Adolescent impatience decreases with increased frontostriatal connectivity

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 29, 2015, Pages E3765-E3774

  Van Den Bos, Wouter ^a,b   Rodriguez, Christian A ^b   Schweitzer, Julie B ^c,d   McClure, Samuel M ^b  

^a MAX PLANCK INSTITUTE FOR HUMAN DEVELOPMENT   (Germany)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adolescence; Connectivity; Delay discounting; DTI; Impatience

Indexed keywords

ADOLESCENT; ADOLESCENT BEHAVIOR; ADULT; AMYGDALOID NUCLEUS; ARTICLE; BEHAVIOR CHANGE; CEREBELLUM; CHILD; CONNECTOME; CORPUS STRIATUM; DELAY DISCOUNTING; DIFFUSION TENSOR IMAGING; DORSOLATERAL PREFRONTAL CORTEX; EXECUTIVE FUNCTION; FEMALE; FRONTOSTRIATUM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; IMPATIENCE; IMPULSIVENESS; LATERAL PREFRONTAL CORTEX; MALE; MEDIAL ORBITOFRONTAL CORTEX; NORMAL HUMAN; PARIETAL CORTEX; PATIENCE; POSTERIOR CINGULATE; PRIORITY JOURNAL; REWARD; SUPPLEMENTARY MOTOR AREA; AGE; ANATOMY AND HISTOLOGY; DECISION MAKING; NEOSTRIATUM; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; TASK PERFORMANCE; YOUNG ADULT;

ADOLESCENT; ADULT; AGE FACTORS; CHILD; CHOICE BEHAVIOR; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; IMPULSIVE BEHAVIOR; MAGNETIC RESONANCE IMAGING; MALE; NEOSTRIATUM; NEURAL PATHWAYS; REWARD; TASK PERFORMANCE AND ANALYSIS; YOUNG ADULT;

EID: 84937501624     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1423095112     Document Type: Article

References (94)

1. Steinberg L, et al. (2009) Age differences in future orientation and delay discounting. Child Dev 80(1):28-44.
2. Spear LPP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24(4):417-463.
3. Spear LP (2013) Adolescent neurodevelopment. J Adolesc Health 52(2, Suppl 2):S7-S13.
4. Steinberg L (2007) Risk taking in adolescence: New perspectives from brain and behavioral science. Curr Dir Psychol Sci 16(2):55-59.
5. Eaton DK, et al.; Centers for Disease Control and Prevention (CDC) (2012) Youth risk behavior surveillance - United States, 2011. MMWR Surveill Summ 61(4):1-162.
6. Romer D (2010) Adolescent risk taking, impulsivity, and brain development: Implications for prevention. Dev Psychobiol 52(3):263-276.
7. Defoe IN, Dubas JS, Figner B, van Aken MA (2015) A meta-analysis on age differences in risky decision making: Adolescents versus children and adults. Psychol Bull 141(1):48-84.
8. Whelan R, et al.; IMAGEN Consortium (2012) Adolescent impulsivity phenotypes characterized by distinct brain networks. Nat Neurosci 15(6):920-925.
9. Robbins TW, Gillan CM, Smith DG, de Wit S, Ersche KD (2012) Neurocognitive endophenotypes of impulsivity and compulsivity: Towards dimensional psychiatry. Trends Cogn Sci 16(1):81-91.
10. Reynolds B, Fields S (2012) Delay discounting by adolescents experimenting with cigarette smoking. Addiction 107(2):417-424.
11. Reynolds B (2006) A review of delay-discounting research with humans: Relations to drug use and gambling. Behav Pharmacol 17(8):651-667.
12. Audrain-McGovern J, et al. (2009) Does delay discounting play an etiological role in smoking or is it a consequence of smoking? Drug Alcohol Depend 103(3):99-106.
13. Romer D, Duckworth AL, Sznitman S, Park S (2010) Can adolescents learn self-control? Delay of gratification in the development of control over risk taking. Prev Sci 11(3):319-330.
14. Duckworth AL, Seligman ME (2005) Self-discipline outdoes IQ in predicting academic performance of adolescents. Psychol Sci 16(12):939-944.
15. Madden GJ, Petry NM, Badger GJ, Bickel WK (1997) Impulsive and self-control choices in opioid-dependent patients and non-drug-using control participants: Drug and monetary rewards. Exp Clin Psychopharmacol 5(3):256-262.
16. Barkley RA, Edwards G, Laneri M, Fletcher K, Metevia L (2001) Executive functioning, temporal discounting, and sense of time in adolescents with attention deficit hyperactivity disorder (ADHD) and oppositional defiant disorder (ODD). J Abnorm Child Psychol 29(6):541-556.
17. Scheres A, Tontsch C, Thoeny AL, Kaczkurkin A (2010) Temporal reward discounting in attention-deficit/hyperactivity disorder: The contribution of symptom domains, reward magnitude, and session length. Biol Psychiatry 67(7):641-648.
18. van den Bos W, McClure SM (2013) Towards a general model of temporal discounting. J Exp Anal Behav 99(1):58-73.
19. Peters J, Büchel C (2011) The neural mechanisms of inter-temporal decision-making: Understanding variability. Trends Cogn Sci 15(5):227-239.
20. Kalenscher T, Pennartz CMA (2008) Is a bird in the hand worth two in the future? The neuroeconomics of intertemporal decision-making. Prog Neurobiol 84(3):284-315.
21. van den Bos W, Rodriguez CA, Schweitzer JB, McClure SM (2014) Connectivity strength of dissociable striatal tracts predict individual differences in temporal discounting. J Neurosci 34(31):10298-10310.
22. Loewenstein GF, Prelec D (1992) Anomalies in intertemporal choice: Evidence and an interpretation. Q J Econ 107(2):573-597.
23. Luo S, Ainslie G, Giragosian L, Monterosso JR (2009) Behavioral and neural evidence of incentive bias for immediate rewards relative to preference-matched delayed rewards. J Neurosci 29(47):14820-14827.
24. Figner B, et al. (2010) Lateral prefrontal cortex and self-control in intertemporal choice. Nat Neurosci 13(5):538-539.
25. Hutcherson CA, Plassmann H, Gross JJ, Rangel A (2012) Cognitive regulation during decision making shifts behavioral control between ventromedial and dorsolateral prefrontal value systems. J Neurosci 32(39):13543-13554.
26. Daniel TO, Stanton CM, Epstein LH (2013) The future is now: Comparing the effect of episodic future thinking on impulsivity in lean and obese individuals. Appetite 71:120-125.
27. Berns GS, Laibson DI, Loewenstein G (2007) Intertemporal choice - toward an integrative framework. Trends Cogn Sci 11(11):482-488.
28. Boyer P (2008) Evolutionary economics of mental time travel? Trends Cogn Sci 12(6):219-224.
29. Peters J, Büchel C (2010) Episodic future thinking reduces reward delay discounting through an enhancement of prefrontal-mediotemporal interactions. Neuron 66(1):138-148.
30. Benoit RG, Gilbert SJ, Burgess PW (2011) A neural mechanism mediating the impact of episodic prospection on farsighted decisions. J Neurosci 31(18):6771-6779.
31. Peper JS, et al. (2013) Delay discounting and frontostriatal fiber tracts: A combined DTI and MTR study on impulsive choices in healthy young adults. Cereb Cortex 23(7):1695-1702.
32. Casey BJ (2015) Beyond simple models of self-control to circuit-based accounts of adolescent behavior. Annu Rev Psychol 66:295-319.
33. Ernst M (2014) The triadic model perspective for the study of adolescent motivated behavior. Brain Cogn 89:104-111.
34. Galván A (2013) The teenage brain: Sensitivity to rewards. Curr Dir Psychol Sci 22(2):88-93.
35. Barkley-Levenson E, Galván A (2014) Neural representation of expected value in the adolescent brain. Proc Natl Acad Sci USA 111(4):1646-1651.
36. Lamm C, et al. (2014) Longitudinal study of striatal activation to reward and loss anticipation from mid-adolescence into late adolescence/early adulthood. Brain Cogn 89:51-60.
37. Bjork JM, Smith AR, Chen G, Hommer DW (2010) Adolescents, adults and rewards: Comparing motivational neurocircuitry recruitment using fMRI. PLoS One 5(7):e11440.
38. Bunge SA, Dudukovic NM, Thomason ME, Vaidya CJ, Gabrieli JDE (2002) Immature frontal lobe contributions to cognitive control in children: Evidence from fMRI. Neuron 33(2):301-311.
39. Ordaz SJ, Foran W, Velanova K, Luna B (2013) Longitudinal growth curves of brain function underlying inhibitory control through adolescence. J Neurosci 33(46):18109-18124.
40. Crone EA (2009) Executive functions in adolescence: Inferences from brain and behavior. Dev Sci 12(6):825-830.
41. Zimbardo PG, Boyd JN (1999) Putting time in perspective: A valid, reliable individual-differences metric. J Pers Soc Psychol 77(6):1271-1288.
42. Behrens TEJ, et al. (2003) Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6(7):750-757.
43. Draganski B, et al. (2008) Evidence for segregated and integrative connectivity patterns in the human basal ganglia. J Neurosci 28(28):7143-7152.
44. Tziortzi AC, et al. (2014) Connectivity-based functional analysis of dopamine release in the striatum using diffusion-weighted MRI and positron emission tomography. Cereb Cortex 24(5):1165-1177.
45. Cohen MX, Schoene-Bake J-C, Elger CE, Weber B (2009) Connectivity-based segregation of the human striatum predicts personality characteristics. Nat Neurosci 12(1):32-34.
46. Somerville LH, et al. (2013) The medial prefrontal cortex and the emergence of self-conscious emotion in adolescence. Psychol Sci 24(8):1554-1562.
47. Green L, Fry AF, Myerson J (1994) Discounting of delayed rewards. A life-span comparison. Psychol Sci 5(1):33-36.
48. Olson EA, Hooper CJ, Collins P, Luciana M (2007) Adolescents' performance on delay and probability discounting tasks: Contributions of age, intelligence, executive functioning, and self-reported externalizing behavior. Pers Individ Dif 43(7):1886-1897.
49. de Water E, Cillessen AHN, Scheres A (2014) Distinct age-related differences in temporal discounting and risk taking in adolescents and young adults. Child Dev 85(5):1881-1897.
50. Hayes A (2013) Introduction to Mediation, Moderation, and Conditional Process Analysis: A Regression-Based Approach. Methodology in the Social Sciences (The Guilford Press, New York).
51. Schel MA, Scheres A, Crone EA (2014) New perspectives on self-control development: Highlighting the role of intentional inhibition. Neuropsychologia 65:236-246.
52. Vink M, et al. (2014) Frontostriatal activity and connectivity increase during proactive inhibition across adolescence and early adulthood. Hum Brain Mapp 35(9):4415-4427.
53. Liston C, et al. (2006) Frontostriatal microstructure modulates efficient recruitment of cognitive control. Cereb Cortex 16(4):553-560.
54. Somerville LH, Casey BJ (2010) Developmental neurobiology of cognitive control and motivational systems. Curr Opin Neurobiol 20(2):236-241.
55. Giedd JN (2004) Structural magnetic resonance imaging of the adolescent brain. Ann N Y Acad Sci 1021:77-85.
56. Huttenlocher PR (1979) Synaptic density in human frontal cortex - developmental changes and effects of aging. Brain Res 163(2):195-205.
57. Jones DK, Knösche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: The do's and don'ts of diffusion MRI. Neuroimage 73(C):239-254.
58. Paus T (2010) Growth of white matter in the adolescent brain: Myelin or axon? Brain Cogn 72(1):26-35.
59. Friston KJ, Harrison L, Penny W (2003) Dynamic causal modelling. Neuroimage 19(4):1273-1302.
60. Christakou A, Brammer M, Rubia K (2011) Maturation of limbic corticostriatal activation and connectivity associated with developmental changes in temporal discounting. Neuroimage 54(2):1344-1354.
61. Olson EA, et al. (2009) White matter integrity predicts delay discounting behavior in 9- to 23-year-olds: A diffusion tensor imaging study. J Cogn Neurosci 21(7):1406-1421.
62. Somerville LH, Hare T, Casey BJ (2011) Frontostriatal maturation predicts cognitive control failure to appetitive cues in adolescents. J Cogn Neurosci 23(9):2123-2134.
63. Crone EA, Dahl RE (2012) Understanding adolescence as a period of social-affective engagement and goal flexibility. Nat Rev Neurosci 13(9):636-650.
64. van den Bos W (2013) Neural mechanisms of social reorientation across adolescence. J Neurosci 33(34):13581-13582.
65. Brien LO, et al. (2011) Adolescents prefer more immediate rewards when in the presence of their peers. J Res Adolesc 21(4):747-753.
66. Weigard A, Chein J, Albert D, Smith A, Steinberg L (2014) Effects of anonymous peer observation on adolescents' preference for immediate rewards. Dev Sci 17(1):71-78.
67. Albert D, Chein J, Steinberg L (2013) Peer influences on adolescent decision making. Curr Dir Psychol Sci 22(2):114-120.
68. Steinbeis N, Haushofer J, Fehr E, Singer T (2014) Development of behavioral control and associated vmPFC-DLPFC connectivity explains children's increased resistance to temptation in intertemporal choice. Cereb Cortex, 10.1093/cercor/bhu167.
69. Johnson MH (2011) Interactive specialization: A domain-general framework for human functional brain development? Dev Cogn Neurosci 1(1):7-21.
70. Haber SN, Knutson B (2010) The reward circuit: Linking primate anatomy and human imaging. Neuropsychopharmacology 35(1):4-26.
71. Voorn P, Vanderschuren LJMJ, Groenewegen HJ, Robbins TW, Pennartz CMA (2004) Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci 27(8):468-474.
72. Pfeifer JH, Allen NB (2012) Arrested development? Reconsidering dual-systems models of brain function in adolescence and disorders. Trends Cogn Sci 16(6):322-329.
73. Reyna VF, Brainerd CJ (2011) Dual processes in decision making and developmental neuroscience: A fuzzy-trace model. Dev Rev 31(2-3):180-206.
74. Chick CF, Reyna VF (2012) A fuzzy-trace theory of adolescent risk-taking: Beyond self-control and sensation seeking. The Adolescent Brain: Learning, Reasoning, and Decision Making, eds Reyna VF, Chapman SB, Dougherty MR, Confrey J (American Psychological Association, Washington, DC), pp 379-428.
75. Chapman SB, Gamino JF, Mudar RA (2012) Higher order strategic gist reasoning in adolescence. The Adolescent Brain: Learning, Reasoning, and Decision Making, eds Reyna VF, Chapman SB, Dougherty MR, Confrey J (American Psychological Association, Washington, DC), pp 123-151.
76. Todorov V, Filzmoser P (2009) An object-oriented framework for robust multivariate analysis. J Stat Softw 32(3):1-47.
77. Verbruggen F, Logan GD, Stevens MA (2008) STOP-IT: Windows executable software for the stop-signal paradigm. Behav Res Methods 40(2):479-483.
78. Bedard A-C, et al. (2002) The development of selective inhibitory control across the life span. Dev Neuropsychol 21(1):93-111.
79. Crosbie J, et al. (2013) Response inhibition and ADHD traits: Correlates and heritability in a community sample. J Abnorm Child Psychol 41(3):497-507.
80. Soreni N, Crosbie J, Ickowicz A, Schachar R (2009) Stop signal and Conners' continuous performance tasks: Test-retest reliability of two inhibition measures in ADHD children. J Atten Disord 13(2):137-143.
81. Brevers D, et al. (2012) Impulsive action but not impulsive choice determines problem gambling severity. PLoS One 7(11):e50647.
82. de Wit H (2009) Impulsivity as a determinant and consequence of drug use: A review of underlying processes. Addict Biol 14(1):22-31.
83. Berkman ET, Burklund L, Lieberman MD (2009) Inhibitory spillover: Intentional motor inhibition produces incidental limbic inhibition via right inferior frontal cortex. Neuroimage 47(2):705-712.
84. Berkman ET, Graham AM, Fisher PA (2012) Training self-control: A domain-general translational neuroscience approach. Child Dev Perspect 6(4):374-384.
85. Tabibnia G, et al. (2011) Different forms of self-control share a neurocognitive substrate. J Neurosci 31(13):4805-4810.
86. Nurmi J (1991) How do adolescents see their future? A review of the development of future orientation and planning. Dev Rev 11(1):1-59.
87. Furby L, Beyth-Marom R (1992) Risk taking in adolescence: A decision-making perspective. Dev Rev 12(1):1-44.
88. Raven JC (1941) Standardization of progressive matrices. Br J Med Psychol 19(1):137-150.
89. Peper JS, Dahl RE (2013) The teenage brain: Surging hormones - brain-behavior interactions during puberty. Curr Dir Psychol Sci 22(2):134-139.
90. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59(3):2142-2154.
91. Mazaika P, Hoeft F, Glover GH, Reiss AL (2009) Methods and Software for fMRI Analysis for Clinical Subjects. Human Brain Mapping. Available at cibsr.stanford.edu/tools/human-brain-project/artrepair-software.html. Accessed May 26, 2015.
92. Forstmann BU, et al. (2012) Cortico-subthalamic white matter tract strength predicts interindividual efficacy in stopping a motor response. Neuroimage 60(1):370-375.
93. Gitelman DR, Penny WD, Ashburner J, Friston KJ (2003) Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. Neuroimage 19(1):200-207.
94. Petersen AC, 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(2):117-133.