Neural systems supporting cognitive-affective interactions in adolescence: The role of puberty and implications for affective disorders

Frontiers in Integrative Neuroscience

Volumn , Issue AUGUST 2012, 2012, Pages

  Ladouceur, Cecile D ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Adolescence; Affective disorders; Cognition; Cognitive control; Development; Emotion; Puberty

Indexed keywords

ANDROSTENEDIONE; PRASTERONE; PRASTERONE SULFATE; SEX HORMONE; TESTOSTERONE;

ADOLESCENCE; ADULTHOOD; AFFECTIVE NEUROSIS; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ANXIETY DISORDER; ASSOCIATION; BRAIN DEVELOPMENT; COGNITION; CORPUS STRIATUM; EMOTION; EMOTIONAL DISORDER; FACIAL EXPRESSION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; LIMBIC CORTEX; MOOD DISORDER; MOTIVATION; NERVOUS SYSTEM; NEUROENDOCRINE SYSTEM; NEUROIMAGING; PREFRONTAL CORTEX; PUBERTY; REACTION TIME; REVIEW; SACCADIC EYE MOVEMENT; TASK PERFORMANCE; WORKING MEMORY;

EID: 84864984749     PISSN: 16625145     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnint.2012.00065     Document Type: Review

References (115)

1. Ahmed, E.I., Zehr, J.L., Schulz, K.M., Lorenz, B.H., Doncarlos, L.L., and Sisk, C.L. (2008). Pubertal hormones modulate the addition of new cells to sexually dimorphic brain regions. Nat Neurosci 11, 995-997.
2. Angold, A., Costello, E.J., Erkanli, A., and Worthman, C.M. (1999). Pubertal changes in hormone levels and depression in girls. Psychol Med 29, 1043-1053.
3. Angold, A., Costello, E.J., and Worthman, C.M. (1998). Puberty and depression: the roles of age, pubertal status and pubertal timing. Psychol Med 28, 51-61.
4. Asato, M.R., Terwilliger, R., Woo, J., and Luna, B. (2010). White matter development in adolescence: a DTI study. Cerebral Cortex 20, 2122-2131.
5. Aubele, T., and Kritzer, M.F. (2011). Gonadectomy and hormone replacement affects in vivo Basal extracellular dopamine levels in the prefrontal cortex but not motor cortex of adult male rats. Cerebral Cortex 21, 222-232.
6. Berman, K.F., Schmidt, P.J., Rubinow, D.R., Danaceau, M.A., Van Horn, J.D., Esposito, G., Osstrem, J.L., and Weinberger, D.R. (1997). Modulation of cognition-specific cortical activity by gonadal steroids: a position-emission tomography study in women. Proceedings of the National Academic of Sciences USA 94, 8836-8841.
7. Biro, F.M., Greenspan, L.C., and Galvez, M.P. (2012). Puberty in girls of the 21st Century. Journal of Pediatric and Adolescent Gynecology.
8. Bjork, J.M., Knutson, B., Fong, G.W., Caggiano, D.M., Bennett, S.M., and Hommer, D.W. (2004). Incentive-Elicited Brain Activation in Adolescents: Similarities and Differences from Young Adults. Journal of Neuroscience 24, 1793-1802.
9. Blakemore, S.J. (2008). The social brain in adolescence. Nature Reviews, Neuroscience 9, 267-277.
10. Blakemore, S.J., Burnett, S., and Dahl, R.E. (2010). The role of puberty in the developing adolescent brain. Human Brain Mapping 31, 926-933.
11. Bodo, C., and Rissman, E.F. (2006). New roles for estrogen receptor beta in behavior and neuroendocrinology. Frontiers of Neuroendocrinology 27, 217-232.
12. Bos, P.A., Panksepp, J., Bluthe, R.M., and Van Honk, J. (2011). Acute effects of steroid hormones and neuropeptides on human social-emotional behavior: A review of single administration studies. Frontiers in Neuroendocrinology 33, 17-35.
13. Bramen, J.E., Hranilovich, J.A., Dahl, R.E., Chen, J., Rosso, C., Forbes, E.E., Dinov, I.D., Worthman, C.M., and Sowell, E.R. (2012). Sex matters during adolescence: Testosterone-related cortical thickness maturation differences between boys and girls. PLoS ONE 7, e33850.
14. Bramen, J.E., Hranilovich, J.A., Dahl, R.E., Forbes, E.E., Chen, J., Toga, A.W., Dinov, I.D., Worthman, C.M., and Sowell, E.R. (2010). Puberty influences medial temporal lobe and cortical gray matter maturation differently in boys than girls matched for sexual maturity. Cerebral Cortex 21, 636-646.
15. Casey, B.J., Duhoux, S., and Cohen, M.M. (2010). Adolescence: What do transmission, transition, and translation have to do with it? Neuron 67, 749-760.
16. Casey, B.J., Jones, R.M., and Somerville, L.H. (2011). Braking and accelerating of the adolescent brain. Journal of Research on Adolescence 21, 21-33.
17. Cauffman, E., and Steinberg, L. (1995). The cognitive and affective influences on adolescent decision-making. Temple Law Review 68, 1763-1789.
18. Costello, E., Angold, A., Burns, B., Erkanli, A., Stangl, D., and Tweed, D. (1996). The Great Smoky Mountains Study of Youth. Functional impairment and serious emotional disturbance. Archives of General Psychiatry 53, 1229-1136.
19. Costello, E., Copeland, W., and Angold, A. (2011). Trends in psychopathology across adolescent years: What changes when children become adolescents, and when adolescents become adults? J Child Psychol Psychiatry 52, 1015-1025.
20. Cutler, G.B., Schiebinger, R.J., Albertson, B.D., Cassorla, F.G., Chrousos, G.P., Comite, F., and Al., E. (1990). Adrenarche (human and animals), in Control of the onset of puberty, eds. M.M. Grumbach, P.C. Sizonenko & M.L. Aubert. (Baltimore: Williams & Wilkins), 506-533.
21. Dahl, R.E. (2001). Affect regulation, brain development, and behavioral/emotional health in adolescence. CNS Spectrums 6, 60-72.
22. Dahl, R.E., and Spear, L. (2004). Adolescent Brain Development: Vulnerabilities and Opportunities. Annals of the New York Academy of Sciences 1021.
23. Deardorff, J., Gonzales, N.A., Christopher, F.S., Roosa, M.W., and Millsap, R. (2005). Early puberty and adolescent pregnancy: the influence of alcohol use. Pediatrics 116, 1451-1456.
24. Delemarre-Van De Waal, H.A. (2002). Regulation of puberty. Best Practice & Research Clinical Endocrinology & Metabolism 16, 1-12.
25. Demir, A., Voutilainen, R., Juul, A., Dunkel, L., Alfthan, H., Skakkebaek, N.E., and Stenman, U.H. (1996). Increase in the first morning voided urinary luteinizing hormone levels precedes the physical onset of puberty. Journal of Clinical Endocrinology and Metabolism 81, 2963-2967.
26. Derntl, B., Windischberger, C., Robinson, S., Kryspin-Exner, I., Gur, R.C., Moser, E., and Habel, U. (2009). Amygdala activity to fear and anger in healthy young men is associated with testosterone. Psychoneuroendocrinology 34, 687-693.
27. Dick, D.M., Rose, R.J., Viken, R.J., and Kaprio, J. (2000). Pubertal timing and substance use: Associations between and within families across adolescence. Developmental Psychology 36, 180-189.
28. Dolcos, F., Iordan, A.D., and Dolcos, S. (2011). Neural correlates of emotion-cognition interactions: A review of evidence from brain imaging investigations. Journal of Cognitive Psychology 23, 669-694.
29. Dorn, L.D., Dahl, R.E., Woodward, H.R., and Biro, F. (2006). Defining boundaries of early adolescence: A user's guide to assessing pubertal status and pubertal timing in research with adolescents. Applied Developmental Science 10, 30-56.
30. Eisenegger, C., Haushofer, J., and Fehr, E. (2011). The role of testoterone in social interaction. Trends in Cognitive Sciences 15, 263-271.
31. Elliott, R., Zahn, R., Deakin, J.F., and Anderson, I.M. (2010). Affective cognition and its disruption in mood disorders. Neuropsychopharmacology 36, 153-182.
32. Ellis, B.J. (2004). Timing of pubertal maturation in girls: An integrated life history approach. Psychological Bulletin 130, 920-958.
33. Ellis, B.J., Boyce, W.T., Belsky, J., Bakermans-Kranenburg, M.J., and Van Ijzendoorn, M.H. (2011a). Differential susceptibility to the environment: An evolutionaryneurodevelopmental theory. Development and Psychopathology 23, 7-28.
34. Ellis, B.J., Shirtcliff, E.A., Boyce, W.T., Deardorff, J., and Essex, M.J. (2011b). Quality of early family relationships and the timing and tempo of puberty: effects depend on biological sensitivity to context. Developmental Psychopathology 23, 85-99.
35. Ernst, M., Daniele, T., and Frantz, K. (2011). New perspectives on adolescent motivated behavior: attention and conditioning. Developmental Cognitive Neuroscience 1, 377-389.
36. Ernst, M., Pine, D.S., and Hardin, M. (2006). Triadic model of the neurobiology of motivated behavior in adolescence. Psychological Medicine 36, 299-312.
37. Forbes, E.E., and Dahl, R.E. (2010). Pubertal development and behavior: hormonal activation of social and motivational tendencies. Brain and Cognition 72, 66-72.
38. Forbes, E.E., Phillips, M.L., Ryan, N.D., and Dahl, R.E. (2011). Neural systems of threat processing in adolescents: Role of pubertal maturation and relation to measures of negative affect. Developmental Neuropsychology 36, 429-452.
39. Force, U. (1996). Guide to clinical preventive services, 2nd ed. Alexandria, VA: International Medical Publishing.
40. Geier, C.F., Terwilliger, T., Velanova, K., and Luna, B. (2010). Immaturities in reward processing and its influence on inhibitory control in adolescence. Cerebral Cortex 20, 1613-1629.
41. Giedd, J.N., Blumenthal, J., Jeffries, N.O., Castellanos, F.X., Liu, H., Zijdenbos, A., Paus, T., Evans, A.C., and Rapoport, J.L. (1999). Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 2, 861-863.
42. Giedd, J.N., Clasen, L.S., Lenroot, R., Greenstein, D., Wallace, G.L., Ordaz, S., Molloy, E.A., Blumenthal, J.D., Tossell, J.W., Stayer, C., Samango-Sprouse, C., Shen, D., Davatzikos, C., Merke, D., and Chrousos, G.P. (2006). Puberty-related influences on brain development. Molecular and Cellular Endocrinology 254-255, 154-162.
43. Grumbach, M.M., and Styne, D.M. (2003). Puberty: Ontogeny, neuroendocrinology, physiology, and disorders, in Williams Textbook of Endocrinology, Tenth Ed., eds. P.R. Larsen, H.M. Kronenberg, S. Melmed & K.S. Polonsky. (New York: Elsevier), 1115-1286.
44. Hare, T.A., Tottenham, N., Galvan, A., Voss, H.U., Glover, G.H., and Casey, B.J. (2008). Biological substrates of emotional reactivity and regulation in adolescence during an emotional Go-Nogo task. Biological Psychiatry 63, 927-934.
45. Hermans, E.J., Ramsey, N.F., and Van Honk, J. (2008). Exogenous testosterone enhances responsiveness to social threat in the neural circuitry of social aggression in humans. Biol Psychiatry 63, 263-270.
46. Herting, M.M., Maxwell, E.C., Irvine, C., and Nagel, B.J. (2011). The impact of sex, puberty, and hormones on white matter microstructure in adolescents. Cerebral Cortex doi: 10.1093/cercor/bhr246.
47. Jacobs, E., and D'esposito, M. (2011). Estrogen shapes dopamine-dependent cognitive processes: Implications for women's health. The Journal of Neuroscience 31, 5286-5293.
48. Joinson, C., Heron, J., Araya, R., Paus, T., Croudace, T., Rubin, M., Marcus, M., and Lewis, G. (2012). Association between pubertal development and depressive symptoms in girls from a UK cohort. Psychological Medicine 12, 1-11.
49. Ladouceur, C.D., Dahl, R.E., Williamson, D.E., Birmaher, B., Ryan, N.D., and Casey, B.J. (2005). Altered emotional processing in pediatric anxiety disorder, depression, and comorbid anxiety and depression. Journal of Abnormal Child Psychology 33, 165-177.
50. Ladouceur, C.D., Peper, J.S., and Dahl, R.E. (2012). White matter development in adolescence: The influence of puberty and implications for affective disorders. Developmental Cognitive Neuroscience 2, 34-56.
51. Ladouceur, C.D., Silk, J.S., Dahl, R.E., Ostapenko, L., Kronhaus, D., and Phillips, M.L. (2009). Fearful faces influence attentional control processes in anxious youth and adults. Emotion 9, 855-864.
52. Larson, R.W., and Asmussen, L. (1991). Anger, worry, and hurt in early adolescence: An enlarging world of negative emotions, in Adolescent stress: Causes and consequences, eds. M.E. Colten & S. Gore. (Hawthorne, NY: Aldine de Gruyter), 21-41.
53. Lenroot, R.K., and Giedd, J.N. (2010). Sex differences in the adolescent brain. Brain and Cognition 72, 46-55.
54. Lenroot, R.K., Gogtay, N., Greenstein, D.K., Wells, E.M., Wallace, G.L., Clasen, L.S., Blumenthal, J.D., Lerch, J., Zijdenbos, A.P., Evans, A.C., Thompson, P.M., and Giedd, J.N. (2007). Sexual dimorphism of brain development trajectories during childhood and adolescence. NeuroImage 36, 1065-1073.
55. Lewis, D.A. (1997). Development of the prefrontal cortex during adolescence: insights into vulnerable neural circuits in schizophrenia. Neuropsychopharmacology 16, 385-398.
56. Luna, B., Garver, K., Urban, T., Lazar, N., and Sweeney, J. (2004). Maturation of cognitive processes from late childhood to adulthood. Child Development 75, 1357-1372.
57. Manuck, S.B., Marsland, A.L., Flory, J.D., Gorka, A., Ferrell, R.E., and Hariri, A.R. (2010). Salivary testosterone and a trinucleotide (CAG) length polymorphism in the androgen receptor gene predict amygdala reactivity in men. Psychoneuroendocrinology 35, 94-104.
58. Marshall, W.A., and Tanner, J.M. (1969). Variations in pattern of pubertal changes in girls. Archives of Disease in Childhood 44, 291-303.
59. Marshall, W.A., and Tanner, J.M. (1970). Variations in the pattern of pubertal changes in boys. Archives of Disease in Childhood 45, 13-23.
60. Martin, C.A., Kelly, T.H., Rayens, M.K., Brogli, B.R., Brenzel, A., Smith, W.J., and Hatim, A.O. (2002). Sensation seeking, puberty, and nicotine, alcohol, and marijuana use in adolescence. Journal of the American Academic Child and Adolescent Psychiatry 41, 1495-1502.
61. Mayberg, H. (2001). Depression and Frontal-Subcortical Circuits: Focus on refrontal-Limbic Interactions, in Frontal-Subcortical Circuits in Psychiatric and Neurological Disorders, ed. D.G.C. Lichter, J.L. (New York: The Guilford Press), 177-206.
62. Mcclure, E.B., Monk, C.S., Nelson, E.E., Parrish, J.M., Adler, A.D., Blair, R.J., Fromm, S., Charney, D.S., Leibenluft, E., Ernst, M., and Pine, D.S. (2007). Abnormal attention modulation of fear circuit function in pediatric generalized anxiety disorder. Archives of General Psychiatry 64, 97-106.
63. Mehta, P.H., and Beer, J. (2010). Neural mechanisms of the testosterone-aggression relation: the role of orbito-frontal cortex. J Cogn Neurosci 22, 2357-2368.
64. Mendle, J., Harden, K.P., Brooks-Gunn, J., and Graber, J.A. (2010). Development's tortoise and hare: pubertal timing, pubertal tempo, and depressive symptoms in boys and girls. Developmental Psychology 46, 1341-1353.
65. Mendle, J., Harden, K.P., Brooks-Gunn, J., and Graber, J.A. (2012). Peer relationship and depressive symptomatology in boys at puberty. Developmental Psychology 48, 429-435.
66. Merikangas, K.R., Akiskal, H.S., Angst, J., Greenberg, P.E., Hirschfeld, R.M., Petukhova, M., and Kessler, R.C. (2007). Lifetime and 12-month prevalence of bipolar spectrum disorder in the National Comorbidity Survey replication. Archives of General Psychiatry 64, 543-552.
67. Monk, C.S., Klein, R.G., Telzer, E.H., Schroth, E.A., Mannuzza, S., Moulton Iii, J.L., Guardino, M., Mcclure-Tone, E.B., Fromm, S., Blair, J.R., Pine, D.S., and Ernst, M. (2008). Amygdala and nucleus accumbens activation to emotional facial expressions in children and adolescents at risk for major depression. American Journal of Psychiatry 165, 90-98.
68. Monk, C.S., Mcclure, E.B., Nelson, E.E., Zarahn, E., Bilder, R.M., Leibenluft, E., Charney, D.S., Ernst, M., and Pine, D.S. (2003). Adolescent immaturity in attention-related brain engagement to emotional facial expressions. Neuroimage 20, 420-428.
69. Moore Iii, W.E., Pfeifer, J.H., Masten, C.L., Mazziotta, J.C., Iacoboni, M., and Dapretto, M. (2012). Facing puberty: associations between pubertal development and neural responses to affective facial displays. Social Cognitive and Affective Neuroscience 7, 35-43.
70. Mueller, S.C. (2011). The influence of emotion on cognitive control: relevance for development and adolescent psychopathology. Frontiers in Psychology doi:10.3389/fpsyg.2011.00327.
71. Naftolin, F., and Malaspina, D. (2007). Estrogen, estrogen treatment and the post-reproductive woman's brain. Maturitas 20, 23-26.
72. Natsuaki, M.N., Klimes-Dougan, B., Ge, X., Shirtcliff, E.A., Hastings, P.D., and Zahn-Waxler, C. (2009). Early pubertal maturation and internalizing problems in adolescence: sex differences in the role of cortisol reactivity to interpersonal stress. Journal of Clinical Child and Adolescent Psychology 38, 513-524.
73. Nelson, E.E., Leibenluft, E., Mcclure, E., and Pine, D.S. (2005). The social-orientation of adolescence: A neuroscience perspective on the process and its relation to psychopathology. Psychol Med 35, 163-174.
74. Neufang, S., Specht, K., Hausmann, M., Gunturkun, O., Herpertz-Dahlmann, B., Fink, G.R., and Konrad, K. (2009). Sex differences and the impact of steroid hormones on the developing human brain. Cerebral Cortex 19, 464-473.
75. Op De Macks, Z.A., Moor, B.G., Overgaauw, S., Guroglu, B., Dahl, R.E., and Crone, E.A. (2011). Testosterone levels correspond with increased ventral striatum activation in response to monetary rewards in adolescents. Developmental Cognitive Neuroscience 1, 506-516.
76. Ozer, E.M., Macdonald, T., and Irwin, C.E., Jr. (2002). Adolescent health care in the United States: Implications and projections for the new millennium, in The changing adolescent experience: Societal trends and the transition to adulthood, eds. J.T. Mortimer & R.W. Larson. (New York: Cambridge University Press), 129-174.
77. Parker, L.N. (1991). Adrenarche. Endocrinology and Metabolism Clinics of America 20, 71-83.
78. Paus, T. (2010). Growth of white matter in the adolescent brain: myelin or axon? Brain and Cognition 72, 26-35.
79. Pavuluri, M.N., O'connor, M.M., Harral, E.M., and Sweeney, J.A. (2008). An fMRI study of the interface between affective and cognitive neural circuitry in pediatric bipolar disorder. Psychiatry Research 162, 244-255.
80. Peper, J.S., Brouwer, R.M., Schnack, H.G., Van Baal, G.C., Van Leeuwen, M., van den Berg, S.M., Delemarre-Van De Waal, H.A., Boomsma, D.I., Kahn, R.S., and Hulshoff Pol, H.E. (2009). Sex steroids and brain structure in pubertal boys and girls. Psychoneuroendocrinology 34, 332-342.
81. Peper, J.S., Brouwer, R.M., Schnack, H.G., Van Baal, G.C., Van Leeuwen, M., van den Berg, S.M., Delemarre-Van De Waal, H.A., Janke, A.L., Collins, D.L., Evans, A.C., Boomsma, D.I., Kahn, R.S., and Hulshoff Pol, H.E. (2008). Cerebral white matter in early puberty is associated with luteinizing hormone concentrations. Psychoneuroendocrinology 33, 909-915.
82. Peper, J.S., Pol, H.E.H., Crone, E.A., and Van Honk, J. (2011). Sex steroids and brain structure in pubertal boys and girls: a mini-review of neuroimaging studies. Neuroscience doi:10.1016/j.neuroscience.2011.02.014.
83. Perrin, J.S., Herve, P.Y., Leonard, G., Perron, M., Pike, G.B., Pitiot, A., Richer, L., Veillette, S., Pausova, Z., and Paus, T. (2008). Growth of white matter in the adolescent brain: role of testosterone and androgen receptor. Journal of Neuroscience 28, 9519-9524.
84. Phillips, M.L., Drevets, W.C., Rauch, S.L., and Lane, R. (2003). Neurobiology of emotion perception II: Implications for major psychiatric disorders. Biological Psychiatry 54, 15-528.
85. Phillips, M.L., Ladouceur, C.D., and Drevets, W.C. (2008). A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Molecular Psychiatry 13, 833-857.
86. Pine, D.S., Cohen, P., Gurley, D., Brook, J., and Ma, Y. (1998). The risk for early-adulthood anxiety and depressive disorders in adolescents with anxiety and depressive disorders. Archives of General Psychiatry 55, 56-64.
87. Price, J.L., and Drevets, W.C. (2010). Neurocircuitry of mood disorders. Neuropsychopharmacology 35, 192-216.
88. Raznahan, A., Lee, Y., Stidd, R., Long, R., Greenstein, D., Clasen, L., Addington, A., Gogtay, N., Rapoport, J.L., and Giedd, J.N. (2010). Longitudinally mapping the influence of sex and androgen signaling on the dynamics of human cortical maturation in adolescence. Proceedings of the National Academic of Sciences USA 107, 16988-16993.
89. Reyna, V.F., and Farley, F. (2006). Risk and rationality in adolescent decision making: Implications for theory, practice, and public policy. Psychological Science in the Public Interest 7, 1-44.
90. Sarkey, S., Azcoitia, I., Garcia-Segura, L.M., Garcia-Ovejero, D., and Doncarlos, L.L. (2008). Classical androgen receptors in non-classical sites in the brain. Hormones and Behavior 53, 753-764.
91. Savitz, J., and Drevets, W.C. (2009). Bipolar and major depressive disorder: Neuroimaging the developmental-degenerative divide. Neuroscience and Biobehavioral Reviews 33, 699-771.
92. Schulz, K.M., Molenda-Figueira, H., and Sisk, C. (2009). Back to the future: the organizational-activational hypothesis adapted to puberty and adolescence. Hormones and Behavior 55, 597-604.
93. Shirtcliff, E.A., Dahl, R.E., and Pollak, S.D. (2009). Pubertal development: correspondence between hormonal and physical development. Child Abuse and Neglect 80, 327-337.
94. Siegle, G.J., Steinhauer, S.R., and Thase, M.E. (2004). Pupillary assessment and computational modeling of the Stroop task in depression. International Journal of Psychophysiology 52, 63-76.
95. Silk, J.S., Davis, S., Mcmakin, D.L., Dahl, R.E., and Forbes, E.E. (2012a). Why do anxious children become depressed teenagers? The role of social evaluative threat and reward processing. Psychological Medicine 17, 1-13.
96. Silk, J.S., Siegle, G.J., Whalen, D.J., Ostapenko, L.J., Ladouceur, C.D., and Dahl, R.E. (2009). Pubertal changes in emotional information processing: Pupillary, behavioral, and subjective evidence during emotional work identification. Development and Psychopathology 21, 7-26.
97. Silk, J.S., Stroud, L.R., Siegle, G.J., Dahl, R.E., Lee, K.H., and Nelson, E.E. (2012b). Peer acceptance and rejection through the eyes of youth: pupillary, eyetracking and ecological data from the Chatroom Interact task. Social Cognitive and Affective Neuroscience 7, 93-105.
98. Simerly, R.B., Chang, C., Muramatsu, M., and Swanson, L.W. (1990). Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridation study. Journal of Comparative Neurology 294, 76-95.
99. Sisk, C.L., and Zehr, J.L. (2005). Pubertal hormones organize the adolescent brain and behavior. Frontiers in Neuroendocrinology 26, 163-174.
100. Smith, A.B., Halari, R., Giampetro, V., Brammer, M., and Rubia, K. (2011). Developmental effects of reward on sustained attention networks. Neuroimage 56, 1693-1704.
101. Sowell, E.R., Petersen, B.S., Thompson, P.M., Welcome, S.E., Henkenius, A.L., and Toga, A.W. (2003). Mapping cortical change across the human life span. Nature Neuroscience 6, 309-315.
102. Spear, L.P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews 24, 417-463.
103. Spear, L.P. (2010). The behavioral neuroscience of adolescence. New York: WW Norton & Company Inc.
104. Stanton, S.J., Wirth, M.M., Waugh, C.E., and Schultheiss, O.C. (2009). Endogenous testosterone levels are associated with amygdala and ventromedial prefrontal cortex responses to anger faces in men but not women. Biol Psychol 81, 118-122.
105. Steinberg, L. (2005). Cognitive and affective development in adolescence. Trends in Cognitive Sciences 9, 69-74.
106. Steinberg, L. (2007). Risk-taking in adolescence: New perspectives from brain and behavioral science. Current Directions in Psychological Science 16, 55-59.
107. Styne, D., and Grumbach, M. (2002). Puberty in boys and girls, in Hormones, brain, and behavior, eds. D. Pfaff, A. Arnold, A. Etgen, S. Fahrbach & R. Rubin. (San Francisco: Academic Press), 661-716.
108. Tottenham, N., Hare, T.A., and Casey, B.J. (2011). Behavioral assessment of emotion discrimination, emotion regulation, and cognitive control in childhood, adolescence, and adulthood. Frontiers in Psychology 2, doi:10.3389/fpsyg.2011.00039.
109. Van Wingen, G.A., Ossewaarde, L., Backstrom, T., Hermans, E.J., and Fernandez, G. (2011). Gonadal hormone regulation of the emotion circuitry in humans. Neuroscience 191.
110. Van Wingen, G.A., Zylicz, S.A., Pieters, S., Mattern, C., Verkes, R.J., Buitelaar, J.K., and Fernandez, G. (2010). Testosterone reduces amygdala-orbitofrontal cortex coupling. Psychoneuroendocrinology 35, 105-113.
111. Vermeersch, H., T'sjoen, T., Kaufman, J., and Vincke, J. (2008). The role of testosterone in aggressive and non-aggressive risk-taking behavior in adolescent boys. Hormones and Behavior 53, 463-471.
112. Volman, I., Toni, I., Verhagen, L., and Roelofs, K. (2011). Endogenous testosterone modulates prefrontal-amygdala connectivity during social emotional behavior. Cerebral Cortex 21, 2282-2290.
113. Wahlstrom, D., White, T., and Luciana, M. (2010). Neurobehavioral evidence for changes in dopamine system activity during adolescence. Neuroscience and Biobehavioral Reviews 34, 631-648.
114. Walf, A.A., and Frye, C.A. (2006). A review and update of mechanisms of estrogen in the hippocampus and amygdala for anxiety and depression behavior. Neuropsychopharmacology 31, 1097-1111.
115. Worthman, C. (1999). Epidemiology of human development, in Hormones, health, and behavior: A socio-ecological and lifespan perspectives, eds. C. Panter-Brick & C. Worthman. (New York: Cambridge University Press), 47-104.