CoChat
Sign Up
Cited by 521Neural and Behavioral Psychology StudiesNeurotransmitter Receptor Influence on BehaviorGambling Behavior and Treatments

Adolescent development of the reward system

Open access
Galvan·2010·Frontiers in Human Neuroscience
DOI 10.3389/neuro.09.006.2010PMC PMC2826184
Open this paper in CoChat — free accountOpen PDF

Abstract

Adolescence is a developmental period characterized by increased reward-seeking behavior. Investigators have used functional magnetic resonance imaging (fMRI) in conjunction with reward paradigms to test two opposing hypotheses about adolescent developmental changes in the striatum, a region implicated in reward processing. One hypothesis posits that the striatum is relatively hypo-responsive to rewards during adolescence, such that heightened reward-seeking behavior is necessary to achieve the same activation as adults. Another view suggests that during adolescence the striatal reward system is hyper-responsive, which subsequently results in greater reward-seeking. While evidence for both hypotheses has been reported, the field has generally converged on this latter hypothesis based on compelling evidence. In this review, I describe the evidence to support this notion, speculate on the disparate fMRI findings and conclude with future areas of inquiry to this fascinating question.

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/neuro.09.006.2010

Cites

12 of 12 references verified0 citation errors · 0 not checkable

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.

A few free checks a day · papers already verified open instantly · results are public

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?

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

Flagged first, then by citations

Research works printed but not linked: 64

  1. Andersen S. L. Dumont N. L. Teicher M. H. (1997). Developmental differences in dopamine synthesis inhibition by 7-OH-DPAT. Naunyn Schmiedebergs Arch. Pharmacol. 356, 173– 181 10.1007/PL00005038 9272722 · DOI
  2. Andersen S. L. Gazzara R. A. (1993). The ontogeny of apomorphine-induced alterations of neostriatal dopamine release: effects of spontaneous release. J. Neurochem. 61, 2247– 2255 10.1111/j.1471-4159.1993.tb07466.x 8245975 · DOI
  3. Andersen S. L Teicher M. H. (2000). Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse 37, 167– 169 10.1002/1098-2396(200008)37:2<167::AID-SYN11>3.0.CO;2-B 10881038 · DOI
  4. Bandettini P. A. Ungerleider L. G. (2001). From neuron to BOLD: new connections. Nat. Neurosci. 412, 864– 866 10.1038/nn0901-864 11528412 · DOI
  5. Benca R. M. (2004). Regulation of sleep and arousal: Introduction to part VII. Ann. N. Y. Acad. Sci. 1021, 260– 261 10.1196/annals.1308.030 15251895 · DOI
  6. Blum K. Braverman E. Holder J. Lubar J. Monastra V. Miller D. Lubar J. Chen T. Comings D. (2000). Reward deficiency syndrome: a biogenetic model for the diagnosis and treatment of impulsive, addictive and compulsive behaviors. J. Psychoactive Drugs 2, 1– 112 11280926
  7. Bolanos C. A. Glatt S. J. Jackson D. (1998). Subsensitivity to dopaminergic drugs in periadolescent rats: a behavioral and neurochemical analysis. Dev. Brain Res. 111, 25– 33 10.1016/S0165-3806(98)00116-3 9804875 · DOI
  8. Brenhouse H. C. Sonntag K. C. Andersen S. L. (2008). Transient D1 dopamine receptor expression on prefrontal cortex projection neurons: relationship to enhanced motivational salience of drug cues in adolescence. J. Neurosci. 28, 2375– 2382 10.1523/JNEUROSCI.5064-07.2008 18322084 PMC4028226 · DOI · Paper page
  9. Casey B. J. Galván A. Hare T. A. (2005). Changes in cerebral functional organization during cognitive development. Curr. Opin. Neurobiol. 15, 239– 244 10.1016/j.conb.2005.03.012 15831409 · DOI
  10. Casey B. J. Getz S. Galván A. (2008). The adolescent brain. Dev. Rev. 28, 62– 77 18688292 PMC2500212
  11. Caviness V. Kennedy D. Richelme C. Rademacher J. Filipek P. (1996). The human brain age 7–11 years: a volumetric analysis based on magnetic resonance images. Cereb. Cortex 6, 726– 736 10.1093/cercor/6.5.726 8921207 · DOI · Paper page
  12. Chambers R. A. Taylor J. R. Potenza M. N. (2003). Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability. Am. J. Psychiatry 160, 1041– 1052 10.1176/appi.ajp.160.6.1041 12777258 PMC2919168 · DOI · Paper page
  13. Csikszentmihalyi M. Larson R. Prescott S. (1977). The ecology of adolescent activity and experience. J. Youth Adolesc. 6, 281– 294 10.1007/BF02138940 24408457 · DOI · Paper page
  14. Dahl R. E. Lewin D. S. (2002). Pathways to adolescent health sleep regulation and behavior. J. Adolesc. Health 31, 175– 184 10.1016/S1054-139X(02)00506-2 12470913 · DOI
  15. DeGraff C. Zandstra E. (1999). Sweetness intensity and pleasantness in children, adolescents and adults. Physiol. Behav. 67, 513– 520 10.1016/S0031-9384(99)00090-6 10549887 · DOI
  16. Eigsti I. M. Zayas V. Mischel W. Shoda Y. Ayduk O. Dadlani M. B. Davidson M. C. Lawrence Aber J. Casey B. J. (2006). Predicting cognitive control from preschool to late adolescence and young adulthood. Psychol. Sci. 17, 478– 484 10.1111/j.1467-9280.2006.01732.x 16771797 · DOI · Paper page
  17. Ernst M. Mueller S. C. (2008). The adolescent brain: insights from functional neuroimaging research. Dev Neurobiol 68, 729– 743 10.1002/dneu.20615 18383544 PMC2788780 · DOI
  18. Ernst M. Romeo R. D. Andersen S. L. (2009). Neurobiology of the development of motivated behaviors in adolescence: a window into a neural systems model. Pharmacol. Biochem. Behav. 93, 199– 211 10.1016/j.pbb.2008.12.013 19136024 · DOI
  19. Eshel N. Nelson E. E. Blair R. J. 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 10.1016/j.neuropsychologia.2006.10.004 17118409 PMC2700731 · DOI · Paper page
  20. Galván 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. J. Neurosci. 26, 6885– 6892 10.1523/JNEUROSCI.1062-06.2006 16793895 PMC6673830 · DOI · Paper page
  21. Geier C. F. Terwilliger R. Teslovich T. Velanova K. Luna B. (2009). Immaturities in reward processing and its influence on inhibitory control in adolescence. Cereb. Cortex [Epub ahead of print]. 19875675 PMC2882823
  22. Giedd J. N. (2004). Structural MRI of the Adolescent Brain. Ann. N. Y. Acad. Sci. 1021: 77 10.1196/annals.1308.009 15251877 · DOI · Paper page
  23. Giedd J. N. Blumenthal J. Jeffries N. O. Castellanos F.X Liu H Zijdenbos A. Paus T. Evans A. C. Rapoport J. L. (1999). Brain development during childhood and adolescence: a longitudinal MRI study. Nat. Neurosci. 2, 861– 863 10.1038/13158 10491603 · DOI · Paper page
  24. Giedd J. N. Snell J. Lange N. Rajapakse J. Casey B. Kozuch P. Vaituzis A. Vauss Y. Hamburger S. Kaysen D. Rapoport J. L. (1996). Quantitative magnetic resonance imaging of human brain development: ages 4–18. Cereb. Cortex 6 551– 560 10.1093/cercor/6.4.551 8670681 · DOI · Paper page
  25. Guyer A. E. McClure-Tone E. B. Shiffrin N. D. Pine D. S. Nelson E. E. (2009). Probing the neural correlates of anticipated peer evaluation in adolescence. Child Dev. 80, 1000– 1015 10.1111/j.1467-8624.2009.01313.x 19630890 PMC2791675 · DOI · Paper page
  26. Holm S. M. Forbes E. E. Ryan N. D. Phillips M. L. Tarr J. A. Rahl R. E. (2009). Reward-related brain function and sleep in pre/early pubertal and mid/ate pubertal adolescents. J. Adolesc. Health 45, 319– 320 10.1016/j.jadohealth.2009.04.001 19766936 PMC2817965 · DOI · Paper page
  27. Kennedy D. N. Haselgrove C. McInerney S. (2003). MRI-based morphometric of typical and atypical brain development. Ment. Retard Dev. Disabil. Res. Rev. 9, 155– 160 10.1002/mrdd.10075 12953294 · DOI
  28. Knutson B. Fong G. W. Adams C. M. Varner J. L. Hommer D. (2001). Dissociation of reward anticipation and outcome with event-related fMRI. Neuroreport 12, 3683– 3687 10.1097/00001756-200112040-00016 11726774 · DOI · Paper page
  29. Koob G. F. Swerdlow N. R. (1988). The functional output of the mesolimbic dopamine system. Ann. N. Y. Acad. Sci. 537, 216– 227 10.1111/j.1749-6632.1988.tb42108.x 3059925 · DOI · Paper page
  30. Kotsoni E. Byrd D. Casey B. J. (2006). Special considerations for functional magnetic resonance imaging of pediatric populations. J. Magn. Reson. Imaging 23, 877– 886 10.1002/jmri.20578 16649204 PMC3014526 · DOI
  31. Kuhnen C. M. Knutson B. (2005). The neural basis of financial risk taking. Neuron 47, 763– 770 10.1016/j.neuron.2005.08.008 16129404 · DOI · Paper page
  32. Laviola G. Macri S. Morley-Fletcher S. Adriani W. (2003). Risk-taking behavior in adolescent mice: psychobiological determinants and early epigenetic influence. Neurosci. Biobehav. Rev. 27, 19– 31 10.1016/S0149-7634(03)00006-X 12732220 · DOI · Paper page
  33. Laviola G. Pascucci T. Pieretti S. (2001). Striatal dopamine sensitization to D-amphetamine in periadolescent but not in adult rats. Pharmacol. Biochem. Behav. 68, 115– 124 10.1016/S0091-3057(00)00430-5 11274716 · DOI · Paper page
  34. Maggs J. L Almeida D. M Galambos N. L. (1995). Risky business: the paradoxical meaning of problem behavior for young adolescents. J. Early Adolesc. 15, 344– 362 10.1177/0272431695015003004 · DOI
  35. Matthews S. C. Simmons A. N. Lane S. D. Paulus M. P. (2004). Selective activation of the nucleus accumbens during risk-taking decision making. Neuroreport 15, 2123– 2127 10.1097/00001756-200409150-00025 15486494 · DOI · Paper page
  36. May J. C. Delgado M. R. Dahl R. E. Stenger V. A. Ryan N. D. Fiez J. A. Carter C. S. (2004). Event-related functional magnetic resonance imaging of reward-related brain circuitry in children and adolescents. Biol. Psychiatry 55, 359– 366 10.1016/j.biopsych.2003.11.008 14960288 · DOI
  37. Montague D. M. Lawler C. P. Mailman R. B. Gilmore J. H. (1999). Developmental regulation of the dopamine D1 receptor in human caudate and putamen. Neuropsychopharmacology 21, 641– 649 10.1016/S0893-133X(99)00062-7 10516960 · DOI
  38. Montague P. R. Berns G. S. (2002). Neural economics and the biological substrates of valuation. Neuron 36, 265– 284 10.1016/S0896-6273(02)00974-1 12383781 · DOI · Paper page
  39. Palacios J. M. Camps M. Corte R. Probst A. (1988). Mapping dopamine receptors in the human brain. J. Neural. Transm. Suppl. 27, 227– 235 2969952
  40. Panksepp J. (1998). Affective Neuroscience. New York, Oxford University Press
  41. Paus T. Keshavan M Giedd J. N. (2008). Why do so many psychiatric disorders emerge during adolescence? Nat. Rev. Neurosci. 9, 947– 957 19002191 PMC2762785
  42. Rutter M. Graham P. Chadwick O. Yule W. (1976). Adolescent turmoil: fact or fiction? J. Child Psychol. Psychiatry 17, 35– 56 10.1111/j.1469-7610.1976.tb00372.x 1249139 · DOI
  43. Schlaggar B. L. Brown T. T. Lugar H. M. Visscher K. M. Miezin F. M. Petersen S. E. (2002). Functional neuroanatomical differences between adults and school-age children in the processing of single words. Science 296, 1476– 1479 10.1126/science.1069464 12029136 · DOI · Paper page
  44. Schultz W. (1998). Predictive reward signal of dopamine neurons. J. Neurophysiol. 80, 1– 27 9658025
  45. Seeman P. Bzowej N. H. Guan H.-C. Bergeron C. Becker L. E. Reynolds G. P. Bird E. D. Riederer P. Jellinger K. Watanabe S. Tourtellotte W. W. (1987). Human brain dopamine receptors in children and aging adults. Synapse 1, 399– 404 10.1002/syn.890010503 3505371 · DOI · Paper page
  46. Shaw P. Kabani N. J. Lerch J. P. Eckstrand K. Lenroot R. Gogtay N. Greenstein D. Clasen L. Evans A. Rapoport J. L. Giedd J. N. Wise S. P. (2008). Neurodevelopmental trajectories of the human cerebral cortex. J. Neurosci. 28, 3586– 3594 10.1523/JNEUROSCI.5309-07.2008 18385317 PMC6671079 · DOI · Paper page
  47. Somerville L. H. Jones R. M. Casey B. J. (2009). A time of change: Behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues. Brain Cogn. [Epub ahead of print]. PMC2814936 19695759
  48. Sowell E. R. Peterson B. S. Thompson P. M. Welcome S. E. Henkenius A. L. Toga A. W. (2003). Mapping cortical change across the human life span. Nat. Neurosci. 6, 309– 315 10.1038/nn1008 12548289 · DOI · Paper page
  49. Sowell E. R. Thompson P. M. Holmes C. J. Jernigan T. L. Toga A. W. (1999). In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nat. Neurosci. 2, 859– 861 10.1038/13154 10491602 · DOI · Paper page
  50. Spear L. P. (2000). The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. Rev. 24, 417– 463 10.1016/S0149-7634(00)00014-2 10817843 · DOI · Paper page
  51. Stamford J. A. (1989). Development and ageing of the rat nigrostriatal dopamine system studied with fast cyclic voltammetry. J. Neurochem. 52, 1582– 1589 10.1111/j.1471-4159.1989.tb09212.x 2709014 · DOI
  52. Steinberg L. (2004). Risk taking in adolescence: what changes, and why? Ann. N. Y. Acad. Sci. 1021, 51– 58 10.1196/annals.1308.005 15251873 · DOI · Paper page
  53. Steinberg L. (2005). A social neuroscience perspective on adolescent risk-taking. Dev. Rev. 28, 78– 106 10.1016/j.dr.2007.08.002 18509515 PMC2396566 · DOI · Paper page
  54. Steinberg L. (2008). A social neuroscience perspective on adolescent risk- taking. Dev. Rev 28, 78– 106 10.1016/j.dr.2007.08.002 18509515 PMC2396566 · DOI · Paper page
  55. Tarazi F. I. Tomasini E. C. Baldessarini R. J. (1998). Postnatal development of dopamine D4-like receptors in rat forebrain regions: comparison with D2-like receptors. Dev. Brain Res. 110, 227– 233 10.1016/S0165-3806(98)00111-4 9748595 · DOI · Paper page
  56. Tarazi F. I. Tomasini E. C. Baldessarini R. J. (1999). Postnatal development of dopamine D1-like receptors in rat cortical and striatolimbic brain regions: an autoradiographic study. Dev. Neurosci. 21, 43– 49 10.1159/000017365 10077701 · DOI · Paper page
  57. Teicher M. H. Andersen S. L. Hostetter J. C. Jr. (1995). Evidence for dopamine receptor pruning between adolescence and adulthood in striatum but not nucleus accumbens. Dev. Brain Res. 89, 167– 172 10.1016/0165-3806(95)00109-Q 8612321 · DOI · Paper page
  58. Teicher M. H. Barber N. I. Gelbard H. A. Gallitano A. L. Campbell A Marsh E Baldessarini R. J. (1993). Developmental differences in acute nigrostriatal and mesocorticolimbic system response to haloperidol. Neuropsychopharmacology 9, 147– 156 8216697
  59. Thomason M. E. Burrows B. E. Gabrieli J. D. E. Glover G. H. (2005). Breath holding reveals differences in fMRI BOLD signal in children, and adults. Neuroimage 25, 824– 837 10.1016/j.neuroimage.2004.12.026 15808983 · DOI · Paper page
  60. 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 10.1126/science.1134239 17255512 · DOI · Paper page
  61. van de Moortele P. F. Pfeuffer J. Glover G. H. Ugurbil K. Hu X. (2002). Respiration-induced B0 fluctuations and their spatial distribution in the human brain at 7 Tesla. Magn. Reson. Med. 47, 888– 895 10.1002/mrm.10145 11979567 · DOI
  62. van Leijenhorst L. Zanolie K. van Meel C. S. Westenberg P. M Rombouts S. A Crone E. A. (2009). What motivates the adolescent? Brain regions mediating reward sensitivity across adolescence. Cereb. Cortex [Epub ahead of print]. 19406906
  63. Watson D. Clark L. (1984). Negative affectivity: the disposition to experience aversive emotional states. Psychol. Bull. 96, 465– 490 10.1037/0033-2909.96.3.465 6393179 · DOI · Paper page
  64. Willis T. A. Vacarro D. McNamara G. (1994). Novelty seeking, risk taking, and related constructs as predictors of adolescence substance abuse: an application of Cloniger's theory. J. Subst. Abuse 6, 1– 20 10.1016/S0899-3289(94)90039-6 8081104 · DOI

Cited by

Sorted by citations

Authors
Galvan
Venue
Frontiers in Human Neuroscience
Publisher
Frontiers Media SA
Published
2010
Volume
4
Pages
6-6
ISSN
1662-5161 (ISSN-L)
DOI
10.3389/neuro.09.006.2010
PMC
PMC2826184
OpenAlex
W1992630689
Cited by
521
References
12
Citations by year
2026: 24 · 2025: 37 · 2024: 29 · 2023: 29 · 2022: 45 · 2021: 46 · 2020: 37 · 2019: 36 · 2018: 26 · 2017: 32 · 2016: 31 · 2015: 31 · 2014: 38 · 2013: 35 · 2012: 22
FWCI
15.32
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Human Neuroscience (publishedVersion, cc-by)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • eScholarship (California Digital Library) (submittedVersion)
  • PubMed
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 › Psychology › Clinical Psychology › Gambling Behavior and Treatments
Keywords
adolescent development, reward systems, striatum, reward-seeking behavior, reward processing

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