The role of the anterior insula in adolescent decision making

Developmental Neuroscience

Volumn 36, Issue 3-4, 2014, Pages 196-209

  Smith, Ashley R ^a   Steinberg, Laurence ^a   Chein, Jason ^a  

^a TEMPLE UNIVERSITY   (United States)

Author keywords

Adolescence; Anterior insula; Neural development; Risky decision making

Indexed keywords

ADOLESCENCE; ADOLESCENT; ADULTHOOD; ANTERIOR INSULA; ANTICIPATION; AROUSAL; AUTOREGULATION; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN MATURATION; BRAIN REGION; DECISION MAKING; DIFFUSION TENSOR IMAGING; EMOTIONALITY; EXECUTIVE FUNCTION; FUNCTIONAL NEUROIMAGING; HIGH RISK BEHAVIOR; HUMAN; IMPULSIVENESS; NERVE CELL NETWORK; NEUROIMAGING; PRIORITY JOURNAL; PSYCHOLOGICAL THEORY; REVIEW; REWARD; SENSATION; SOMATOSENSORY CORTEX; NERVE CELL DIFFERENTIATION; NEUROBIOLOGY; THEORY; ADOLESCENT BEHAVIOR; BRAIN CORTEX; PHYSIOLOGY;

ADOLESCENT; ADOLESCENT BEHAVIOR; CEREBRAL CORTEX; DECISION MAKING; HUMANS; REWARD; RISK-TAKING;

EID: 84906936372     PISSN: 03785866     EISSN: 14219859     Source Type: Journal    
DOI: 10.1159/000358918     Document Type: Review

References (118)

1. Church JA, Petersen SE, Schlaggar BL: The 'Task B problem' and other considerations in developmental functional neuroimaging. Hum Brain Mapp 2010; 31: 852-862.
2. Piquero AR: Taking stock of developmental trajectories of criminal activity over the life course; in Liberman A (ed): The Long View of Crime: A Synthesis of Longitudinal Research. New York, Springer, 2008, pp 23-78.
3. Harris JJ, Reynell C, Attwell D: The physiology of developmental changes in BOLD functional imaging signals. Dev Cogn Neurosci 2011; 1: 199-216.
4. Twisk DAM, Stacey C: Trends in young driver risk and countermeasures in European countries. J Safety Res 2007; 38: 245-257.
5. CDC: Your Risk Surveillance Survey - United States, 2011 (ed 61). Washington, CDC, 2012.
6. SAMHSA: Results from the 2010 National Survey on Drug Use and Health: Mental Health Findings (ed 42). Rockville, Substance Abuse and Mental Health Services Administration, 2012.
7. Cole MW, Schneider W: The cognitive control network: Integrated cortical regions with dissociable functions. Neuroimage 2007; 37: 343-360.
8. Naqvi NH, Bechara A: The hidden island of addiction: The insula. Trends Neurosci 2009; 32: 56-67.
9. Garavan H: Insula and drug cravings. Brain Struct Funct 2010; 214: 593-601.
10. Menon V, Uddin LQ: Saliency, switching, attention and control: A network model of insula function. Brain Struct Funct 2010; 214: 655-667.
11. Dahl RE: Adolescent brain development: A period of vulnerabilities and opportunities. Ann NY Acad Sci 2004; 1021: 1-22.
12. Sisk CL, Zehr JL: Pubertal hormones organize the adolescent brain and behavior. Front Neuroendocrinol 2005; 26: 163-174.
13. Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijenbos A, et al: Brain development during childhood and adolescence: A longitudinal MRI study. Nat Neurosci 1999; 2: 861-863.
14. Casey BJ, Getz S, Galvan A: The adolescent brain. Dev Rev 2008; 28: 62-77.
15. Ernst M, Pine DS, Hardin M: Triadic model of the neurobiology of motivated behavior in adolescence. Psychol Med 2006; 36: 299-312.
16. Reyna VF, Farley F: Risk and rationality in adolescent decision making. Psychol Sci Public Interest 2006; 7: 1-46.
17. Steinberg L: A social neuroscience perspective on adolescent risk-taking. Dev Rev 2008; 28: 78-106.
18. Crone EA, Dahl RE: Understanding adolescence as a period of social-Affective engagement and goal flexibility. Nat Rev Neurosci 2012; 13: 636-650.
19. Pfeifer JH, Allen NB: Arrested development?. Reconsidering dual-systems models of brain function in adolescence and disorders. Trends Cogn Sci 2012; 16: 322-329.
20. Zuckerman M: Behavioral Expressions and Biosocial Bases of Sensation Seeking. New York, Cambridge University Press, 1994.
21. Smith AR, Chein J, Steinberg L: Impact of socio-emotional context, brain development, and pubertal maturation on adolescent risk-taking. Horm Behav 2013; 64: 323-332.
22. Luna B, Padmanabhan A, O'Hearn K: What has fmri told us about the development of cognitive control through adolescence?. Brain Cogn 2010; 72: 101-113.
23. Galvan A: Adolescent development of the reward system. Front Hum Neurosci 2010; 4: 1-9.
24. Luciana M, Wahlstrom D, Porter JN, Collins PF: Dopaminergic modulation of incentive motivation in adolescence: Age-related changes in signaling, individual differences, and implications for the development of self-regulation. Dev Psychol 2012; 48: 844-861.
25. Steinberg L: A dual systems model of adolescent risk-taking. Dev Psychobiol 2010; 52: 216-224.
26. Richards JM, Plate RC, Ernst M: A systematic review of fmri reward paradigms used in studies of adolescents vs. adults: The impact of task design and implications for understanding neurodevelopment. Neurosurgery 2013; 37: 976-991.
27. Cho YT, Fromm S, Guyer AE, Detloff A, Pine DS, Fudge JL, et al: Nucleus accumbens, thalamus and insula connectivity during incentive anticipation in typical adults and adolescents. Neuroimage 2013; 66: 508-521.
28. Churchwell JC, Yurgelun-Todd DA: Age-related changes in insula cortical thickness and impulsivity: Significance for emotional development and decision-making. Dev Cogn Neurosci 2013; 6: 80-86.
29. Bartels A, Zeki S: The neural correlates of maternal and romantic love. Neuroimage 2004; 21: 1155-1166.
30. Ackermann H, Riecker A: The contribution of the insula to motor aspects of speech production: A review and a hypothesis. Brain Lang 2004; 89: 320-328.
31. Masten CL, Eisenberger NI, Borofsky LA, Pfeifer JH, McNealy K, Mazziotta JC, et al: Neural correlates of social exclusion during adolescence: Understanding the distress of peer rejection. Soc Cogn Affect Neurosci 2009; 4: 143-157.
32. Craig A: How do you feel - now?. The anterior insula and human awareness. Nat Rev Neurosci 2009; 10: 59-70.
33. Ture U, Yasargil D, Al-Mefty O, Yasargil MG: Topographic anatomy of the insular region. J Neurosurg 1999; 90: 720-733.
34. Augustine JR: Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Rev 1996; 22: 229-244.
35. Mesulam MM, Mufson EJ: Insula of the old world monkey. III. Efferent cortical output and comments on function. J Comp Neurol 1982; 212: 38-52.
36. Mufson EJ, Mesulam MM: Insula of the old world monkey. II. Afferent cortical input and comments on the claustrum. J Comp Neurol 1982; 212: 23-37.
37. Critchley HD: Neural mechanisms of autonomic, affective, and cognitive integration. J Comp Neurol 2005; 493: 154-166.
38. Critchley HD, Elliott R, Mathias CJ, Dolan RJ: Neural activity relating to generation and representation of Galvanic skin conductance responses: A functional magnetic resonance imaging study. J Neurosci 2000; 20: 3033-3040.
39. Critchley HD, Wiens S, Rotshtein P, Öhman A, Dolan RJ: Neural systems supporting interoceptive awareness. Nat Neurosci 2004; 7: 189-195.
40. Damasio AR, Grabowski TJ, Bechara A, Damasio H, Ponto LL, Parvizi J, et al: Subcortical and cortical brain activity during the feeling of self-generated emotions. Nat Neurosci 2000; 3: 1049-1056.
41. Lovero KL, Simmons AN, Aron JL, Paulus MP: Anterior insular cortex anticipates impending stimulus significance. Neuroimage 2009; 45: 976-983.
42. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, et al: Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 2007; 27: 2349-2356.
43. Jabbi M, Keysers C: Inferior frontal gyrus activity triggers anterior insula response to emotional facial expressions. Emotion 2008; 8: 775-780.
44. Ham TE, De Boissezon X, Leff A, Beckmann C, Hughes E, Kinnunen KM, et al: Distinct frontal networks are involved in adapting to internally and externally signaled errors. Cereb Cortex 2013; 23: 703-713.
45. Sridharan D, Levitin DJ, Menon V: A critical role for the right fronto-insular cortex in switching between central-executive and default mode networks. Proc Natl Acad Sci USA 2008; 105: 12569-12574.
46. Brass M, Haggard P: The hidden side of intentional action: The role of the anterior insular cortex. Brain Struct Funct 2010; 214: 603-610.
47. Aron AR, Robbins TW, Poldrack RA: Inhibition and the right inferior frontal cortex. Trends Cogn Sci 2004; 8: 170-177.
48. Chambers CD, Bellgrove MA, Stokes M, Henderson TR, Garavan H, Robertson IH, et al: Executive 'brake failure' following deactivation of human frontal lobe. J Cogn Neurosci 2006; 18: 444-455.
49. Swick D, Ashley V, Turken U: Are the neural correlates of stopping and not going identical?. Quantitative meta-Analysis of two response inhibition tasks. Neuroimage 2011; 56: 1655-1665.
50. Swick D, Ashley V, Turken AU: Left inferior frontal gyrus is critical for response inhibition. BMC Neurosci 2008; 9: 102.
51. Venkatraman V, Payne JW, Bettman JR, Luce MF, Huettel SA: Separate neural mechanisms underlie choices and strategic preferences in risky decision making. Neuron 2009; 62: 593-602.
52. Xue G, Lu Z, Levin IP, Bechara A: The impact of prior risk experiences on subsequent risky decision-making: The role of the insula. Neuroimage 2010; 50: 709-716.
53. Saad ZS, Ropella KM, DeYoe EA, Bandettini PA: The spatial extent of the BOLD response. Neuroimage 2003; 19: 132-144.
54. Lai S, Hopkins AL, Haacke EM, Li D, Wasserman BA, Buckley P, et al: Identification of vascular structures as a major source of signal contrast in high resolution 2D and 3D functional activation imaging of the motor cortex at l.5 T preliminary results. Magn Reson Med 2005; 30: 387-392.
55. Rostrup E, Law I, Blinkenberg M, Larsson HBW, Born AP, Holm S, et al: Regional differences in the CBF and BOLD responses to hypercapnia: A combined PET and fmri study. Neuroimage 2000; 11: 87-97.
56. Wise RG, Ide K, Poulin MJ, Tracey I: Resting fluctuations in arterial carbon dioxide induce significant low frequency variations in BOLD signal. Neuroimage 2004; 21: 1652-1664.
57. Chang C, Thomason ME, Glover GH: Mapping and correction of vascular hemodynamic latency in the bold signal. Neuroimage 2008; 43: 90-102.
58. Craig A: Emotional moments across time: A possible neural basis for time perception in the anterior insula. Philos Trans R Soc Lond B Biol Sci 2009; 364: 1933-1942.
59. Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijenbos A, et al: Brain development during childhood and adolescence: A longitudinal MRI study. Nat Neurosci 1999; 2: 861-863.
60. Shaw P, Kabani NJ, Lerch JP, Eckstrand K, Lenroot R, Gogtay N, et al: Neurodevelopmental trajectories of the human cerebral cortex. J Neurosci 2008; 28: 3586-3594.
61. Dennis EL, Jahanshad N, McMahon KL, De Zubicaray GI, Martin NG, Hickie IB, et al: Development of insula connectivity between ages 12 and 30 revealed by high angular resolution diffusion imaging. Hum Brain Mapp 2014; 35: 1790-1800.
62. Tamnes C, Østby Y, Fjell A, Westlye L, Due- Tonnessen P, Walhovd K: Brain maturation in adolescence and young adulthood: Regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb Cortex 2010; 20: 534-548.
63. Teicher MH, Andersen SL, Hostetter J: Evidence for dopamine receptor pruning between adolescence and adulthood in striatum but not nucleus accumbens. Dev Brain Res 1995; 89: 167-172.
64. Chang LJ, Yarkoni T, Khaw MW, Sanfey AG: Decoding the role of the insula in human cognition: Functional parcellation and large-scale reverse inference. Cereb Cortex 2013; 23: 739-749.
65. Fair DA, Dosenbach NUF, Church JA, Cohen AL, Brahmbhatt S, Miezin FM, et al: Development of distinct control networks through segregation and integration. Proc Nat Acad Sci USA 2007; 104: 13507-13512.
66. Strang N, Pruessner J, Pollack S: Developmental changes in adolescents' neural response to challenge. Dev Cogn Neurosci 2011; 1: 560-569.
67. Hwang K, Velanova K, Luna B: Strengthening of top-down frontal cognitive control networks underlying the development of inhibitory control: A functional magnetic resonance imaging effective connectivity study. J Neurosci 2010; 30: 15535-15545.
68. Somerville LH, Hare T, Casey B: Frontostriatal maturation predicts cognitive control failure to appetitive cues in adolescents. J Cogn Neurosci 2011; 23: 2123-2134.
69. Stevens MC, Pearlson GD, Calhoun VD: Changes in the interaction of resting-state neural networks from adolescence to adulthood. Hum Brain Mapp 2009; 30: 2356-2366.
70. 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: 2037-2078.
71. Klein C, Foerster F: Development of prosaccade and antisaccade task performance in participants aged 6 to 26 years. Psychophysiology 2001; 38: 179-189.
72. Luna B, Garver KE, Urban TA, Lazar NA, Sweeney JA: Maturation of cognitive processes from late childhood to adulthood. Child Dev 2004; 75: 1357-1372.
73. Adleman N: A developmental fmri study of the Stroop color-word task. Neuroimage 2002; 16: 61-75.
74. Andrews-Hanna JR, Mackiewicz Seghete KL, Claus ED, Burgess GC, Ruzic L, Banich MT: Cognitive control in adolescence: Neural underpinnings and relation to self-report behaviors. PLoS ONE 2011; 6:e21598.
75. Bunge S, Dudukovic NM, Thomason ME, Vaidya CJ, Gabrieli JD: Immature frontal lobe contributions to cognitive control in children: Evidence from fMRI. Neuron 2002; 33: 301-311.
76. Marsh R, Zhu H, Schultz R, Quackenbush G, Royal J, Skudlarski P, et al: A developmental fmri study of self-regulatory control. Hum Brain Mapp 2006; 27: 848-863.
77. Rubia K, Smith AB, Woolley J, Nosarti C, Heyman I, Taylor E, Brammer M: Progressive increase of frontostriatal brain activation from childhood to adulthood during event- related tasks of cognitive control. Hum Brain Map 2006;27:973-993.
78. Rubia K, Lim L, Ecker C, Halari R, Giampietro V, Simmons A, et al: Effects of age and gender on neural networks of motor response inhibition: From adolescence to mid-Adulthood. Neuroimage 2013;83:690-703.
79. Rubia K, Smith AB, Woolley J, Nosarti C, Heyman I, Taylor E, et al: Progressive increase of frontostriatal brain activation from childhood to adulthood during event-related tasks of cognitive control. Hum Brain Mapp 2006; 27: 973-993.
80. Velanova K, Wheeler ME, Luna B: The maturation of task set-related activation supports late developmental improvements in inhibitory control. J Neurosci 2009; 29: 12558-12567.
81. Booth JR, Burman DD, Meyer JR, Lei Z, Trommer BL, Davenport ND, et al: Neural development of selective attention and response inhibition. Neuroimage 2003; 20: 737-751.
82. Casey B, Trainor RJ, Orendi JL, Schubert AB, Nystrom LE, Giedd JN, et al: A developmental functional MRI study of prefrontal activation during performance of a go/no-go task. J Cogn Neurosci 1997; 9: 835-847.
83. Luna B, Thulborn KR, Munoz DP, Merriam EP, Garver KE, Minshew NJ, et al: Maturation of widely distributed brain function subserves cognitive development. Neuroimage 2001; 13: 786-793.
84. Tamm L, Menon V, Reiss A: Maturation of brain function associated with response inhibition. J Am Acad Child Adolesc Psychiatry 2002; 41: 1231-1238.
85. Rubia K, Smith AB, Taylor E, Brammer M: Linear age-correlated functional development of right inferior fronto-striato-cerebellar networks during response inhibition and anterior cingulate during error-related processes. Hum Brain Mapp 2007; 28: 1163-1177.
86. 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; 44: 1764-1778.
87. Blakemore S-J: The social brain in adolescence. Nat Rev Neurosci 2008; 9: 267-277.
88. Casey B, Jones RM, Hare T: The adolescent brain. Ann NY Acad Sci 2008; 1124: 111-126.
89. Steinberg L: A dual systems model of adolescent risk-taking. Dev Psychobiol 2010; 52: 216-224.
90. Galvan A, Hare TA, Parra CE, Penn J, Voss H, Glover G, et al: Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. J Neurosci 2006; 26: 6885-6892.
91. Van Leijenhorst L, Zanolie K, Van Meel C, Westenberg PM, Rombouts SARB, Crone EA: What motivates the adolescent?. Brain regions mediating reward sensitivity across adolescence. Cereb Cortex 2010; 20: 61-69.
92. Bjork JM, Knuston B, Fong GW, Caggiano DM, Bennett SM, Hommer DW: Incentiveelicited brain activation in adolescents: Similarities and differences from young adults. J Neurosci 2004; 24: 1793-1802.
93. Bjork JM, Smith AR, Chen G, Hommer DW: Adolescents, adults and rewards: Comparing motivational neurocircuitry recruitment using fMRI. PLoS ONE 2010; 5:e11440.
94. Geier CF, Terwilliger R, Teslovich T, Velanova K, Luna B: Immaturities in reward processing and its influence on inhibitory control in adolescence. Cereb Cortex 2010; 20: 1613-1629.
95. Krain AL, Hefton S, Pine DS, Ernst M, Xavier Castellanos F, Klein RG, et al: An fmri examination of developmental differences in the neural correlates of uncertainty and decision-making. J Child Psychol Psychiatry 2006; 47: 1023-1030.
96. Padmanabhan A, Geier C, Ordaz S, Teslovich T, Luna B: Developmental changes in brain function underlying the influence of reward processing on inhibitory control. Dev Cogn Neurosci 2011; 1: 517-529.
97. Van Leijenhorst L, Moor BG, De Macks ZAO, Rombouts SARB, Westenberg PM, Crone EA: Adolescent risky decision-making: Neurocognitive development of reward and control regions. Neuroimage 2010; 51: 345-355.
98. Galvan A, McGlennen KM: Enhanced striatal sensitivity to aversive reinforcement in adolescents versus adults. J Cogn Neurosci 2013; 25: 284-296.
99. Jarcho JM, Benson BE, Plate RC, Guyer AE, Detloff AM, Pine DS, et al: Developmental effects of decision-making on sensitivity to reward: An fmri study. Dev Cogn Neurosci 2012; 2: 437-447.
100. Galvan A, Hare T, Voss H, Glover G, Casey BJ: Risk-taking and the adolescent brain: Who is at risk?. Dev Sci 2007; 10:F8-F14.
101. Barkley-Levenson EE, Van Leijenhorst L, Galvan A: Behavioral and neural correlates of loss aversion and risk avoidance in adolescents and adults. Dev Cogn Neurosci 2013; 3: 72-83.
102. Bjork JM, Smith AR, Danube CL, Hommer DW: Developmental differences in posterior mesofrontal cortex recruitment by risky rewards. J Neurosci 2007; 27: 4839-4849.
103. Chein J, Albert D, O'Brien L, Uckert K, Steinberg L: Peers increase adolescent risk taking by enhancing activity in the brain's reward circuitry. Dev Sci 2011; 14:F1-F10.
104. Eshel N, Nelson EE, Blair RJ, Pine DS, Ernst M: Neural substrates of choice selection in adults and adolescents: Development of the ventrolateral prefrontal and anterior cingulate cortices. Neuropsychologia 2007; 45: 1270-1279.
105. Paulsen DJ, Carter R, Platt M, Huettal SA, Brannon E: Neurocognitive development of risk aversion from early childhood to adulthood. Front Hum Neurosci 2012; 5: 178.
106. Bechara A, Damasio AR: The somatic marker hypothesis: A neural theory of economic decision. Games Econ Behav 2005; 52: 336-372.
107. Christakou A, Brammer M, Rubia K: Maturation of limbic corticostriatal activation and connectivity associated with developmental changes in temporal discounting. Neuroimage 2011; 54: 1344-1354.
108. Smith AB, Halari R, Giampetro V, Brammer M, Rubia K: Developmental effects of reward on sustained attention networks. Neuroimage 2011; 56: 1693-1704.
109. Goldenberg D, Telzer EH, Lieberman MD, Fuligni A, Galvan A: Neural mechanisms of impulse control in sexually risky adolescents. Dev Cogn Neurosci 2013; 6: 23-29.
110. Steinberg L, Graham S, O'Brien L, Woolard J, Cauffman E, Banich M: Age differences in future orientation and delay discounting. Child Dev 2009; 80: 28-44.
111. Church JA, Petersen SE, Schlaggar BL: The 'Task B problem' and other considerations in developmental functional neuroimaging. Hum Brain Mapp 2010; 31: 852-862.
112. Harris JJ, Reynell C, Attwell D: The physiology of developmental changes in BOLD functional imaging signals. Dev Cogn Neurosci 2011; 1: 199-216.
113. Cohen JR, Asarnow RF, Sabb FW, Bilder RM, Bookheimer SY, Knowlton BJ, Poldrack RA: Decoding developmental differences and individual variability in response inhibition through predictive analyses across individuals. Front Hum Neurosci 2010;4.
114. Hoogendam JM, Kahn RS, Hillegers MH, Van Buuren M, Vink M: Different developmental trajectories for anticipation and receipt of reward during adolescence. Dev Cogn Neurosci 2013;6:113-124.
115. Teslovich T, Mulder M, Franklin NT, Ruberry EJ, Millner A, Somerville LH, Simen P, Dustron S, Casey BJ: Adolescents let sufficient evidence accumulate before making a decision when large incentives are at stake. Dev Sci 2014;17:59-70.
116. Van Leijenhorst L, Crone EA, Bunge SA: Neural correlates of developmental differences in risk estimation and feedback processing. Neuropsychologia 2006;44:2158-2170.
117. Casey BJ, Thomas KM, Davidson MC, Kunz K, Franzen PL: Dissociating striatal and hippocampal function developmentally with a stimulus-response compatibility task. J Neurosci 2002;22:8647-8652.
118. Christakou A, Gershman SJ, Niv Y, Simmons A, Brammer M, Rubia K: Neural and psychological maturation of decision-making in adolescence and young adulthood. J Cogn Neurosci 2013;25:1807-1823.