CoChat
Sign Up
Cited by 692Neural and Behavioral Psychology StudiesSubstance Abuse Treatment and OutcomesNeurotransmitter Receptor Influence on Behavior

Neurobiology of the Adolescent Brain and Behavior: Implications for Substance Use Disorders

Open access
Casey, B.J., Jones, Rebecca M.·2010·Journal of the American Academy of Child & Adolescent Psychiatry
DOI 10.1016/j.jaac.2010.08.017PMC PMC3099425
Open this paper in CoChat — free account

Abstract

Objective Adolescence is a developmental period that entails substantial changes in risk-taking behavior and experimentation with alcohol and drugs. Understanding how the brain is changing during this period relative to childhood and adulthood and how these changes vary across individuals are key in predicting risk for later substance abuse and dependence. Method This review discusses recent human imaging and animal work in the context of an emerging view of adolescence as characterized by a tension between early emerging "bottom-up" systems that express exaggerated reactivity to motivational stimuli and later maturing "top-down" cognitive control regions. Behavioral, clinical, and neurobiological evidences are reported for dissociating these two systems developmentally. The literature on the effects of alcohol and its rewarding properties in the brain is discussed in the context of these two systems. Results Collectively, these studies show curvilinear development of motivational behavior and the underlying subcortical brain regions, with a peak inflection from 13 to 17 years. In contrast, prefrontal regions, important in top-down regulation of behavior, show a linear pattern of development well into young adulthood that parallels that seen in behavioral studies of impulsivity. Conclusions The tension or imbalance between these developing systems during adolescence may lead to cognitive control processes being more vulnerable to incentive-based modulation and increased susceptibility to the motivational properties of alcohol and drugs. As such, behavior challenges that require cognitive control in the face of appetitive cues may serve as useful biobehavioral markers for predicting which teens may be at greater risk for alcohol and substance dependence.

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 · 10.1016/j.jaac.2010.08.017

Cites

32 of 32 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: 95

  1. [3]Casey BJ Jones RM Hare TA The adolescent brain Ann N Y Acad Sci 2008 Mar 1124 111 126 18400927 PMC2475802
  2. [4]Sowell ER Peterson BS Thompson PM Welcome SE Henkenius AL Toga AW Mapping cortical change across the human life span Nat Neurosci 2003 Mar 6 3 309 315 12548289
  3. [6]Galvan A Hare TA Parra CE Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents Journal of Neuroscience 2006 Jun 21 26 25 6885 6892 16793895 PMC6673830
  4. [7]Hare TA Tottenham N Galvan A Voss HU Glover GH Casey BJ Biological substrates of emotional reactivity and regulation in adolescence during an emotional go-nogo task Biol Psychiatry 2008 May 15 63 10 927 934 18452757 PMC2664095
  5. [8]Bourgeois JP Goldman-Rakic PS Rakic P Synaptogenesis in the prefrontal cortex of rhesus monkeys Cerebral Cortex 1994 4 78 96 8180493
  6. [9]Huttenlocher PR Synaptic density in human frontal cortex - developmental changes and effects of aging Brain Research 1979 163 195 205 427544
  7. [10]Rakic Pea Synaptic development of the cerebral cortex: implications for learning, memory and mental illness Prog. Brain Res 1994 102 227 243 7800815
  8. [11]Windle M Spear LP Fuligni AJ Transitions into underage and problem drinking: developmental processes and mechanisms between 10 and 15 years of age Pediatrics 2008 121 S273 S289 18381494 PMC2892675
  9. [12]Eaton LK Kann L Kinchen S Youth Risk Behavior Surveillance - United States, 2007, surveillance summaries Morbidity and Mortality Weekly Report 2008 57 SS04 1 131 18528314
  10. [13]Laviola G Adriani W Terranova ML Gerra G Psychobiological risk factors for vulnerability to psychostimulants in human adolescents and animal models Neurosci Biobehav Rev 1999 Nov 23 7 993 1010 10580313
  11. [14]Spear LP The adolescent brain and age-related behavioral manifestations Neuroscience and Biobehavioral Reviews 2000 24 4 417 463 10817843
  12. [17]Geier CF Terwilliger R Teslovich T Velanova K Luna B Immaturities in Reward Processing and Its Influence on Inhibitory Control in Adolescence Cereb Cortex 2009 Oct 29 PMC2882823 19875675
  13. [19]Van Leijenhorst L Zanolie K Van Meel CS Westenberg PM Rombouts SA Crone EA What motivates the adolescent? Brain regions mediating reward sensitivity across adolescence Cereb Cortex 2010 Jan 20 1 61 69 19406906
  14. [20]Somerville LH Hare TA Casey BJ Frontostriatal maturation predicts behavioral regulation failures to appetitive cues in adolescence Journal of Cognitive Neuroscience In Press PMC3131482 20809855
  15. [22]Ernst M Romeo RD Andersen SL Neurobiology of the development of motivated behaviors in adolescence: a window into a neural systems model Pharmacol Biochem Behav 2009 Sep 93 3 199 211 19136024
  16. [23]Steinberg L A social neuroscience perspective on adolescent risk-taking Developmental Review 2008 28 78 106 18509515 PMC2396566
  17. [26]Levita L Hare TA Voss HU Glover G Ballon DJ Casey BJ The bivalent side of the nucleus accumbens Neuroimage 2009 Feb 1 44 3 1178 1187 18976715 PMC2659952
  18. [29]Eigsti IM Zayas V Mischel W Predicting cognitive control from preschool to late adolescence and young adulthood Psychol Sci 2006 Jun 17 6 478 484 16771797
  19. [31]Evenden JL Varieties of impulsivity Psychopharmacology (Berl) 1999 Oct 146 4 348 361 10550486
  20. [33]Davidson MC Amso D Anderson LC Diamond A Development of cognitive control and executive functions from 4 to 13 years: evidence from manipulations of memory, inhibition, and task switching Neuropsychologia 2006 44 11 2037 2078 16580701 PMC1513793
  21. [36]Jazbec S Hardin MG Schroth E McClure E Pine DS Ernst M Age-related influence of contingencies on a saccade task Exp Brain Res 2006 Oct 174 4 754 762 16733706 PMC2733163
  22. [39]Crone EA van der Molen MW Developmental changes in real life decision making: performance on a gambling task previously shown to depend on the ventromedial prefrontal cortex Dev Neuropsychol 2004 25 3 251 279 15147999
  23. [42]Steinberg L Albert D Cauffman E Banich M Graham S Woolard J Age differences in sensation seeking and impulsivity as indexed by behavior and self-report: evidence for a dual systems model Dev Psychol 2008 Nov 44 6 1764 1778 18999337
  24. [43]Casey BJ Giedd JN Thomas KM Structural and functional brain development and its relation to cognitive development Biol Psychol 2000 Oct 54 1–3 241 257 11035225
  25. [44]Delgado MR Reward-related responses in the human striatum Ann N Y Acad Sci 2007 May 1104 70 88 17344522
  26. [45]Pasupathy A Miller EK Different time courses of learning-related activity in the prefrontal cortex and striatum Nature 2005 Feb 24 433 7028 873 876 15729344
  27. [47]Cardinal RN Pennicott DR Sugathapala CL Robbins TW Everitt BJ Impulsive choice induced in rats by lesions of the nucleus accumbens core Science 2001 Jun 29 292 5526 2499 2501 11375482
  28. [48]Gill TM Castaneda PJ Janak PH Dissociable Roles of the Medial Prefrontal Cortex and Nucleus Accumbens Core in Goal-Directed Actions for Differential Reward Magnitude Cereb Cortex 2010 Apr 1 20308201
  29. [49]Galvan A Hare TA Davidson M Spicer J Glover G Casey BJ The role of ventral frontostriatal circuitry in reward-based learning in humans J Neurosci 2005 Sep 21 25 38 8650 8656 16177032 PMC6725514
  30. [50]Brenhouse HC Sonntag KC Andersen SL Transient D1 dopamine receptor expression on prefrontal cortex projection neurons: relationship to enhanced motivational salience of drug cues in adolescence J Neurosci 2008 Mar 5 28 10 2375 2382 18322084 PMC4028226
  31. [51]Benes FM Taylor JB Cunningham MC Convergence and plasticity of monoaminergic systems in the medial prefrontal cortex during the postnatal period: implications for the development of psychopathology Cereb Cortex 2000 Oct 10 10 1014 1027 11007552
  32. [52]Cunningham MG Bhattacharyya S Benes FM Increasing Interaction of amygdalar afferents with GABAergic interneurons between birth and adulthood Cereb Cortex 2008 Jul 18 7 1529 1535 17971342
  33. [53]Tseng KY O'Donnell P Dopamine modulation of prefrontal cortical interneurons changes during adolescence Cereb Cortex 2007 May 17 5 1235 1240 16818475 PMC2204087
  34. [54]Seeman P Bzowej NH Guan HC Human brain dopamine receptors in children and aging adults Synapse 1987 1 5 399 404 3505371
  35. [56]Teicher MH Krenzel E Thompson AP Andersen SL Dopamine receptor pruning during the peripubertal period is not attenuated by NMDA receptor antagonism in rat Neurosci Lett 2003 Mar 20 339 2 169 171 12614921
  36. [57]Andersen SL Thompson AT Rutstein M Hostetter JC Teicher MH Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats Synapse 2000 Aug 37 2 167 169 10881038
  37. [59]Fonseca Rd Ramos JA Bonnin A Fernandez-Ruiz JJ Presence of cannabinoid binding sites in the brain from early postnatal ages NeuroReport 1993 4 2 135 138 8453049
  38. [61]Robinson TE Berridge KC The neural basis of drug craving: an incentive-sensitization theory of addiction Brain Res Brain Res Rev 1993 Sep-Dec 18 3 247 291 8401595
  39. [62]Volkow ND Swanson JM Variables that affect the clinical use and abuse of methylphenidate in the treatment of ADHD Am J Psychiatry 2003 Nov 160 11 1909 1918 14594733
  40. [63]Robinson TE Berridge KC Addiction Annu Rev Psychol 2003 54 25 53 12185211
  41. [65]Forbes EE Ryan ND Phillips ML Healthy adolescents' neural response to reward: associations with puberty, positive affect, and depressive symptoms J Am Acad Child Adolesc Psychiatry 2010 Feb 49 2 162 172 e161 e165 20215938 PMC2837556
  42. [66]Romeo RD Puberty: a period of both organizational and activational effects of steroid hormones on neurobehavioural development J Neuroendocrinol 2003 Dec 15 12 1185 1192 14636181
  43. [67]Forbes EE Dahl RE Pubertal development and behavior: hormonal activation of social and motivational tendencies Brain Cogn 2010 Feb 72 1 66 72 19942334 PMC3955709
  44. [70]Asato MR Terwilliger R Woo J Luna B White Matter Development in Adolescence: A DTI Study Cereb Cortex 2010 Jan 5 PMC2923214 20051363
  45. [72]Luna B Padmanabhan A O'Hearn K What has fMRI told us about the development of cognitive control through adolescence Brain and Cognition 2010 PMC2815087 19765880
  46. [73]Astle DE Scerif G Using developmental cognitive neuroscience to study behavioral and attentional control Developmental Psychobiology 2009 51 2 107 118 18973175
  47. [74]Luna B Thulborn KR Munoz DP Maturation of widely distributed brain function subserves cognitive development Neuroimage 2001 May 13 5 786 793 11304075
  48. [76]Bitan T Burman DD Lu D Weaker top-down modulation from the left inferior frontal gyrus in children Neuroimage 2006 33 991 998 16978881 PMC2615533
  49. [77]Tamm L Menon V Reiss AL Maturation of brain function associated with response inhibition J Am Acad Child Adolesc Psychiatry 2002 Oct 41 10 1231 1238 12364845
  50. [78]Stevens MC Skudlarski P Pearlson GD Calhoun VD Age-related cognitive gains are mediated by the effects of white matter development on brain network integration Neuroimage 2009 Dec 48 4 738 746 19577651 PMC2753497
  51. [79]Giedd JN Blumenthal J Jeffries NO Brain development during childhood and adolescence: a longitudinal MRI study Nat Neurosci 1999 Oct 2 10 861 863 10491603
  52. [80]Huttenlocher PR Morphometric study of human cerebral cortex development Neuropsychologia 1990 28 6 517 527 2203993
  53. [81]Casey BJ Thomas KM Davidson MC Kunz K Franzen PL Dissociating striatal and hippocampal function developmentally with a stimulus-response compatibility task The Journal of Neuroscience 2002 22 19 8647 8652 12351738 PMC6757769
  54. [83]Delgado MR Nystrom LE Fissell C Noll DC Fiez JA Tracking the hemodynamic responses to reward and punishment in the striatum Journal of Neurophysiology 2000 Dec 84 6 3072 3077 11110834
  55. [84]Kuhnen CM Knutson B The neural basis of financial risk taking Neuron 2005 Sep 1 47 5 763 770 16129404
  56. [85]Matthews SC Simmons AN Lane SD Paulus MP Selective activation of the nucleus accumbens during risk-taking decision making Neuroreport 2004 Sep 15 15 13 2123 2127 15486494
  57. [86]Casey BJ Galvan A Hare TA Changes in cerebral functional organization during cognitive development Current Opinion in Neurobiology 2005 Apr 15 2 239 244 15831409
  58. [87]Boes AD Bechara A Tranel D Anderson SW Richman L Nopoulos P Right ventromedial prefrontal cortex: a neuroanatomical correlate of impulse control in boys Soc Cogn Affect Neurosci 2009 Mar 4 1 1 9 19015086 PMC2656876
  59. [88]Vaidya CJ Austin G Kirkorian G Selective effects of methylphenidate in attention deficit hyperactivity disorder: a functional magnetic resonance study Proc Natl Acad Sci U S A 1998 Nov 24 95 24 14494 14499 9826728 PMC24401
  60. [90]Scheres A Milham MP Knutson B Castellanos FX Ventral striatal hyporesponsiveness during reward anticipation in attention-deficit/hyperactivity disorder Biol Psychiatry 2007 Mar 1 61 5 720 724 16950228
  61. [91]Bjork JM Knutson B Hommer DW Incentive-elicited striatal activation in adolescent children of alcoholics Addiction 2008 Aug 103 8 1308 1319 18851716
  62. [92]Hardin MG Ernst M Functional brain imaging of development-related risk and vulnerability for substance use in adolescents J Addict Med 2009 Jun 1 3 2 47 54 20161036 PMC2753522
  63. [94]Witt ED Research on alcohol and adolescent brain development: opportunities and future directions Alcohol 2010 Feb 44 1 119 124 20113880
  64. [95]Grant BF Dawson DA Age at onset of alcohol use and its association with DSM-IV alcohol abuse and dependence: results from the National Longitudinal Alcohol Epidemiologic Survey J Subst Abuse 1997 9 103 110 9494942
  65. [96]Li TK Hewitt BG Grant BF Is there a future for quantifying drinking in the diagnosis, treatment, and prevention of alcohol use disorders? Alcohol Alcohol 2007 Mar-Apr 42 2 57 63 17307789
  66. [97]Volkow ND Fowler JS Wang GJ Goldstein RZ Role of dopamine, the frontal cortex and memory circuits in drug addiction: insight from imaging studies Neurobiol Learn Mem 2002 Nov 78 3 610 624 12559839
  67. [98]Maldonado R Rodriguez de Fonseca F Cannabinoid addiction: behavioral models and neural correlates J Neurosci 2002 May 1 22 9 3326 3331 11978807 PMC6758395
  68. [99]French ED Dillon K Wu X Cannabinoids excite dopamine neurons in the ventral tegmentum and substantia nigra Neuroreport 1997 Feb 10 8 3 649 652 9106740
  69. [100]Robinson TE Berridge KC The incentive sensitization theory of addiction: some current issues Philos Trans R Soc Lond B Biol Sci 2008 Oct 12 363 1507 3137 3146 Review 18640920 PMC2607325
  70. [101]Doremus TL Brunell SC Varlinskaya EI Spear LP Anxiogenic effects during withdrawal from acute ethanol in adolescent and adult rats Pharmacol Biochem Behav 2003 May 75 2 411 418 12873633
  71. [102]Spear LP Varlinskaya EI Adolescence. Alcohol sensitivity, tolerance, and intake Recent Dev Alcohol 2005 17 143 159 15789864
  72. [103]Pautassi RM Myers M Spear LP Molina JC Spear NE Adolescent but not adult rats exhibit ethanol-mediated appetitive second-order conditioning Alcohol Clin Exp Res 2008 Nov 32 11 2016 2027 18782343 PMC2588482
  73. [104]Varlinskaya EI Spear LP Acute effects of ethanol on social behavior of adolescent and adult rats: role of familiarity of the test situation Alcohol Clin Exp Res 2002 Oct 26 10 1502 1511 12394283
  74. [105]White AM Swartzwelder HS Age-related effects of alcohol on memory and memory-related brain function in adolescents and adults Recent Dev Alcohol 2005 17 161 176 15789865
  75. [106]Sircar R Basak AK Sircar D Repeated ethanol exposure affects the acquisition of spatial memory in adolescent female rats Behav Brain Res 2009 Sep 14 202 2 225 231 19463705 PMC2694351
  76. [107]Sircar R Sircar D Adolescent rats exposed to repeated ethanol treatment show lingering behavioral impairments Alcohol Clin Exp Res 2005 Aug 29 8 1402 1410 16131847
  77. [108]Carpenter-Hyland EP Chandler LJ Adaptive plasticity of NMDA receptors and dendritic spines: implications for enhanced vulnerability of the adolescent brain to alcohol addiction Pharmacol Biochem Behav 2007 Feb 86 2 200 208 17291572 PMC2662130
  78. [109]De Bellis MD Clark DB Beers SR Hippocampal volume in adolescent-onset alcohol use disorders Am J Psychiatry 2000 May 157 5 737 744 10784466
  79. [110]Nagel BJ Schweinsburg AD Phan V Tapert SF Reduced hippocampal volume among adolescents with alcohol use disorders without psychiatric comorbidity Psychiatry Res 2005 Aug 30 139 3 181 190 16054344 PMC2270700
  80. [111]Brown SA Tapert SF Adolescence and the trajectory of alcohol use: basic to clinical studies Ann N Y Acad Sci 2004 Jun 1021 234 244 15251893
  81. [112]Medina KL McQueeny T Nagel BJ Hanson KL Schweinsburg AD Tapert SF Prefrontal cortex volumes in adolescents with alcohol use disorders: unique gender effects Alcohol Clin Exp Res 2008 Mar 32 3 386 394 18302722 PMC2825148
  82. [114]Tapert SF Cheung EH Brown GG Neural response to alcohol stimuli in adolescents with alcohol use disorder Arch Gen Psychiatry 2003 Jul 60 7 727 735 12860777
  83. [115]Pulido C Brown SA Cummins K Paulus MP Tapert SF Alcohol cue reactivity task development Addict Behav 2010 Feb 35 2 84 90 19800172 PMC2783802
  84. [117]Schweinsburg AD Paulus MP Barlett VC An FMRI study of response inhibition in youths with a family history of alcoholism Ann N Y Acad Sci 2004 Jun 1021 391 394 15251915
  85. [118]Deckel AW Hesselbrock V Behavioral and cognitive measurements predict scores on the MAST: a 3-year prospective study Alcohol Clin Exp Res 1996 Oct 20 7 1173 1178 8904966
  86. [119]Tarter RE Kirisci L Mezzich A Neurobehavioral disinhibition in childhood predicts early age at onset of substance use disorder Am J Psychiatry 2003 Jun 160 6 1078 1085 12777265
  87. [120]Behar D Berg CJ Rapoport JL Behavioral and physiological effects of ethanol in high-risk and control children: a pilot study Alcohol Clin Exp Res 1983 Fall 7 4 404 410 6318590
  88. [121]Dahl RE Affect regulation, brain development, and behavioral/emotional health in adolescence CNS Spectr 2001 Jan 6 1 60 72 17008832
  89. [122]Chambers RA Taylor JR Potenza MN Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability American Journal of Psychiatry 2003 Jun 160 6 1041 1052 12777258 PMC2919168
  90. [123]Nelson EE Leibenluft E McClure EB Pine DS The social re-orientation of adolescence: a neuroscience perspective on the process and its relation to psychopathology Psychol Med 2005 Feb 35 2 163 174 15841674
  91. [124]Mannuzza S Klein RG Long-term prognosis in attention-deficit/hyperactivity disorder Child Adolesc Psychiatr Clin N Am 2000 Jul 9 3 711 726 10944664
  92. [125]Mischel W Underwood B Instrumental ideation in delay of gratification Child Dev 1974 Dec 45 4 1083 1088 4143856
  93. [126]Ayduk O Mendoza-Denton R Mischel W Downey G Peake PK Rodriguez M Regulating the interpersonal self: strategic self-regulation for coping with rejection sensitivity J Pers Soc Psychol 2000 Nov 79 5 776 792 11079241
  94. [127]Tripodi SJ Bender K Litschge C Vaughn MG Interventions for reducing adolescent alcohol abuse: a meta-analytic review Arch Pediatr Adolesc Med 2010 Jan 164 1 85 91 20048247
  95. [128]Somerville LH Casey B Developmental neurobiology of cognitive control and motivational systems Curr Opin Neurobiol 2010 Feb 16 PMC3014528 20167473

Cited by

Sorted by citations

Authors
Casey, B. J., & Jones, R. M.
Affiliations
  • Weill Cornell Medicine (US)
  • Cornell University (US)
Corresponding author
Casey, B.J.
ORCID
Venue
Journal of the American Academy of Child & Adolescent Psychiatry
Publisher
Elsevier BV
Published
2010-12
Volume
49
Issue
12
Pages
1189-1201
ISSN
0890-8567 (ISSN-L)
DOI
10.1016/j.jaac.2010.08.017
PMC
PMC3099425
OpenAlex
W2011786285
Cited by
692
References
32
Citations by year
2026: 29 · 2025: 42 · 2024: 42 · 2023: 35 · 2022: 48 · 2021: 60 · 2020: 59 · 2019: 46 · 2018: 48 · 2017: 42 · 2016: 53 · 2015: 47 · 2014: 46 · 2013: 50 · 2012: 34
FWCI
2.21
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Journal of the American Academy of Child & Adolescent Psychiatry (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute on Drug Abuse (R01DA018879, DA007274, T32DA007274)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Health Sciences › Medicine › Epidemiology › Substance Abuse Treatment and Outcomes
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords
adolescent brain development, substance use disorders, cognitive control, top-down control, prefrontal cortex maturation, impulsivity, alcohol reward, risk prediction
MeSH terms
Adolescent, Alcohol Drinking, Arousal, Brain, Brain Mapping, Child, Humans, Impulsive Behavior, Motivation, Risk-Taking, Prefrontal Cortex, Substance-Related Disorders, 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