A cross-sectional and longitudinal analysis of reward-related brain activation: Effects of age, pubertal stage, and reward sensitivity
Open accessAbstract
Neurobiological models suggest that adolescents are driven by an overactive ventral striatum (VS) response to rewards that may lead to an adolescent increase in risk-taking behavior. However, empirical studies showed mixed findings of adolescents' brain response to rewards. In this study, we aimed to elucidate the relationship between reward-related brain activation and risky decision-making. In addition, we examined effects of age, puberty, and individuals' reward sensitivity. We collected two datasets: Experiment 1 reports cross-sectional brain data from 75 participants (ages 10-25) who played a risky decision task. Experiment 2 presents a longitudinal extension in which a subset of these adolescents (n=33) was measured again 2years later. Results showed that (1) a reward-related network including VS and medial PFC was consistently activated over time, (2) the propensity to choose the risky option was related to increased reward-related activation in VS and medial PFC, and (3) longitudinal comparisons indicated that self-reported reward sensitivity was specifically related to VS activation over time. Together, these results advance our insights in the brain circuitry underlying reward processing across adolescence.
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?
These findings are similar to several other studies that examined relations with BAS scales and neural responses to images of food or monetary rewards.
“These findings are similar to several other studies that examined relations with BAS scales and neural responses to images of food (Beaver et al., 2006) or monetary rewards (Costumero et al., 2013;van Duijvenvoorde et al., 2014).”
From Longitudinal Changes in Adolescent Risk-Taking: A Comprehensive Study of Neural Responses to Rewards, Pubertal Development, and Risk-Taking Behavior (2015) · cites this paper as van Duijvenvoorde et al., 2014
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
Saliency, switching, attention and control: a network model of insula function
Menon, V., & Uddin, L. Q. (2010) · Brain Structure and Function · doi:10.1007/s00429-010-0262-0 · Cited by 5,592 · see citing works
The reward circuit: linking primate anatomy and human imaging
Haber, S. N., & Knutson, B. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.129 · Cited by 3,718 · see citing works
Adolescent Brain Development: A Period of Vulnerabilities and Opportunities. Keynote Address
DAHL, R. E. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1308.001 · Cited by 1,667 · see citing works
Self-citationPubertal hormones organize the adolescent brain and behavior
Sisk, C. L., & Zehr, J. L. (2005) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2005.10.003 · Cited by 1,082 · see citing works
The role of puberty in the developing adolescent brain
Blakemore, S., Burnett, S., & Dahl, R. E. (2010) · Human Brain Mapping · doi:10.1002/hbm.21052 · Cited by 1,011 · see citing works
Self-citationDecision-making in the adolescent brain
Blakemore, S.-J., & Robbins, T. W. (2012) · Nature Neuroscience · doi:10.1038/nn.3177 · Cited by 711 · see citing works
Ernst, M., Nelson, E. E., Jazbec, S., McClure, E. B., Monk, C. S., Leibenluft, E., Blair, J., & Pine, D. S. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2004.12.038 · Cited by 635 · see citing works
Risk-taking and the adolescent brain: Who is at risk?
Galvan, A., Hare, T., Voss, H., Glover, G., & Casey, B. J. (2007) · Developmental Science · doi:10.1111/j.1467-7687.2006.00579.x · Cited by 568 · see citing works
Incentive-elicited brain activation in adolescents: Similarities and differences from young adults
Bjork, J. M., Knutson, B., Fong, G. W., Caggiano, D. M., Bennett, S. M., & Hommer, D. W. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.4862-03.2004 · Cited by 567 · see citing works
Adolescent risky decision-making: Neurocognitive development of reward and control regions
Van Leijenhorst, L., Moor, B. G., Op de Macks, Z. A., Rombouts, S. A. R. B., Westenberg, P. M., & Crone, E. A. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.02.038 · Cited by 467 · see citing works
Self-citationGambling near-misses enhance motivation to gamble and recruit win-related brain circuitry
Clark, L., Lawrence, A. J., Astley-Jones, F., & Gray, N. (2009) · Neuron · doi:10.1016/j.neuron.2008.12.031 · Cited by 410 · 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
Adolescents, adults and rewards: Comparing motivational neurocircuitry recruitment using fMRI
Bjork, J. M., Smith, A. R., Chen, G., & Hommer, D. W. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011440 · Cited by 271 · see citing works
Op de Macks, Z. A., Moor, B. G., Overgaauw, S., Güroğlu, B., Dahl, R. E., & Crone, E. A. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.06.003 · Cited by 203 · see citing works
Self-citationPadmanabhan, A., Geier, C. F., Ordaz, S. J., Teslovich, T., & Luna, B. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.06.004 · Cited by 202 · see citing works
Cho, Y. T., Fromm, S., Guyer, A. E., Detloff, A., Pine, D. S., Fudge, J. L., & Ernst, M. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2012.10.013 · Cited by 173 · see citing works
Functional neuroimaging of intertemporal choice models: a review
Carter, R. M., Meyer, J. R., & Huettel, S. A. (2010) · Journal of Neuroscience Psychology and Economics · doi:10.1037/a0018046 · Cited by 124 · see citing works
Berns, G. S., Moore, S., & Capra, C. M. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006773 · Cited by 91 · see citing works
Pubertal maturation and sex steroids are related to alcohol use in adolescents
de Water, E., Braams, B. R., Crone, E. A., & Peper, J. S. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.11.018 · Cited by 56 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 41
- Barkley-Levenson, E. E., Van Leijenhorst, L., & Galvan, A. (2013). Behavioral and neural correlates of loss aversion and risk avoidance in adolescents and adults. Developmental Cognitive Neuroscience, 3, 72-83. http://dx.doi.org/10.1016/ j.dcn.2012.09.007. · DOI · Paper page
- Beaver, J. D., Lawrence, A. D., Van Ditzhuijzen, J., Davis, M. H., Woods, A., & Calder, A. J. (2006). Individual differences in reward drive predict neural responses to images of food. Journal of Neuroscience, 26, 5160-5166. http://dx.doi.org/ 10.1523/JNEUROSCI.0350-06.2006. · DOI · Paper page
- Bjork, J. M., Knutson, B., & Hommer, D. W. (2008). Incentive-elicited striatal activation in adolescent children of alcoholics. Addiction, 103, 1308-1319. http://dx.doi.org/10.1111/j.1360-0443.2008.02250.x. · DOI · Paper page
- Buckholtz, J. W., Treadway, M. T., Cowan, R. L., Woodward, N. D., Benning, S. D., Li, R., et al. (2010). Mesolimbic dopamine reward system hypersensitivity in individuals with psychopathic traits. Nature Neuroscience, 13, 419-421. http:// dx.doi.org/10.1038/nn.2510. · DOI
- Carver, C. S., & White, T. L. (1994). Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: The BIS/BAS scales. Journal of Personality and Social Psychology, 67, 319-333.
- Cohen, M. X., Bour, L., Mantione, M., Figee, M., Vink, M., Tijssen, M. A. J., et al. (2012). Top-down directed synchrony from medial frontal cortex to nucleus accumbens during reward anticipation. Human Brain Mapping, 33, 246-252. http:// dx.doi.org/10.1002/hbm.21195. · DOI
- Delgado, M. R. (2007). Reward-related responses in the human striatum. Annals of the New York Academy of Sciences, 1104, 70-88. http://dx.doi.org/10.1196/ annals.1390.002. · DOI · Paper page
- Ernst, M., & Fudge, J. L. (2009). A developmental neurobiological model of motivated behavior: Anatomy, connectivity and ontogeny of the triadic nodes. Neuroscience and Biobehavioral Reviews, 33, 367-382. http://dx.doi.org/ 10.1016/j.neubiorev.2008.10.009. · DOI · Paper page
- Eshel, N., Nelson, E. E., Blair, J. R., Pine, D. S., & Ernst, M. (2007). Neural substrates of choice selection in adults and adolescents: Development of the ventrolateral prefrontal and anterior cingulate cortices. Neuropsychologia, 45, 1270-1279. http://dx.doi.org/10.1016/j.neuropsychologia.2006.10.004. · DOI · Paper page
- Forbes, E. E., Ryan, N. D., Phillips, M. L., Manuck, S. B., Worthman, C. M., Moyles, D. L., et al. (2010). Healthy adolescents' neural response to reward: Associations with puberty, positive affect, and depressive symptoms. Journal of the American Academy of Child and Adolescent Psychiatry, 49, 162-172.
- Friston, K. J., Buechel, C., Fink, G. R., Morris, J., Rolls, E., & Dolan, R. J. (1997). Psychophysiological and modulatory interactions in neuroimaging. NeuroImage, 6, 218-229. http://dx.doi.org/10.1006/nimg.1997.0291. · DOI · Paper page
- Galvan, A. (2010). Adolescent development of the reward system. Frontiers in Human Neuroscience, 4, 1-9. http://dx.doi.org/10.3389/neuro.09.006.2010. · DOI · Paper page
- Galvan, A., Hare, T. A., Davidson, M., Spicer, J., Glover, G., & Casey, B. J. (2005). The role of ventral frontostriatal circuitry in reward-based learning in humans. Journal of Neuroscience, 25, 8650-8656. http://dx.doi.org/10.1523/ JNEUROSCI.2431-05.2005. · DOI · Paper page
- Galvan, A., Hare, T. A., Parra, C. E., Penn, J., Voss, H., Glover, G., et al. (2006). Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. Journal of Neuroscience, 26, 6885-6892. http://dx.doi.org/10.1523/JNEUROSCI.1062-06.2006. · DOI · Paper page
- Gunther Moor, B., Op de Macks, Z., Gürog ˘lu, B., Rombouts, S. A. R. B., Van der Molen, M. W., & Crone, E. A. (2012). Neurodevelopmental changes of reading the mind in the eyes. Social Cognitive and Affective Neuroscience, 7, 44-52. http:// dx.doi.org/10.1093/scan/nsr020. · DOI
- Kennerley, S. W., & Walton, M. E. (2011). Decision making and reward in frontal cortex: Complementary evidence from neurophysiological and neuropsychological studies. Behavioral Neuroscience, 125, 297-317. http:// dx.doi.org/10.1037/a0023575. · DOI
- Kuhnen, C. M., & Knutson, B. (2005). The neural basis of financial risk taking. Neuron, 47, 763-770. http://dx.doi.org/10.1016/j.neuron.2005.08.008. · DOI · Paper page
- Liu, X., Powell, D. K., Wang, H., Gold, B. T., Corbly, C. R., & Joseph, J. E. (2007). Functional dissociation in frontal and striatal areas for processing of positive and negative reward information. Journal of Neuroscience, 27, 4587-4597. http://dx.doi.org/10.1523/JNEUROSCI.5227-06.2007. · DOI
- Luciana, M., & Collins, P. F. (2012). Incentive motivation, cognitive control, and the adolescent brain: Is it time for a paradigm shift? Child Development Perspectives, 6, 392-399. http://dx.doi.org/10.1111/j.1750-8606.2012.00252.x. · DOI · Paper page
- Mohr, P. N., Biele, G., & Heekeren, H. R. (2010). Neural processing of risk. Journal of Neuroscience, 30, 6613-6619. http://dx.doi.org/10.1523/JNEUROSCI.0003- 10.2010. · DOI · Paper page
- Nelson, E. E., Leibenluft, E., McClure, E. B., & Pine, D. S. (2005). The social re- orientation of adolescence: A neuroscience perspective on the process and its relation to psychopathology. Psychological Medicine, 35, 163-174. http:// dx.doi.org/10.1017/S0033291704003915. · DOI · Paper page
- Paulsen, D. J., McKell Carter, R., Platt, M. L., Huettel, S. A., & Brannon, E. M. (2012). Neurocognitive development of risk aversion from early childhood to adulthood. Frontiers in Human Neuroscience, 5, 178. http://dx.doi.org/10.3389/ fnhum.2011.00178. · DOI · Paper page
- Paulus, M. P., Rogalsky, C., Simmons, A., Feinstein, J. S., & Stein, M. B. (2003). Increased activation in the right insula during risk-taking decision making is related to harm avoidance and neuroticism. NeuroImage, 19, 1439-1448. http:// dx.doi.org/10.1016/S1053-8119(03)00251-9. · DOI · Paper page
- Peper, J. S., Mandl, R. C. W., Braams, B. R., de Water, E., Heijboer, A. C., Koolschijn, P. C. M. P., et al. (2012). Delay discounting and frontostriatalfiber tracts: A combined DTI and MTR study on impulsive choices in healthy young adults. Cerebral Cortex. http://dx.doi.org/10.1093/cercor/bhs163 (epub ahead of print). · DOI · Paper page
- Petersen, A. C., Crockett, L., Richards, M., & Boxer, A. (1988). A self-report measure of pubertal status: Reliability, validity, and initial norms. Journal of Youth and Adolescence, 17, 117-133. http://dx.doi.org/10.1007/BF01537962. · DOI · Paper page
- Rao, H., Korczykowski, M., Pluta, J., Hoang, A., & Detre, J. A. (2008). Neural correlates of voluntary and involuntary risk taking in the human brain: An fMRI study of the balloon analog risk task (BART). NeuroImage, 42, 902-910. http://dx.doi.org/ 10.1016/j.neuroimage.2008.05.046. · DOI
- Richards, J., Plate, R. C., & Ernst, M. (2013). A systematic review of fMRI reward paradigms used in studies of adolescents vs. adults: The impact of task design and implications for understanding neurodevelopment. Neuroscience and Biobehavioral Reviews, 37, 976-991. http://dx.doi.org/10.1016/ j.neubiorev.2013.03.004. · DOI · Paper page
- Rushworth, M., Mars, R. B., & Summerfield, C. (2012). General mechanisms for making decisions? Current Opinion in Neurobiology, 19, 75-83. http://dx.doi.org/ 10.1016/j.conb.2009.02.005. · DOI
- Rushworth, M., Noonan, M. P., Boorman, E. D., Walton, M. E., & Behrens, T. E. (2011). Frontal cortex and reward-guided learning and decision-making. Neuron, 70, 1054-1069. http://dx.doi.org/10.1016/j.neuron.2011.05.014. · DOI · Paper page
- Somerville, L. H., Jones, R. M., & Casey, B. J. (2010). A time of change: Behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues. Brain and Cognition, 72, 124-133. http://dx.doi.org/ 10.1016/j.bandc.2009.07.003. · DOI · Paper page
- Steinberg, L., Albert, D., Cauffman, E., Banich, M., Graham, S., & Woolard, J. (2008). Age differences in sensation seeking and impulsivity as indexed by behavior and self report: Evidence for a dual system model. Developmental Psychobiology, 44, 1764-1778. http://dx.doi.org/10.1037/a0012955. · DOI · Paper page
- Tom, S. M., Fox, C. R., Trepel, C., & Poldrack, R. A. (2007). The neural basis of loss aversion in decision-making under risk. Science, 315, 515-518. http:// dx.doi.org/10.1126/science.1134239. · DOI · Paper page
- Tricomi, E. M., Delgado, M. R., & Fiez, J. A. (2004). Modulation of caudate activity by action contingency. Neuron, 41, 281-292. http://dx.doi.org/10.1016/S0896- 6273(03)00848-1. · DOI
- Tymula, A., Rosenberg Belmaker, L. A., Roy, A. K., Ruderman, L., Manson, K., Glimcher, P. W., et al. (2012). Adolescents' risk-taking behavior is driven by tolerance to ambiguity. PNAS, 109, 17135-17140. http://dx.doi.org/10.1073/ pnas.1207144109. · DOI · Paper page
- Van den Bos, W., Cohen, M. X., Kahnt, T., & Crone, E. A. (2012). Striatum-medial prefrontal cortex connectivity predicts developmental changes in reinforcement learning. Cerebral Cortex, 22, 1247-1255. http://dx.doi.org/ 10.1093/cercor/bhr198. · DOI · Paper page
- Van Duijvenvoorde, A. C. K., & Crone, E. A. (2013). A neuroeconomic approach to adolescent decision-making. Current Directions in Psychological Science, 22, 108-113. http://dx.doi.org/10.1177/0963721413475446. · DOI
- Van Leijenhorst, L., Zanolie, K., Van Meel, C. S., Westenberg, P. M., Rombouts, S. A. R. B., & Crone, E. A. (2010). What motivates the adolescent? Brain regions mediating reward sensitivity across adolescence. Cerebral Cortex, 20, 61-69. http://dx.doi.org/10.1093/cercor/bhp078. · DOI · Paper page
- Wechsler, D. (1991). Wechsler intelligence scale for children-Manual (3rd ed.). San Antonio: The Psychological Corporation.
- Wechsler, D. (1997). Wechsler adult intelligence scale-Administration and scoring manual (3rd ed.). San Antonio: The Psychological Corporation.
- Xue, G., Lu, Z., Levin, I. P., Weller, J. A., Li, X., & Bechara, A. (2009). Functional dissociations of risk and reward processing in the medial prefrontal cortex. Cerebral Cortex, 19, 1019-1027. http://dx.doi.org/10.1093/cercor/bhn147. · DOI
- Yu, R., Branje, S. J. T., Keijsers, L., & Meeus, W. H. J. (2011). Psychometric characteristics of Carver and White's BIS/BAS scales in Dutch adolescents and their mothers. Journal of Personality Assessment, 93, 500-507. http://dx.doi.org/ 10.1080/00223891.2011.595745. · DOI
Cited by
Sorted by citations
The dual systems model: Review, reappraisal, and reaffirmation
Shulman, E. P., Smith, A. R., Silva, K., Icenogle, G., Duell, N., Chein, J., & Steinberg, L. (2016) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.12.010 · Cited by 867 · see citing works
“…(Collado et al., 2014; Kretschmer et al., 2014), and risk taking in laboratory contexts (Collado et al., 2014; Kretsch and Harden, 2014; Steinberg et al., 2008; but see van Duijvenvoorde et al., 2014 who did not find a correlation between pubertal status and performance on a gambling task).”
Braams, B. R., van Duijvenvoorde, A. C. K., Peper, J. S., & Crone, E. A. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.4764-14.2015 · Cited by 617 · see citing works
Self-citationSteinberg, L., Icenogle, G., Shulman, E. P., Breiner, K., Chein, J., Bacchini, D., Chang, L., Chaudhary, N., Giunta, L. D., Dodge, K. A., et al. (2018) · Developmental Science · doi:10.1111/desc.12532 · Cited by 514 · see citing works
Silverman, M. H., Jedd, K., & Luciana, M. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.07.083 · Cited by 277 · 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
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-citationHarden, K. P., Kretsch, N., Mann, F. D., Herzhoff, K., Tackett, J. L., Steinberg, L., & Tucker-Drob, E. M. (2017) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2016.12.007 · Cited by 77 · 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
Hasler, B. P., Casement, M. D., Sitnick, S. L., Shaw, D. S., & Forbes, E. E. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.02.024 · Cited by 59 · see citing works
Puberty and functional brain development in humans: convergence in findings?
Dai, J., & Scherf, K. S. (2019) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2019.100690 · Cited by 51 · see citing works
- Authors
- van Duijvenvoorde, A. C. K., Op de Macks, Z. A., Overgaauw, S., Gunther Moor, B., Dahl, R. E., & Crone, E. A.
- Affiliations
- Leiden University (NL)
- University of California, Berkeley (US)
- Venue
- Brain and Cognition
- Publisher
- Elsevier BV
- Published
- 2014-08
- Volume
- 89
- Pages
- 3-14
- ISSN
- 0278-2626 (ISSN-L)
- OpenAlex
- W2053837442
- Cited by
- 118
- References
- 19
- Citations by year
- 2026: 5 · 2024: 7 · 2023: 7 · 2022: 3 · 2021: 12 · 2020: 9 · 2019: 6 · 2018: 27 · 2017: 11 · 2016: 15 · 2015: 12 · 2014: 4
- FWCI
- 7.79
- Type
- journal article
- Language
- en
- Open access
- green
- escholarship.org
- Locations
- Brain and Cognition (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Social Sciences › Decision Sciences › General Decision Sciences › Decision-Making and Behavioral Economics
- Keywords
- reward processing, ventral striatum, medial prefrontal cortex, risky decision making, reward sensitivity, puberty, adolescence, age differences, risk-taking
- MeSH terms
- Adolescent, Adult, Age Factors, Brain Mapping, Child, Cross-Sectional Studies, Decision Making, Female, Humans, Longitudinal Studies, Magnetic Resonance Imaging, Male, Puberty, Reward, Risk-Taking, Prefrontal Cortex, Young Adult, Ventral Striatum
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
