Frontostriatal maturation predicts cognitive control failure to appetitive cues in adolescents.
Adolescent risk-taking is a public health issue that increases the odds of poor lifetime outcomes. One factor thought to influence adolescents' propensity for risk-taking is an enhanced sensitivity to appetitive cues, relative to an immature capacity to exert sufficient cognitive control. We tested this hypothesis by characterizing interactions among ventral striatal, dorsal striatal, and prefrontal cortical regions with varying appetitive load using fMRI scanning. Child, teen, and adult participants performed a go/no-go task with appetitive (happy faces) and neutral cues (calm faces). Impulse control to neutral cues showed linear improvement with age, whereas teens showed a nonlinear reduction in impulse control to appetitive cues. This performance decrement in teens was paralleled by enhanced activity in the ventral striatum. Prefrontal cortical recruitment correlated with overall accuracy and showed a linear response with age for no-go versus go trials. Connectivity analyses identified a ventral frontostriatal circuit including the inferior frontal gyrus and dorsal striatum during no-go versus go trials. Examining recruitment developmentally showed that teens had greater between-subject ventral-dorsal striatal coactivation relative to children and adults for happy no-go versus go trials. These findings implicate exaggerated ventral striatal representation of appetitive cues in adolescents relative to an intermediary cognitive control response. Connectivity and coactivity data suggest these systems communicate at the level of the dorsal striatum differentially across development. Biased responding in this system is one possible mechanism underlying heightened risk-taking during adolescence.
Somerville
Leah H
LH
Sackler Institute for Developmental Psychobiology, Weill Cornell Medical College, 1300 York Avenue, Box 140, New York, NY 10065, USA. lhs2003@med.cornell.edu
Hare
Todd
T
Casey
B J
BJ
D000293:Adolescent; D000328:Adult; D000704:Analysis of Variance; D001066:Appetite; D001931:Brain Mapping; D002648:Child; D003072:Cognition Disorders / Q000175:diagnosis*; D003342:Corpus Striatum / Q000098:blood supply / Q000254:growth & development*; D003463:Cues; D004644:Emotions / Q000502:physiology; D005260:Female; D006801:Humans; D007091:Image Processing, Computer-Assisted; D007266:Inhibition, Psychological; D008279:Magnetic Resonance Imaging / Q000379:methods; D008297:Male; D009434:Neural Pathways / Q000098:blood supply / Q000254:growth & development; D009483:Neuropsychological Tests; D010100:Oxygen / Q000097:blood; D010775:Photic Stimulation / Q000379:methods; D011237:Predictive Value of Tests; D017397:Prefrontal Cortex / Q000098:blood supply / Q000254:growth & development*; D011930:Reaction Time; D055815:Young Adult
D010100:Oxygen
J Neurosci. 2006 Aug 9;26(32):8368-76
16899732
Proc Natl Acad Sci U S A. 2006 Jun 13;103(24):9315-20
16738055
Psychiatry Res. 2009 Aug 15;168(3):242-9
19564050
Ann N Y Acad Sci. 2008 Mar;1124:111-26
18400927
Biol Psychiatry. 2008 May 15;63(10):927-34
18452757
J Cogn Neurosci. 2002 Jan 1;14(1):1-10
11798382
Neuroimage. 2002 Jun;16(2):449-53
12030830
J Cogn Neurosci. 2006 Dec;18(12):1973-83
17129185
Brain Cogn. 2010 Feb;72(1):66-72
19942334
Neuroimage. 2005 May 1;25(4):1112-23
15850729
Neuroimage. 2001 May;13(5):786-93
11304075
Neuropsychopharmacology. 2010 Jan;35(1):4-26
19812543
Neuroimage. 2007 Jan 1;34(1):455-61
17049884
J Am Acad Child Adolesc Psychiatry. 2002 Dec;41(12):1495-502
12447037
Magn Reson Med. 2004 Apr;51(4):863-8
15065263
Neuron. 2002 Jan 17;33(2):301-11
11804576
Neurosci Biobehav Rev. 2000 Jun;24(4):417-63
10817843
Cereb Cortex. 2000 Mar;10(3):272-84
10731222
MMWR Surveill Summ. 2008 Jun 6;57(4):1-131
18528314
J Exp Psychol Learn Mem Cogn. 2009 May;35(3):709-30
19379045
Biol Psychiatry. 2005 Mar 15;57(6):624-32
15780849
Ann N Y Acad Sci. 2004 Jun;1021:1-22
15251869
Brain Res. 2001 Jan 19;889(1-2):71-7
11166688
J Child Psychol Psychiatry. 2009 Dec;50(12):1550-8
19573033
Nature. 2005 Feb 24;433(7028):873-6
15729344
Nat Neurosci. 2004 Oct;7(10):1040-7
15452575
Psychol Med. 2005 Feb;35(2):163-74
15841674
Dev Rev. 2008 Mar;28(1):78-106
18509515
J Am Acad Child Adolesc Psychiatry. 1997 Mar;36(3):374-83
9055518
Nat Rev Neurosci. 2004 Jun;5(6):483-94
15152198
Curr Opin Neurobiol. 2010 Apr;20(2):236-41
20167473
Ann N Y Acad Sci. 2004 Jun;1021:296-309
15251900
Cereb Cortex. 2010 Jul;20(7):1613-29
19875675
Nat Neurosci. 1999 Oct;2(10):861-3
10491603
Neuropsychology. 1999 Oct;13(4):564-74
10527065
Hum Brain Mapp. 2006 Dec;27(12):973-93
16683265
Neuroimage. 1997 Oct;6(3):218-29
9344826
J Neurosci. 1996 May 1;16(9):3112-22
8622141
Brain Cogn. 2010 Feb;72(1):101-13
19765880
Trends Neurosci. 1990 Jul;13(7):266-71
1695401
Cereb Cortex. 2008 Nov;18(11):2505-22
18281300
Psychol Med. 2006 Mar;36(3):299-312
16472412
Neuroimage. 2003 Dec;20(4):2135-41
14683717
Curr Opin Neurobiol. 2007 Apr;17(2):251-7
17383865
Comput Biomed Res. 1996 Jun;29(3):162-73
8812068
J Neurosci. 2006 Jun 21;26(25):6885-92
16793895
Curr Opin Neurobiol. 2007 Apr;17(2):243-50
17321127
Proc Natl Acad Sci U S A. 2000 Jul 18;97(15):8728-33
10900023
Cereb Cortex. 2010 Jan;20(1):61-9
19406906
Annu Rev Neurosci. 2001;24:167-202
11283309
J Child Psychol Psychiatry. 2007 Sep;48(9):899-913
17714375
Dev Psychol. 2010 Jan;46(1):193-207
20053017
J Child Psychol Psychiatry. 2004 Oct;45(7):1185-98
15335339
Biol Psychiatry. 2001 Feb 15;49(4):309-16
11239901
Proc Natl Acad Sci U S A. 1998 Nov 24;95(24):14494-9
9826728
Am J Psychiatry. 2007 Nov;164(11):1729-36
17974939
Dev Psychobiol. 2002 Apr;40(3):237-54
11891636
Hum Brain Mapp. 2010 Jun;31(6):926-33
20496383
Neuroimage. 2003 May;19(1):200-7
12781739
Neuroimage. 2005 May 1;25(4):1279-91
15850746
Dev Rev. 2008;28(1):62-77
18688292
Ann N Y Acad Sci. 2004 Jun;1021:51-8
15251873
Nature. 1996 Jul 18;382(6588):255-7
8717040
Cereb Cortex. 2004 Sep;14(9):1022-30
15115748
J Neurosci. 2007 Aug 1;27(31):8161-5
17670959
J Neurosci. 2005 Sep 21;25(38):8650-6
16177032
Biol Psychiatry. 2003 May 15;53(10):871-8
12742674
Neuroimage. 2007 Jan 15;34(2):565-74
17126038
Dev Sci. 2006 Jan;9(1):1-8
16445387