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The Journal of Neuroscience, September 17, 2008, 28(38):9495-9503; doi:10.1523/JNEUROSCI.1485-08.2008

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Behavioral/Systems/Cognitive
Evaluating the Negative or Valuing the Positive? Neural Mechanisms Supporting Feedback-Based Learning across Development

Anna C. K. van Duijvenvoorde,^1,2,3 Kiki Zanolie,^1,3,4 Serge A. R. B. Rombouts,^1,3,5 Maartje E. J. Raijmakers,² and Eveline A. Crone^1,3

¹Leiden University Institute for Psychological Research, Leiden University, 2333 AK Leiden, The Netherlands, ²Department of Developmental Psychology, University of Amsterdam, 1018 WB Amsterdam, The Netherlands, ³Leiden Institute for Brain and Cognition, Leiden University, 2300 RC Leiden, The Netherlands, ⁴Department of Psychology, Erasmus University Rotterdam, 3000 DR Rotterdam, The Netherlands, and ⁵Department of Radiology, Leiden University Medical Center, 2333 ZA Leiden, The Netherlands

Correspondence should be addressed to Dr. Eveline A. Crone, Department of Developmental Psychology, Leiden University Institute for Psychological Research, Leiden University, Wassenaarseweg 52, 2333 AK Leiden, The Netherlands. Email: ecrone{at}fsw.leidenuniv.nl

How children learn from positive and negative performance feedback lies at the foundation of successful learning and is therefore of great importance for educational practice. In this study, we used functional magnetic resonance imaging (fMRI) to examine the neural developmental changes related to feedback-based learning when performing a rule search and application task. Behavioral results from three age groups (8–9, 11–13, and 18–25 years of age) demonstrated that, compared with adults, 8- to 9-year-old children performed disproportionally more inaccurately after receiving negative feedback relative to positive feedback. Additionally, imaging data pointed toward a qualitative difference in how children and adults use performance feedback. That is, dorsolateral prefrontal cortex and superior parietal cortex were more active after negative feedback for adults, but after positive feedback for children (8–9 years of age). For 11- to 13-year-olds, these regions did not show differential feedback sensitivity, suggesting that the transition occurs around this age. Pre-supplementary motor area/anterior cingulate cortex, in contrast, was more active after negative feedback in both 11- to 13-year-olds and adults, but not 8- to 9-year-olds. Together, the current data show that cognitive control areas are differentially engaged during feedback-based learning across development. Adults engage these regions after signals of response adjustment (i.e., negative feedback). Young children engage these regions after signals of response continuation (i.e., positive feedback). The neural activation patterns found in 11- to 13-year-olds indicate a transition around this age toward an increased influence of negative feedback on performance adjustment. This is the first developmental fMRI study to compare qualitative changes in brain activation during feedback learning across distinct stages of development.

Key words: development; fMRI; prefrontal cortex; cognitive control; learning; feedback

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Received Jan. 6, 2008; revised July 2, 2008; accepted Aug. 5, 2008.

Correspondence should be addressed to Dr. Eveline A. Crone, Department of Developmental Psychology, Leiden University Institute for Psychological Research, Leiden University, Wassenaarseweg 52, 2333 AK Leiden, The Netherlands. Email: ecrone{at}fsw.leidenuniv.nl

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