-related changes in involuntary and voluntary attention as reflected in components of the event-related potentials (ERP). Biological Psychology, 54, 107–143.
Kopp, B., & Rist, F. (1999). An event-related brain potential substrate of disturbed response monitoring in paranoid schizophrenic patients. Journal of Abnormal Psychology, 108, 337–346.
Li, S. C., & Lindenberger, U. (1999). Cross-level unification: A computational exploration of the link between deterioration of neurotransmitter systems and dedifferentiation of cognitive abilities in old age. In L. G. Nilsson & H. J. Markowitsch (Eds.), Cognitive neuroscience of memory (pp. 103–146). Seattle: Hogrefe & Huber.
Miltner, W. H. R., Braun, C. H., & Coles, M. G. H. (1997). Eventrelated brain potentials following incorrect feedback in a time-estimation task: Evidence for a generic neural system for error detection. Journal of Cognitive Neuroscience, 9, 788–798.
Moscovitch, M., & Winocur, G. (1995). Frontal lobes, memory, and aging. In J. Grafman, K. J. Holyoak, & F. Boller (Eds.), Structure and functions of the human prefrontal cortex (Annals of the New York Academy of Sciences, Vol. 769, pp. 119–151). New York: New York Academy of Sciences.
Nieuwenhuis, S., Ridderinkhof, K. R., Blom, J., Band, G. P. H., & Kok, A. (2001). Error-related brain potentials are differentially related to awareness of response errors: Evidence from an antisaccade task. Psychophysiology, 38, 752–760.
Phillips, L. H., & Della Sala, S. (1996). Aging, intelligence, and anatomical segregation in the frontal lobes. Learning & Individual Differences, 10, 217–243.
Rabbitt, P. M. A. (1979). How old and young participants monitor and control responses for accuracy and speed. British Journal of Psychology, 70, 305–311.
Raven, J. C., Court, J. H., & Raven, J. (1988). Manual for Raven’s progressive matrices and vocabulary scales: Sec. 3. Standard progressive matrices. London: Lewis.
Scheffers, M. K., & Coles, M. G. H. (2000). Performance monitoring in a confusing world: Event-related brain activity, judgements of response accuracy, and types of errors. Journal of Experimental Psychology: Human Perception & Performance, 26, 141–151.
Scheffers, M. K., Coles, M. G. H., Bernstein, P., Gehring, W. J., & Donchin, E. (1996). Event-related brain potentials and error-related processing: An analysis of incorrect responses to go and no-go stimuli. Psychophysiology, 33, 42–53.
Sutton, R. S., & Barto, A. G. (1998). Reinforcement learning: An introduction. Cambridge, MA: MIT Press.
Van der Molen, M. W., & Ridderinkhof, K. R. (1998). The growing and aging brain: Life-span changes in brain and cognitive functioning. In A. Demetriou, W. Doise, & C. F. M. van Lieshout (Eds.), Life-span developmental psychology: A European perspective (pp. 35–99). Chichester, U.K.: Wiley.
Van der Veen, F. M., Nieuwenhuis, S., Van der Molen, M. W., Crone, E. A., & Jennings, J. R. (2001). Heart rate and error-related negativity reflect different aspects of feedback processing during probability learning. Manuscript in preparation.
Volkow, N. D., Gur, R. C., Wang, G. J., Fowler, J. S., Moberg, P. J., Ding, Y. S., Hitzemann, R., Smith, G., & Logan, J. (1998). Association between decline in brain dopamine activity with age and cognitive and motor impairment in healthy individuals. American Journal of Psychiatry, 155, 344–349.
Woestenburg, J. C., Verbaten, M. N., & Slangen J. L. (1983). The removal of the eye-movement artifact from the EEG by regression analysis in the frequency domain. Biological Psychology, 16, 127–147.
Yeung, N., Botvinick, M. M., & Cohen, J. D. (2001). The neural basis of error detection: Conflict monitoring and the error-related negativity. Manuscript submitted for publication.
Zeef, E. J., & Kok, A. (1993). Age-related differences in the timing of stimulus and response processes during visual selective attention: Performance and psychophysiological analyses. Psychophysiology, 30, 138–151.
Zeef, E. J., Sonke, C. J., Kok, A., Buiten, M. M., & Kenemans, J. L. (1996). Perceptual factors affecting age-related differences in focused attention: Performance and psychophysiological analyses. Psychophysiology, 33, 555–565.
Author information
Authors and Affiliations
Corresponding author
Additional information
The research of K.R.R. has been made possible by a fellowship of the Royal Netherlands Academy of Arts and Sciences.
Rights and permissions
About this article
Cite this article
Nieuwenhuis, S., Ridderinkhof, K.R., Talsma, D. et al. A computational account of altered error processing in older age: Dopamine and the error-related negativity. Cognitive, Affective, & Behavioral Neuroscience 2, 19–36 (2002). https://doi.org/10.3758/CABN.2.1.19
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.3758/CABN.2.1.19