Striatum-medial prefrontal cortex connectivity predicts developmental changes in reinforcement learning
Open accessAbstract
During development, children improve in learning from feedback to adapt their behavior. However, it is still unclear which neural mechanisms might underlie these developmental changes. In the current study, we used a reinforcement learning model to investigate neurodevelopmental changes in the representation and processing of learning signals. Sixty-seven healthy volunteers between ages 8 and 22 (children: 8-11 years, adolescents: 13-16 years, and adults: 18-22 years) performed a probabilistic learning task while in a magnetic resonance imaging scanner. The behavioral data demonstrated age differences in learning parameters with a stronger impact of negative feedback on expected value in children. Imaging data revealed that the neural representation of prediction errors was similar across age groups, but functional connectivity between the ventral striatum and the medial prefrontal cortex changed as a function of age. Furthermore, the connectivity strength predicted the tendency to alter expectations after receiving negative feedback. These findings suggest that the underlying mechanisms of developmental changes in learning are not related to differences in the neural representation of learning signals per se but rather in how learning signals are used to guide behavior and expectations.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Previous studies found differential activations between adolescents and adults in striatal areas, but another study did not replicate that finding and instead found differences in connectivity between ventromedial prefrontal cortex and ventral striatum.
“While Cohen et al. (2010) found differential activations between adolescents and adults in striatal areas, van den Bos et al. (2012) were not able to replicate that finding, but found differences in the connectivity between the ventromedial prefrontal cortex and the ventral striatum.”
From Cognitive flexibility in adolescence: Neural and behavioral mechanisms of reward prediction error processing in adaptive decision making during development (2015) · cites this paper as van den Bos et al., 2012
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Holroyd, C. B., & Coles, M. G. H. (2002) · Psychological Review · doi:10.1037/0033-295x.109.4.679 · Cited by 4,027 · see citing works
Separate neural systems value immediate and delayed monetary rewards
McClure, S. M., Laibson, D. I., Loewenstein, G., & Cohen, J. D. (2004) · Science · doi:10.1126/science.1100907 · Cited by 3,089 · see citing works
Daw, N. D., Niv, Y., & Dayan, P. (2005) · Nature Neuroscience · doi:10.1038/nn1560 · Cited by 2,533 · see citing works
Functional and effective connectivity in neuroimaging: a synthesis
Friston, K. J. (1994) · Human Brain Mapping · doi:10.1002/hbm.460020107 · Cited by 2,452 · see citing works
Region of interest analysis using an SPM toolbox
Brett, M. (2002) · NeuroImage · Cited by 2,273 · see citing works
A framework for studying the neurobiology of value-based decision making
Rangel, A., Camerer, C., & Montague, P. R. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2357 · Cited by 2,184 · see citing works
Barto, A. (1998) · IFAC Proceedings Volumes · doi:10.1016/s1474-6670(17)38315-5 · Cited by 2,172 · see citing works
By Carrot or by Stick: Cognitive Reinforcement Learning in Parkinsonism
Frank, M. J., Seeberger, L. C., & O'Reilly, R. C. (2004) · Science · doi:10.1126/science.1102941 · Cited by 1,964 · see citing works
Zhang, B., Li, C., & Lin, N. (2020) · De Gruyter eBooks · doi:10.1515/9783110595567-011 · Cited by 1,939 · see citing works
Age-related change in executive function: Developmental trends and a latent variable analysis
Huizinga, M., Dolan, C. V., & van der Molen, M. W. (2006) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2006.01.010 · Cited by 1,636 · see citing works
Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans
Pessiglione, M., Seymour, B., Flandin, G., Dolan, R. J., & Frith, C. D. (2006) · Nature · doi:10.1038/nature05051 · Cited by 1,584 · see citing works
Temporal difference models and reward-related learning in the human brain
O'Doherty, J. P., Dayan, P., Friston, K., Critchley, H., & Dolan, R. J. (2003) · Neuron · doi:10.1016/s0896-6273(03)00169-7 · Cited by 1,522 · see citing works
FMRI visualization of brain activity during a monetary incentive delay task
Knutson, B., Westdorp, A., Kaiser, E., & Hommer, D. (2000) · NeuroImage · doi:10.1006/nimg.2000.0593 · Cited by 1,414 · see citing works
Galvan, A., Hare, T. A., Parra, C. E., Penn, J., Voss, H., Glover, G., & Casey, B. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1062-06.2006 · Cited by 1,282 · see citing works
Gläscher, J., Daw, N., Dayan, P., & O'Doherty, J. P. (2010) · Neuron · doi:10.1016/j.neuron.2010.04.016 · Cited by 1,166 · see citing works
Computational roles for dopamine in behavioural control
Montague, P. R., Hyman, S. E., & Cohen, J. D. (2004) · Nature · doi:10.1038/nature03015 · Cited by 966 · see citing works
Temporal Prediction Errors in a Passive Learning Task Activate Human Striatum
McClure, S. M., Berns, G. S., & Montague, P. R. (2003) · Neuron · doi:10.1016/s0896-6273(03)00154-5 · Cited by 917 · see citing works
Choice, uncertainty and value in prefrontal and cingulate cortex
Rushworth, M. F. S., & Behrens, T. E. J. (2008) · Nature Neuroscience · doi:10.1038/nn2066 · Cited by 866 · see citing works
Development of large-scale functional brain networks in children
Supekar, K., Musen, M., & Menon, V. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000157 · Cited by 807 · see citing works
Different time courses of learning-related activity in the prefrontal cortex and striatum.
Pasupathy, A., & Miller, E. K. (2005) · Nature · doi:10.1038/nature03287 · Cited by 712 · see citing works
Doya, K. (2008) · Nature Neuroscience · doi:10.1038/nn2077 · Cited by 642 · see citing works
Frank, M. J., & Claus, E. D. (2006) · Psychological Review · doi:10.1037/0033-295x.113.2.300 · Cited by 578 · see citing works
Adolescent development of the reward system
Galvan (2010) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.006.2010 · Cited by 521 · see citing works
(1997) · The MIT Press eBooks · doi:10.7551/mitpress/3917.003.0017 · Cited by 497 · see citing works
Activity in human ventral striatum locked to errors of reward prediction
Pagnoni, G., Zink, C. F., Montague, P. R., & Berns, G. S. (2002) · Nature Neuroscience · doi:10.1038/nn802 · Cited by 451 · see citing works
What Motivates the Adolescent? Brain Regions Mediating Reward Sensitivity across Adolescence
Van Leijenhorst, L., Zanolie, K., Van Meel, C. S., Westenberg, P. M., Rombouts, S. A. R. B., & Crone, E. A. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp078 · Cited by 449 · see citing works
Self-citationHaruno, M., & Kawato, M. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00382.2005 · Cited by 433 · see citing works
Crone, E. A., & van der Molen, M. W. (2004) · Developmental Neuropsychology · doi:10.1207/s15326942dn2503_2 · Cited by 433 · see citing works
Self-citationGenetically Determined Differences in Learning from Errors
Klein, T. A., Neumann, J., Reuter, M., Hennig, J., von Cramon, D. Y., & Ullsperger, M. (2007) · Science · doi:10.1126/science.1145044 · Cited by 424 · see citing works
Characterizing Stimulus–Response Functions Using Nonlinear Regressors in Parametric fMRI Experiments
Büchel, C., Holmes, A. P., Rees, G. E., & Friston, K. J. (1998) · NeuroImage · doi:10.1006/nimg.1998.0351 · Cited by 415 · see citing works
Hooper, C. J., Luciana, M., Conklin, H. M., & Yarger, R. S. (2004) · Developmental Psychology · doi:10.1037/0012-1649.40.6.1148 · Cited by 412 · see citing works
Schönberg, T., Daw, N. D., Joel, D., & O'Doherty, J. P. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2496-07.2007 · Cited by 390 · see citing works
Monk, C. S., Klein, R. G., Telzer, E. H., Schroth, E. A., Mannuzza, S., Moulton, J. L., Guardino, M., Masten, C. L., McClure-Tone, E. B., Fromm, S., et al. (2008) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2007.06111917 · Cited by 335 · see citing works
A unique adolescent response to reward prediction errors
Cohen, J. R., Asarnow, R. F., Sabb, F. W., Bilder, R. M., Bookheimer, S. Y., Knowlton, B. J., & Poldrack, R. A. (2010) · Nature Neuroscience · doi:10.1038/nn.2558 · Cited by 285 · see citing works
Velanova, K., Wheeler, M. E., & Luna, B. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn012 · Cited by 277 · see citing works
Prefrontal Cortex Fails to Learn from Reward Prediction Errors in Alcohol Dependence
Park, S. Q., Kahnt, T., Beck, A., Cohen, M. X., Dolan, R. J., Wrase, J., & Heinz, A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5587-09.2010 · Cited by 257 · see citing works
Self-citationWhite matter development during adolescence as shown by diffusion MRI
Schmithorst, V. J., & Yuan, W. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.06.005 · Cited by 249 · see citing works
van Duijvenvoorde, A. C. K., Zanolie, K., Rombouts, S. A. R. B., Raijmakers, M. E. J., & Crone, E. A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1485-08.2008 · Cited by 211 · see citing works
Self-citationFunctional connectivity with anterior cingulate and orbitofrontal cortices during decision-making
Cohen, M. X., Heller, A. S., & Charan Ranganath, A. (2005) · Cognitive Brain Research · doi:10.1016/j.cogbrainres.2005.01.010 · Cited by 198 · see citing works
Self-citationReinforcement learning, conditioning, and the brain: Successes and challenges
Maia, T. V. (2009) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.9.4.343 · Cited by 184 · see citing works
Nonlinear Regression in Parametric Activation Studies
Büchel, C., Wise, R. J. S., Mummery, C. J., Poline, J.-B., & Friston, K. J. (1996) · NeuroImage · doi:10.1006/nimg.1996.0029 · Cited by 163 · see citing works
Functional connectivity of reward processing in the brain
Camara, E. (2008) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.019.2008 · Cited by 141 · see citing works
Developmental differences in learning and error processing: Evidence from ERPs
Eppinger, B., Mock, B., & Kray, J. (2009) · Psychophysiology · doi:10.1111/j.1469-8986.2009.00838.x · Cited by 137 · see citing works
Learning to avoid in older age.
Frank, M. J., & Kong, L. L. (2008) · Psychology and Aging · doi:10.1037/0882-7974.23.2.392 · Cited by 130 · see citing works
Reward networks in the brain as captured by connectivity measures
Càmara, E. (2009) · Frontiers in Neuroscience · doi:10.3389/neuro.01.034.2009 · Cited by 116 · see citing works
Cohen, M. X., Elger, C. E., & Weber, B. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.10.004 · Cited by 106 · see citing works
Self-citationKahnt, T., Park, S. Q., Cohen, M. X., Beck, A., Heinz, A., & Wrase, J. (2008) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21092 · Cited by 101 · see citing works
Self-citationNeural mechanisms supporting flexible performance adjustment during development
Crone, E. A., Zanolie, K., Van Leijenhorst, L., Westenberg, P. M., & Rombouts, S. A. R. B. (2008) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/cabn.8.2.165 · Cited by 98 · see citing works
Self-citationvan den Bos, W. (2009) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.052.2009 · Cited by 89 · see citing works
Early development of subcortical regions involved in non-cued attention switching
Casey, B. J., Davidson, M. C., Hara, Y., Thomas, K. M., Martinez, A., Galvan, A., Halperin, J. M., Rodríguez‐Aranda, C. E., & Tottenham, N. (2004) · Developmental Science · doi:10.1111/j.1467-7687.2004.00377.x · Cited by 80 · see citing works
Developmental Change in Feedback Processing as Reflected by Phasic Heart Rate Changes.
Crone, E. A., Jennings, J. R., & van der Molen, M. W. (2004) · Developmental Psychology · doi:10.1037/0012-1649.40.6.1228 · Cited by 78 · see citing works
Self-citationMünte, T. F. (2008) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.011.2007 · Cited by 67 · see citing works
Behavioral and neural predictors of upcoming decisions
Cohen, M. X., & Charan Ranganath, A. (2005) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.5.2.117 · Cited by 65 · see citing works
Self-citationDynamic object representations in infants with and without fragile X syndrome
Farzin, F. (2010) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.012.2010 · Cited by 43 · see citing works
Xiong (1999) · doi:10.1002/(sici)1097-0193(1999)8:2/3
Flagged first, then by citations
Research works printed but not linked: 3
- Cosoco CA, Kollokian V, Kwan RKS, Evans AC. Brainweb: online interface of a 3-d mri simulated brain database. Neuroimage. 1997:5–s425. [Google Scholar]
- Wechsler D. Wechsler intelligence scale for children-third edition. Manual. San Antonio (TX): The Psychological Corporation; 1991. [Google Scholar]
- Wechsler D. Wechsler adult intelligence scale—third edition. Administration and scoring manual. San Antonio (TX): The Psychological Corporation; 1997. [Google Scholar]
Cited by
Sorted by citations
Understanding adolescence as a period of social–affective engagement and goal flexibility
Crone, E. A., & Dahl, R. E. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3313 · Cited by 2,507 · see citing works
Self-citationImportance of investing in adolescence from a developmental science perspective
Dahl, R. E., Allen, N. B., Wilbrecht, L., & Suleiman, A. B. (2018) · Nature · doi:10.1038/nature25770 · Cited by 1,196 · see citing works
Beyond simple models of self-control to circuit-based accounts of adolescent behavior
Casey, B. J. (2015) · Annual Review of Psychology · doi:10.1146/annurev-psych-010814-015156 · Cited by 742 · see citing works
Social re-orientation and brain development: An expanded and updated view
Nelson, E. E., Jarcho, J. M., & Guyer, A. E. (2016) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.12.008 · Cited by 447 · see citing works
Future Directions in Emotion Dysregulation and Youth Psychopathology
Beauchaine, T. P. (2015) · Journal of Clinical Child & Adolescent Psychology · doi:10.1080/15374416.2015.1038827 · Cited by 394 · see citing works
Hauser, T. U., Iannaccone, R., Walitza, S., Brandeis, D., & Brem, S. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2014.09.018 · Cited by 203 · see citing works
Beyond simple models of adolescence to an integrated circuit-based account: A commentary
Casey, B., Galván, A., & Somerville, L. H. (2016) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.12.006 · Cited by 206 · see citing works
Smith, A. R., Chein, J., & Steinberg, L. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.03.006 · Cited by 214 · see citing works
Fouragnan, E., Retzler, C., & Philiastides, M. G. (2018) · Human Brain Mapping · doi:10.1002/hbm.24047 · Cited by 176 · see citing works
A computational reward learning account of social media engagement
Lindström, B., Bellander, M., Schultner, D. T., Chang, A., Tobler, P. N., & Amodio, D. M. (2021) · Nature Communications · doi:10.1038/s41467-020-19607-x · Cited by 185 · see citing works
Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex?
Piekarski, D. J., Johnson, C. M., Boivin, J. R., Thomas, A. W., Lin, W. C., Delevich, K., M. Galarce, E., & Wilbrecht, L. (2017) · Brain Research · doi:10.1016/j.brainres.2016.08.042 · Cited by 175 · see citing works
Crone, E. A., van Duijvenvoorde, A. C. K., & Peper, J. S. (2016) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12502 · Cited by 174 · see citing works
Self-citationEarly adversity and learning: implications for typical and atypical behavioral development
Hanson, J. L., van den Bos, W., Roeber, B. J., Rudolph, K. D., Davidson, R. J., & Pollak, S. D. (2017) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12694 · Cited by 136 · see citing works
Self-citationAdolescent-specific patterns of behavior and neural activity during social reinforcement learning
Jones, R. M., Somerville, L. H., Li, J., Ruberry, E. J., Powers, A., Mehta, N., Dyke, J., & Casey, B. J. (2014) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-014-0257-z · Cited by 127 · see citing works
Experiential reward learning outweighs instruction prior to adulthood
Decker, J. H., Lourenco, F. S., Doll, B. B., & Hartley, C. A. (2015) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-014-0332-5 · Cited by 96 · see citing works
Adolescent brain development and contextual influences: a decade in review
Galván, A. (2021) · Journal of Research on Adolescence · doi:10.1111/jora.12687 · Cited by 77 · see citing works
Jarcho, J. M., Romer, A. L., Shechner, T., Galvan, A., Guyer, A. E., Leibenluft, E., Pine, D. S., & Nelson, E. E. (2015) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.03.002 · Cited by 70 · see citing works
Parr, A. C., Calabro, F., Larsen, B., Tervo-Clemmens, B., Elliot, S., Foran, W., Olafsson, V., & Luna, B. (2021) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2021.101997 · Cited by 60 · see citing works
Teslovich, T., Mulder, M., Franklin, N. T., Ruberry, E. J., Millner, A., Somerville, L. H., Simen, P., Durston, S., & Casey, B. J. (2014) · Developmental Science · doi:10.1111/desc.12092 · Cited by 45 · see citing works
Reward feedback processing in children and adolescents: medial frontal theta oscillations
Crowley, M. J., van Noordt, S. J. R., Wu, J., Hommer, R. E., South, M., Fearon, R. M. P., & Mayes, L. C. (2014) · Brain and Cognition · doi:10.1016/j.bandc.2013.11.011 · Cited by 45 · see citing works
- Authors
- van den Bos, W., Cohen, M. X., Kahnt, T., & Crone, E. A.
- Affiliations
- University of Amsterdam (NL)
- Bernstein Center for Computational Neuroscience Berlin (DE)
- Leiden University (NL)
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2012-06
- Volume
- 22
- Issue
- 6
- Pages
- 1247-1255
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- PMC
- PMC6283353
- OpenAlex
- W2167747364
- Cited by
- 276
- References
- 55
- Citations by year
- 2026: 6 · 2025: 15 · 2024: 17 · 2023: 19 · 2022: 23 · 2021: 26 · 2020: 27 · 2019: 17 · 2018: 33 · 2017: 19 · 2016: 23 · 2015: 18 · 2014: 19 · 2013: 9 · 2012: 4
- FWCI
- 5.29
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Cerebral Cortex (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- UvA-DARE (University of Amsterdam) (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Leiden Repository (Leiden University) (submittedVersion)
- UvA-DARE (University of Amsterdam) (submittedVersion)
- Funders
- National Institute of Mental Health (R01MH091068)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Keywords
- brain development, reinforcement learning, ventral striatum, medial prefrontal cortex, functional connectivity, prediction error, negative feedback, expected value, probabilistic learning, children, adolescents, age differences
- MeSH terms
- Adolescent, Child, Corpus Striatum, Female, Forecasting, Humans, Learning, Male, Neural Pathways, Photic Stimulation, Psychomotor Performance, Reinforcement, Psychology, Prefrontal Cortex, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
