Advertisement

Neural mechanisms supporting flexible performance adjustment during development

  • Eveline A. CroneEmail author
  • Kiki Zanolie
  • Linda Van Leijenhorst
  • P. Michiel Westenberg
  • Serge A. R. B. Rombouts
Article

Abstract

Feedback processing is crucial for successful performance adjustment following changing task demands. The present event-related fMRI study was aimed at investigating the developmental differences in brain regions associated with different aspects of feedback processing. Children age 8–11, adolescents age 14–15, and adults age 18–24 performed a rule switch task resembling the Wisconsin Card Sorting Task, and analyses focused on different types of negative and positive feedback. All age groups showed more activation in lateral orbitofrontal cortex (OFC), anterior cingulate cortex (ACC), dorsolateral prefrontal cortex (DLPFC), and superior parietal cortex following negative relative to positive performance feedback, but the regions contributed to different aspects of feedback processing and had separable developmental trajectories. OFC was adultlike by age 8–11, whereas parietal cortex was adultlike by age 14–15. DLPFC and ACC, in contrast, were still developing after age 14–15. These findings demonstrate that changes in separable neural systems underlie developmental differences in flexible performance adjustment. Supplementary data from this study are available online at the Psychonomic Society Archive of Norms, Stimuli, and Data, atwww.psychonomic.org/archive.

Keywords

Parietal Cortex Error Feedback Erroneous Response Correct Rule Correct Positive Feedback 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Supplementary material

Crone-CABN-2008.zip (19 kb)
Supplementary material, approximately 340 KB.

References

  1. Achenbach, T. M. (1991). Manual for the Child Behavior Checklist/ 4-18 and 1991 profile. Burlington: University of Vermont, Department of Psychiatry.Google Scholar
  2. Barceló, F., & Knight, R. T. (2002). Both random and perseverative errors underlie WCST deficits in prefrontal patients. Neuropsychologia, 40, 349–356.PubMedCrossRefGoogle Scholar
  3. Bechara, A., Damasio, H., & Damasio, A. R. (2000). Emotion, decision making and the orbitofrontal cortex. Cerebral Cortex, 10, 295–307.PubMedCrossRefGoogle Scholar
  4. Brett, M., Anton, J.-L., Valabregue, R., & Poline, J.-B. (2002, June). Region of interest analysis using an SPM toolbox. Paper presented at the 8th International Conference on Functional Mapping of the Human Brain, Sendai, Japan.Google Scholar
  5. Bunge, S. A., Hazeltine, E., Scanlon, M. D., Rosen, A. C., & Gabrieli, J. D. E. (2002). Dissociable contributions of prefrontal and parietal cortices to response selection. NeuroImage, 17, 1562–1571.PubMedCrossRefGoogle Scholar
  6. Casey, B. J., Tottenham, N., Liston, C., & Durston, S. (2005). Imaging the developing brain: What have we learned about cognitive development? Trends in Cognitive Sciences, 9, 104–110.PubMedCrossRefGoogle Scholar
  7. Cocosco, C. A., Kollokian, V., Kwan, R. K.-S., & Evans, A. C. (1997). BrainWeb: Online interface to a 3D MRI simulated brain database. NeuroImage, 5, S425.Google Scholar
  8. Crone, E. A., Donohue, S. E., Honomichl, R., Wendelken, C., & Bunge, S. A. (2006). Brain regions mediating flexible rule use during development. Journal of Neuroscience, 26, 11239–11247.PubMedCrossRefGoogle Scholar
  9. Crone, E. A., Jennings, J. R., & van der Molen, M. W. (2004). Developmental change in feedback processing as reflected by phasic heart rate changes. Developmental Psychology, 40, 1228–1238.PubMedCrossRefGoogle Scholar
  10. Crone, E. A., Ridderinkhof, K. R., Worm, M., Somsen, R. J. M., & van der Molen, M. W. (2004). Switching between spatial stimulus- response mappings: A developmental study of cognitive flexibility. Developmental Science, 7, 443–455.PubMedCrossRefGoogle Scholar
  11. Crone, E. A., Somsen, R. J. M., Zanolie, K., & van der Molen, M. W. (2006). A heart rate analysis of developmental change in feedback processing and rule shifting from childhood to early adulthood. Journal of Experimental Child Psychology, 95, 99–116.PubMedCrossRefGoogle Scholar
  12. Crone, E. A., van der Veen, F. M., van der Molen, M. W., Somsen, R. J. M., van Beek, B., & Jennings, J. R. (2003). Cardiac concomitants of feedback processing. Biological Psychology, 64, 143–156.PubMedCrossRefGoogle Scholar
  13. Crone, E. A., Wendelken, C., Donohue, S., Van Leijenhorst, L., & Bunge, S. A. (2006). Neurocognitive development of the ability to manipulate information in working memory. Proceedings of the National Academy of Sciences, 103, 9315–9320.CrossRefGoogle Scholar
  14. Dale, A. M. (1999). Optimal experimental design for event-related fMRI. Human Brain Mapping, 8, 109–114.PubMedCrossRefGoogle Scholar
  15. Davies, P. L., Segalowitz, S. J., & Gavin, W. J. (2004). Development of error-monitoring event-related potentials in adolescents. In R. E. Dahl & L. P. Spear (Eds.), Adolescent brain development: Vulnerabilities and opportunities (Annals of the New York Academy of Sciences, Vol. 1021, pp. 324-328). New York: New York Academy of Sciences.Google Scholar
  16. Demakis, G. J. (2003). A meta-analytic review of the sensitivity of the Wisconsin Card Sorting Test to frontal and lateralized frontal brain damage. Neuropsychology, 17, 255–264.PubMedCrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. Frank, M. J., & Claus, E. D. (2006). Anatomy of a decision: Striatoorbitofrontal interactions in reinforcement learning, decision making, and reversal. Psychological Review, 113, 300–326.PubMedCrossRefGoogle Scholar
  19. Galvan, A., Hare, T. A., Parra, C. E., Penn, J., Voss, H., Glover, G., & Casey, B. J. (2006). Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. Journal of Neuroscience, 26, 6885–6892.PubMedCrossRefGoogle Scholar
  20. Gogtay, N., Giedd, J. N., Lusk, L., Hayashi, K. M., Greenstein, D., Vaituzis, A. C., et al. (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences, 101, 8174–8179.CrossRefGoogle Scholar
  21. Gray, J. R., Chabris, C. F., & Braver, T. S. (2003). Neural mechanisms of general fluid intelligence. Nature Neuroscience, 6, 316–322.PubMedCrossRefGoogle Scholar
  22. Heaton, R. K., Chelune, G. J., Talley, J. L., Kay, G. C., & Curtiss, G. (1993). Wisconsin Card Sorting Test manual: Revised and expanded. Odessa, FL: Psychological Assessment Resources.Google Scholar
  23. Holroyd, C. B., & Coles, M. G. H. (2002). The neural basis of human error processing: Reinforcement learning, dopamine, and the errorrelated negativity. Psychological Review, 109, 679–709.PubMedCrossRefGoogle Scholar
  24. Holroyd, C. B., Nieuwenhuis, S., Yeung, N., Nystrom, L., Mars, R. B., Coles, M. G. H., & Cohen, J. D. (2004). Dorsal anterior cingulate cortex shows fMRI response to internal and external error signals. Nature Neuroscience, 7, 497–498.PubMedCrossRefGoogle Scholar
  25. Huizinga, M., Dolan, C. V., & van der Molen, M. W. (2006). Agerelated change in executive function: Developmental trends and a latent variable analysis. Neuropsychologia, 44, 2017–2036.PubMedCrossRefGoogle Scholar
  26. Kim, E. Y., Iwaki, N., Imashioya, H., Uno, H., & Fujita, T. (2007). Error-related negativity in a visual go/no-go task: Children vs. adults. Developmental Neuropsychology, 31, 181–191.PubMedGoogle Scholar
  27. Klingberg, T., Forssberg, H., & Westerberg, H. (2002). Increased brain activity in frontal and parietal cortex underlies the development of visuospatial working memory capacity during childhood. Journal of Cognitive Neuroscience, 14, 1–10.PubMedCrossRefGoogle Scholar
  28. Knutson, B., Fong, G. W., Bennett, S. M., Adams, C. M., & Hommer, D. (2003). A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: Characterization with rapid event-related fMRI. NeuroImage, 18, 263–272.PubMedCrossRefGoogle Scholar
  29. Ladouceur, C. D., Dahl, R. E., & Carter, C. S. (2004). ERP correlates of action monitoring in adolescence. In R. E. Dahl & L. P. Spear (Eds.), Adolescent brain development: Vulnerabilities and opportunities (Annals of the New York Academy of Sciences, Vol. 1021, pp. 329–336). New York: New York Academy of Sciences.Google Scholar
  30. Liston, C., Matalon, S., Hare, T. A., Davidson, M. C., & Casey, B. J. (2006). Anterior cingulate and posterior parietal cortices are sensitive to dissociable forms of conflict in a task-switching paradigm. Neuron, 50, 643–653.PubMedCrossRefGoogle Scholar
  31. Luciana, M., & Nelson, C. A. (1998). The functional emergence of prefrontally-guided working memory systems in four- to eight-yearold children. Neuropsychologia, 36, 273–293.PubMedCrossRefGoogle Scholar
  32. Luna, B., & Sweeney, J. A. (2004). The emergence of collaborative brain function: fMRI studies of the development of response inhibition. In R. E. Dahl & L. P. Spear (Eds.), Adolescent brain development: Vulnerabilities and opportunities (Annals of the New York Academy of Sciences, Vol. 1021, pp. 296–309). New York: New York Academy of Sciences.Google Scholar
  33. Mars, R. B., Coles, M. G. H., Grol, M. J., Holroyd, C. B., Nieuwenhuis, S., Hulstijn, W., & Toni, I. (2005). Neural dynamics of error processing in medial frontal cortex. NeuroImage, 28, 1007–1013.PubMedCrossRefGoogle Scholar
  34. Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24, 167–202.PubMedCrossRefGoogle Scholar
  35. Milner, B. (1963). Effects of different brain regions on card sorting: The role of the frontal lobes. Archives of Neurology, 9, 90–100.Google Scholar
  36. Monchi, O., Petrides, M., Petre, V., Worsley, K., & Dagher, A. (2001). Wisconsin Card Sorting revisited: Distinct neural circuits participating in different stages of the task identified by event-related functional magnetic resonance imaging. Journal of Neuroscience, 21, 7733–7741.PubMedGoogle Scholar
  37. Nieuwenhuis, S., Slagter, H. A., von Geusau, N. J. A., Heslenfeld, D. J., & Holroyd, C. B. (2005). Knowing good from bad: Differential activation of human cortical areas by positive and negative outcomes. European Journal of Neuroscience, 21, 3161–3168.PubMedCrossRefGoogle Scholar
  38. O’Doherty, J., Critchley, H., Deichmann, R., & Dolan, R. J. (2003). Dissociating valence of outcome from behavioral control in human orbital and ventral prefrontal cortices. Journal of Neuroscience, 23, 7931–7939.PubMedGoogle Scholar
  39. Ravizza, S. M., Delgado, M. R., Chein, J. M., Becker, J. T., & Fiez, J. A. (2004). Functional dissociations within the inferior parietal cortex in verbal working memory. NeuroImage, 22, 562–573.PubMedCrossRefGoogle Scholar
  40. Rizzolatti, G., Luppino, G., & Matelli, M. (1998). The organization of the cortical motor system: New concepts. Electroencephalography & Clinical Neurophysiology, 106, 283–296.CrossRefGoogle Scholar
  41. Rolls, E. T. (2004). The functions of the orbitofrontal cortex. Brain & Cognition, 55, 11–29.CrossRefGoogle Scholar
  42. Somsen, R. J. M. (2007). The development of attention regulation in the Wisconsin Card Sorting Task. Developmental Science, 10, 664–680.PubMedCrossRefGoogle Scholar
  43. Sowell, E. R., Thompson, P. M., Leonard, C. M., Welcome, S. E., Kan, E., & Toga, A. W. (2004). Longitudinal mapping of cortical thickness and brain growth in normal children. Journal of Neuroscience, 24, 8223–8231.PubMedCrossRefGoogle Scholar
  44. Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain: 3-dimensional proportional system. An approach to cerebral imaging (M. Rayport, Trans.). Stuttgart: Thieme.Google Scholar
  45. Van Leijenhorst, L., Crone, E. A., & Bunge, S. A. (2006). Neural correlates of developmental differences in risk estimation and feedback processing. Neuropsychologia, 44, 2158–2170.PubMedCrossRefGoogle Scholar
  46. van Veen, V., Holroyd, C. B., Cohen, J. D., Stenger, V. A., & Carter, C. S. (2004). Errors without conflict: Implications for performance monitoring theories of anterior cingulate cortex. Brain & Cognition, 56, 267–276.CrossRefGoogle Scholar
  47. Walton, M. E., Devlin, J. T., & Rushworth, M. F. S. (2004). Interactions between decision making and performance monitoring within prefrontal cortex. Nature Neuroscience, 7, 1259–1265.PubMedCrossRefGoogle Scholar
  48. Welsh, M. C., Pennington, B. F., & Groisser, D. B. (1991). A normative-developmental study of executive function: A window on prefrontal function in children. Developmental Neuropsychology, 7, 131–149.CrossRefGoogle Scholar
  49. Wiersema, J. R., van der Meere, J. J., & Roeyers, H. (2007). Developmental changes in error monitoring: An event-related potential study. Neuropsychologia, 45, 1649–1657.PubMedCrossRefGoogle Scholar
  50. Zanolie, K., Van Leijenhorst, L., Rombouts, S. A. R. B., & Crone, E. A. (2008). Separable neural mechanisms contribute to feedback processing in a rule-learning task. Neuropsychologia, 46, 117–126.PubMedCrossRefGoogle Scholar

Copyright information

© Psychonomic Society, Inc. 2008

Authors and Affiliations

  • Eveline A. Crone
    • 4
    • 1
    Email author
  • Kiki Zanolie
    • 4
    • 1
    • 2
  • Linda Van Leijenhorst
    • 4
    • 1
  • P. Michiel Westenberg
    • 4
    • 1
  • Serge A. R. B. Rombouts
    • 4
    • 1
    • 3
  1. 1.Leiden Institute for Brain and CognitionLeidenThe Netherlands
  2. 2.Erasmus University RotterdamRotterdamThe Netherlands
  3. 3.Leiden University Medical CenterLeidenThe Netherlands
  4. 4.Department of Developmental PsychologyLeiden UniversityLeidenThe Netherlands

Personalised recommendations