A time of change: Behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues

Brain and Cognition

Volumn 72, Issue 1, 2010, Pages 124-133

  Somerville, Leah H ^a   Jones, Rebecca M ^a   Casey, B J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Adolescence; Amygdala; Brain; Cognitive control; Connectivity; Development; Emotion; fMRI; Function; Nucleus accumbens; Peers; Prefrontal cortex; Reward; Risk

Indexed keywords

SEX HORMONE;

AMYGDALOID NUCLEUS; ANXIETY; ASSOCIATION; AUTOMUTILATION; AVERSION; CHILD BEHAVIOR; COGNITION; CORPUS STRIATUM; DECISION MAKING; DEPRESSION; EMOTION; EMOTIONALITY; HIGH RISK BEHAVIOR; HORMONE ACTION; HUMAN; MENTAL DISEASE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; REVIEW; REWARD; RISK FACTOR; SOCIAL BEHAVIOR; SOCIAL ENVIRONMENT; SOCIAL INTERACTION; STIMULUS RESPONSE; SUICIDE;

ADOLESCENT; ANIMALS; BEHAVIOR; BRAIN; CUES; ENVIRONMENT; HUMANS; MODELS, NEUROLOGICAL;

EID: 72649107448     PISSN: 02782626     EISSN: 10902147     Source Type: Journal    
DOI: 10.1016/j.bandc.2009.07.003     Document Type: Review

References (110)

1. Abe K., and Suzuki T. Prevalence of some symptoms in adolescence and maturity: Social phobias, anxiety symptoms, episodic illusions and ideas of reference. Psychopathology 19 (1986) 200-205
2. Adolphs R. Recognizing emotion from facial expressions: Psychological and neurological mechanisms. Behavioral and Cognitive Neuroscience Reviews 1 1 (2002) 21-62
3. Adriani W., Chiarotti F., and Laviola G. Elevated novelty seeking and peculiar d-amphetamine sensitization in periadolescent mice compared with adult mice. Behavioral Neuroscience 112 5 (1998) 1152-1166
4. Aggleton J.P. The amygdala: A functional analysis (2000), Oxford University Press, New York
5. Arnett J. Adolescent storm and stress, reconsidered. American Psychologist 54 (1999) 317-326
6. Baird A.A., Gruber S.A., Fein D.A., Maas L.C., Steingard R.J., Renshaw P.F., et al. Functional magnetic resonance imaging of facial affect recognition in children and adolescents. Journal of the American Academy of Child and Adolescent Psychiatry 38 2 (1999) 195-199
7. Bjork J.M., Knutson B., Fong G.W., Caggiano D.M., Bennett S.M., and Hommer D.W. Incentive-elicited brain activation in adolescents: Similarities and differences from young adults. Journal of Neuroscience 24 8 (2004) 1793-1802
8. Blakemore S.-J. The social brain in adolescence. Nature Reviews Neuroscience 9 (2008) 267-277
9. Bogin B. Adolescence in evolutionary perspective. Acta Paediatrics Supplement 406 (1994) 29-35
10. Buchanan C.M., Eccles J.S., and Becker J.B. Are adolescents the victims of raging hormones: Evidence for activational effects of hormones on moods and behavior at adolescence. Psychological Bulletin 111 (1992) 62-107
11. Cardinal R.N., Parkinson J.A., Hall J., and Everitt B.J. Emotion and motivation: The role of the amygdala, ventral striatum, and prefrontal cortex. Neuroscience and Biobehavioral Reviews 26 3 (2002) 321-352
12. Cascio C.J., Gerig G., and Piven J. Diffusion tensor imaging: Application to the study of the developing brain. Journal of the American Academy of Child and Adolescent Psychiatry 46 2 (2007) 213-223
13. Casey B.J., Galvan A., and Hare T.A. Changes in cerebral functional organization during cognitive development. Current Opinion in Neurobiology 15 2 (2005) 239-244
14. Casey B.J., Getz S., and Galvan A. The adolescent brain. Developmental Review 28 1 (2008) 62-77
15. Casey B.J., Jones R.M., and Hare T. The adolescent brain. Annals of the New York Academy of Sciences 1124 (2008) 111-126
16. Casey B.J., Tottenham N., Liston C., and Durston S. Imaging the developing brain: What have we learned about cognitive development?. Trends in Cognitive Science 9 3 (2005) 104-110
17. Cauffman, E., Shulman, E. P., Steinberg, L., Claus, E., Banich, M. T., Graham, S. J., et al. (in press). Age differences in affective decision making as indexed by performance on the Iowa Gambling Task. Developmental Psychology.
18. Caviness V.S., Kennedy D.N., Richelme C., Rademacher J., and Filipek P.A. The human brain age 7-11 years: A volumetric analysis based on magnetic resonance images. Cerebral Cortex 6 (1996) 726-736
19. Compas B.E., Hinden B.R., and Gerhardt C.A. Adolescent development: Pathways and processes of risk and resilience. Annual Review of Psychology 46 (1995) 265-293
20. Compas B.E., Orosan P.G., and Grant K.E. Adolescent stress and coping: Implications for psychopathology during adolescence. Journal of Adolescence 16 (1993) 331-349
21. Cooke B., Hegstrom C.D., Villeneuve L.S., and Breedlove S.M. Sexual differentiation of the vertebrate brain: Principles and mechanisms. Frontiers in Neuroendocrinology 19 4 (1998) 323-362
22. Davis M., and Whalen P.J. The amygdala: Vigilance and emotion. Molecular Psychiatry 6 1 (2001) 13-34
23. Daw N.D., O'Doherty J.P., Dayan P., Seymour B., and Dolan R.J. Cortical substrates for exploratory decisions in humans. Nature 441 (2006) 876-879
24. Delgado M.R. Reward-related responses in the human striatum. Annals of the New York Academy of Sciences 1104 (2007) 70-88
25. Delgado M.R., Nystrom L.E., Fissell C., Noll D.C., and Fiez J.A. Tracking the hemodynamic responses to reward and punishment in the striatum. Journal of Neurophysiology 84 6 (2000) 3072-3077
26. Durston S., Davidson M.C., Tottenham N., Galvan A., Spicer J., Fossella J.A., et al. A shift from diffuse to focal cortical activity with development. Developmental Science 9 1 (2006) 1-8
27. Eaton L.K., Kann L., Kinchen S., Shanklin S., Ross J., Hawkins J., et al. Youth risk behavior surveillance - United States, 2007, surveillance summaries. Morbidity and Mortality Weekly Report 57 SS04 (2008) 1-131
28. Eccles J.S., Wigfield A., Flanagan C.A., Miller C., Reuman D.A., and Yee D. Self concepts, domain values, and self-esteem: Relations and changes at early adolescence. Journal of Personality 57 (1989) 283-310
29. Eigsti I.M., Zayas V., Mischel W., Shoda Y., Ayduk O., Dadlani M.B., et al. Predicting cognitive control from preschool to late adolescence and young adulthood. Psychological Science 17 6 (2006) 478-484
30. Eisenberger N.I., Lieberman M.D., and Williams K.D. Does rejection hurt? An fMRI study of social exclusion. Science 302 5643 (2003) 290-292
31. Ernst M., Nelson E.E., Jazbec S., McClure E.B., Monk C.S., Leibenluft E., et al. Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents. Neuroimage 25 4 (2005) 1279-1291
32. Ernst M., Pine D.S., and Hardin M. Triadic model of the neurobiology of motivated behavior in adolescence. Psychological Medicine 36 3 (2006) 299-312
33. Etkin A., Klemenhagen K.C., Dudman J.T., Rogan M.T., Hen R., Kandel E.R., et al. Individual differences in trait anxiety predict the response of the basolateral amygdala to unconsciously processed fearful faces. Neuron 44 6 (2004) 1043-1055
34. Fareri D.S., Martin L.N., and Delgado M.R. Reward-related processing in the human brain: Developmental considerations. Development and Psychopathology 20 (2008) 1191-1211
35. Figner B., Mackinlay R.J., Wilkening F., and Weber E.U. Affective and deliberative processes in risky choice: Age differences in risk taking in the Columbia Card Task. Journal of Experimental Psychology: Learning, Memory, and Cognition 35 3 (2009) 709-730
36. Figner, B., Mackinlay, R. J., Wilkening, F., & Weber, E. U. (2009b). Risky choice in children, adolescents, and adults: Affective versus deliberative processes and the role of executive functions. In Proceedings of the society for research in child development, Denver, CO, USA.
37. Galvan A., Hare T.A., Davidson M., Spicer J., Glover G., and Casey B.J. The role of ventral frontostriatal circuitry in reward-based learning in humans. Journal of Neuroscience 25 38 (2005) 8650-8656
38. Galvan A., Hare T.A., Parra C.E., Penn J., Voss H., Glover G., et al. Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. Journal of Neuroscience 26 25 (2006) 6885-6892
39. Galvan A., Hare T., Voss H., Glover G., and Casey B.J. Risk-taking and the adolescent brain: Who is at risk?. Developmental Science 10 2 (2007) F8-F14
40. Gardener M., and Steinberg L. Peer influence on risk taking, risk preference, and risky decision making in adolescence and adulthood: An experimental study. Developmental Psychology 41 (2005) 625-635
41. Giedd J.N., Castellanos F.X., Rajapakse J.C., Vaituzis A.C., and Rapoport J.L. Sexual dimorphism of the developing human brain. Progress in Neuropsychopharmacology and Biological Psychiatry 21 8 (1997) 1185-1201
42. Giedd J.N., Vaituzis A.C., Hamburger S.D., Lange N., Rajapakse J.C., Kaysen D., et al. Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: Ages 4-18 years. The Journal of Comparative Neurology 366 (1996) 223-230
43. Giedd J.N., Blumenthal J., Jeffries N.O., Castellanos F.X., Liu H., Zijdenbos A., et al. Brain development during childhood and adolescence: A longitudinal MRI study. Nature Neuroscience 2 (1999) 861-863
44. Granger D.A., Shirtcliff E.A., Zahn-Waxler C., Usher B., Klimes-Dougan B., and Hastings P. Salivary testosterone diurnal variation and psychopathology in adolescent males and females: Individual differences and developmental effects. Developmental Psychopathology 15 2 (2003) 431-449
45. Grosbras M.-H., Jansen M., Leonard G., McIntosh A., Osswald K., Poulsen C., et al. Neural mechanisms of resistance to peer influence in early adolescence. Journal of Neuroscience 27 30 (2007) 8040-8045
46. Guyer A.E., Lau J.Y., McClure-Tone E.B., Parrish J., Shiffrin N.D., Reynolds R.C., et al. Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety. Archives of General Psychiatry 65 11 (2008) 1303-1312
47. Guyer A.E., Monk C.S., McClure-Tone E.B., Nelson E.E., Roberson-Nay R., Adler A., et al. A developmental examination of amygdala response to facial expressions. Journal of Cognitive Neuroscience 20 9 (2008) 1565-1582
48. Hall G.S. Adolescence: In psychology and its relation to physiology, anthropology, sociology, sex, crime, religion, and education Vols. I and II (1904), Prentice-Hall, Englewood Cliffs, NJ
49. Hare T.A., and Casey B.J. The neurobiology and development of cognitive and affective control. Cognition, Brain and Behavior 9 3 (2005) 273-286
50. Hare T.A., Tottenham N., Galvan A., Voss H.U., Glover G.H., and Casey B.J. Biological substrates of emotional reactivity and regulation in adolescence during an emotional go-nogo task. Biological Psychiatry 63 10 (2008) 927-934
51. Huttenlocher P.R. Regional differences in synaptogenesis in human cerebral cortex. Journal of Comparative Neurology 387 (1997) 167-178
52. Johansen-Berg H., Gutman D.A., Behrens T.E.J., Matthews P.M., Rushworth M.F.S., Katz E., et al. Anatomical connectivity of the subgenual cingulate region targeted with deep brain stimulation for treatment-resistant depression. Cerebral Cortex 18 (2008) 1374-1383
53. Kessler R.C., Berglund P., Delmer O., Jin R., Merikangas K.R., and Walters E.E. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Archives of General Psychiatry 62 (2005) 593-602
54. Kim, M. J., & Whalen, P. J. The structural integrity of an amygdala-prefrontal pathway predicts trait anxiety. Journal of Neuroscience.
55. Knutson B., Adams C.M., Fong G.W., and Hommer D. Anticipation of increasing monetary reward selectively recruits nucleus accumbens. Journal of Neuroscience 21 16 (2001) RC159
56. Kober H., Barrett L.F., Joseph J., Bliss-Moreau E., Lindquist K., and Wager T.D. Functional grouping and cortical-subcortical interactions in emotion: A meta-analysis of neuroimaging studies. Neuroimage 42 2 (2008) 998-1031
57. Larson R.W., Moneta G., Richards M.H., and Wilson S. Continuity, stability, and change in daily emotional experience across adolescence. Child Development 73 4 (2002) 1151-1165
58. Laviola G., Macri S., Morley-Fletcher S., and Adriani W. Risk-taking behavior in adolescent mice: Psychobiological determinants and early epigenetic influence. Neuroscience Biobehavioral Review 27 1-2 (2003) 19-31
59. LeDoux J.E. Emotion circuits in the brain. Annual Review of Neuroscience 23 (2000) 155-184
60. Liston C., Watts R., Tottenham N., Davidson M.C., Niogi S., Ulug A.M., et al. Frontostriatal microstructure modulates efficient recruitment of cognitive control. Cerebral Cortex 16 4 (2006) 553-560
61. May J.C., Delgado M.R., Dahl R.E., Stenger V.A., Ryan N.D., Fiez J.A., et al. Event-related functional magnetic resonance imaging of reward-related brain circuitry in children and adolescents. Biological Psychiatry 55 4 (2004) 359-366
62. Miller E.K., and Cohen J.D. An integrative theory of prefrontal cortex function. Annual Review of Neuroscience 24 (2001) 167-202
63. Monk C.S., McClure E.B., Nelson E.E., Zarahn E., Bilder R.M., Leibenluff E., et al. Adolescent immaturity in attention-related brain engagement to emotional facial expressions. Neuroimage 20 (2003) 420-428
64. Mościcki E. Epidemiology of attempted and completed suicide: Toward a framework for prevention. Clinical Neuroscience Research 1 (2001) 310-323
65. National Research Council (2007). Preventing teen motor crashes: Contributions from the behavioral and social sciences. Washington, DC: National Academies Press.
66. Nelson E.E., Leibenluft E., McClure E.B., and Pine D.S. The social re-orientation of adolescence: A neuroscience perspective on the process and its relation to psychopathology. Psychological Medicine 35 (2005) 163-174
67. Neufang S., Specht K., Hausmann M., Gunturkun O., Herpertz-Dahlmann B., Fink G.R., et al. Sex differences and the impact of steroid hormones on the developing human brain. Cerebral Cortex 19 2 (2009) 464-473
68. Norjavaara E., Ankarberg C., and Albertsson-Wikland K. Diurnal rhythm of 17 beta-estradiol secretion throughout pubertal development in healthy girls: Evaluation by a sensitive radioimmunoassay. Journal of Clinical Endocrinology and Metabolism 81 11 (1996) 4095-4102
69. O'Doherty J.P. Reward representations and reward-related learning in the human brain: Insights from neuroimaging. Current Opinion in Neurobiology 14 6 (2004) 769-776
70. O'Doherty J.P., Deichmann R., Critchley H.D., and Dolan R.J. Neural responses during anticipation of a primary taste reward. Neuron 33 5 (2002) 815-826
71. Ochsner K.N., and Gross J.J. The cognitive control of emotion. Trends in Cognitive Science 9 5 (2005) 242-249
72. Paus T., Keshavan M., and Giedd J.N. Why do many psychiatric disorders emerge during adolescence?. Nature Reviews Neuroscience 9 (2008) 947-957
73. Perrin J.S., Herve P.Y., Leonard G., Perron M., Pike G.B., Pitiot A., et al. Growth of white matter in the adolescent brain: Role of testosterone and androgen receptor. Journal of Neuroscience 28 38 (2008) 9519-9524
74. Pessoa L. On the relationship between emotion and cognition. Nature Reviews Neuroscience 9 2 (2008)
75. Petersen A.C., Compas B.E., Brooks-Gunn J., Stemmler M., Ey S., and Grant K.E. Depression in adolescence. American Psychologist 48 (1993) 155-168
76. Phelps E.A. Emotion and cognition: Insights from studies of the human amygdala. Annual Review of Psychology 57 (2006) 27-53
77. Pine D.S., Cohen P., and Brook J.S. Emotional reactivity and risk for psychopathology among adolescents. CNS Spectrum 6 1 (2001) 27-35
78. Rakic P., Bourgeois J.P., Eckenhoff M.F., Zecevic N., and Goldman-Rakic P.S. Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science 232 (1986) 232-235
79. Reyna V.F., and Farley F. Risk and rationality in adolescent decision making: Implications for theory, practice, and public policy. Psychological Science in the Public Interest 7 1 (2006) 1-44
80. Rolls E. The orbitofrontal cortex and reward. Cerebral Cortex 10 (2000) 284-294
81. Romeo R.D., Richardson H.N., and Sisk C.L. Puberty and the maturation of the male brain and sexual behavior: Recasting a behavioral potential. Neuroscience and Biobehavioral Reviews 26 3 (2002) 381-391
82. Rutter M., Graham P., Chadwick O.F.D., and Yule W. Adolescent turmoil: Fact or fiction?. Journal of Child Psychology and Psychiatry 17 (1976) 35-56
83. Schaal B., Tremblay R.E., Soussignan R., and Susman E.J. Male testosterone linked to high social dominance but low physical aggression in early adolescence. Journal of the American Academy of Child and Adolescent Psychiatry 35 10 (1996) 1322-1330
84. Schlaggar B.L., Brown T.T., Lugar H.M., Visscher K.M., Miezin F.M., and Petersen S.E. Functional neuroanatomical differences between adults and school-age children in the processing of single words. Science 296 5572 (2002) 1476-1479
85. Schmithorst V.J., Wilke M., Dardzinski B.J., and Holland S.K. Correlation of white matter diffusivity and anisotropy with age during childhood and adolescence: A cross-sectional diffusion-tensor MR imaging study. Radiology 222 (2002) 212-218
86. Schultz W. Behavioral theories and the neurophysiology of reward. Annual Reviews of Psychology 57 (2006) 87-115
87. Schultz W., Dayan P., and Montague P.R. A neural substrate of prediction and reward. Science 275 5306 (1997) 1593-1599
88. Schumann C.M., JHamstra J., Goodlin-Jones B.L., Lotspeich L.J., Kwon H., Buonocore M.H., et al. The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. Journal of Neuroscience 24 28 (2004) 6392-6401
89. Silveri M.M., Tzilos G.K., Pimentel P.J., and Yurgelun-Todd D.A. Trajectories of adolescent emotional and cognitive development: Effects of sex and risk for drug use. Annals of the New York Academy of Sciences 1021 (2004) 363-370
90. Simmons R.G., and Blyth D.A. Moving into adolescence: The impact of pubertal change and school context (1987), Aldine de Gruyter, Hawthorne, NY
91. Simmons R.G., Rosenberg F., and Rosenberg M. Disturbance in the self-image at adolescence. American Sociological Review 38 (1973) 553-568
92. Sisk C.L., and Zehr J.L. Pubertal hormones organize the adolescent brain and behavior. Frontiers in Neuroendocrinology 26 3-4 (2005) 163-174
93. Snook L., Paulson L.A., Roy D., Phillips L., and Beaulieu C. Diffusion tensor imaging of neurodevelopment in children and young adults. Neuroimage 26 (2005) 1164-1173
94. Somerville, L. H., Fani, N., & McClure-Tone, E. B. (in press). Behavioral and neural representations of emotional facial expressions across the lifespan. Developmental Neuropsychology.
95. Somerville L.H., Heatherton T.F., and Kelley W.M. Anterior cingulate cortex responds differentially to expectancy violation and social rejection. Nature Neuroscience 9 8 (2006) 1007-1008
96. Somerville L.H., Kim H., Johnstone T., Alexander A.L., and Whalen P.J. Human amygdala responses during presentation of happy and neutral faces: Correlations with state anxiety. Biological Psychiatry 55 9 (2004) 897-903
97. Sowell E.R., Trauner D.A., Gamst A., and Jernigan T.L. Development of cortical and subcortical brain areas in childhood and adolescence: A structural MRI study. Developmental Medicine and Child Neurology 44 1 (2002) 4-16
98. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews 24 4 (2000) 417-463
99. Stein M.B., Simmons A.N., Feinstein J.S., and Paulus M.P. Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. American Journal of Psychiatry 164 2 (2007) 318-327
100. Steinberg L. Risk taking in adolescence: What changes, and why?. Annals of the New York Academy of Sciences 1021 (2004) 51-58
101. Steinberg L. Cognitive and affective development in adolescence. Trends in Cognitive Sciences 9 2 (2005) 69-74
102. Steinberg L. A social neuroscience perspective on adolescent risk-taking. Developmental Review 28 (2008) 78-106
103. Substance Abuse and Mental Health Services Administration (2007). Results from the 2006 national survey on drug use and health: National findings. Office of Applied Studies NSDUH Series H32, Publication No. SMA 07-4293. Rockville, MD.
104. Thomas K.M., Drevets W.C., Whalen P.J., Eccard C.H., Dahl R.E., Ryan N.D., et al. Amygdala response to facial expressions in children and adults. Biological Psychiatry 49 (2001) 309-316
105. Thornburg H.D., and Jones R.M. Social characteristics of early adolescents: Age vs. grade. Journal of Early Adolescence 2 (1982) 229-239
106. Urry H.L., van Reekum C.M., Johnstone T., Kalin N.H., Thurow M.E., Schaefer H.S., et al. Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict diurnal pattern of cortisol secretion among older adults. Journal of Neuroscience 26 16 (2006) 4415-4425
107. Vermeersch H., T'Sjoen G., Kaufman J.M., and Vincke J. The role of testosterone in aggressive and non-aggressive risk-taking in adolescent boys. Hormones and Behavior 53 3 (2008) 463-471
108. Vermeersch H., T'Sjoen G., Kaufman J.M., and Vincke J. Estradiol, testosterone, differential association and aggressive and non-aggressive risk-taking in adolescent girls. Psychoneuroendocrinology 33 7 (2008) 897-908
109. Williams L.M., Brown K.J., Palmer D., Liddell B.J., Kemp A.H., Olivieri G., et al. The mellow years? Neural basis of improving emotional stability with age. Journal of Neuroscience 26 24 (2006) 6422-6430
110. Zuckerman M., Eysenck S., and Eysenck H.J. Sensation seeking in England and America: Cross-cultural, age, and sex comparisons. Journal of Consulting and Clinical Psychology 46 (1978) 139-149