Risky decision-making in adolescent girls: The role of pubertal hormones and reward circuitry

Psychoneuroendocrinology

Volumn 74, Issue , 2016, Pages 77-91

  Op de Macks, Zdeňa A ^a   Bunge, Silvia A ^a   Bell, Orly N ^a   Wilbrecht, Linda ^a   Kriegsfeld, Lance J ^a   Kayser, Andrew S ^b,c   Dahl, Ronald E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VA NORTHERN CALIFORNIA HEALTH CARE SYSTEM   (United States)

Author keywords

Estradiol; fMRI; Nucleus accumbens; Orbitofrontal cortex; Puberty; Testosterone

Indexed keywords

ESTRADIOL; TESTOSTERONE;

ADOLESCENT; ADOLESCENT BEHAVIOR; ARTICLE; CONTROLLED STUDY; DECISION MAKING; ELECTROENCEPHALOGRAPHY; ESTRADIOL BLOOD LEVEL; FEEDBACK SYSTEM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; GLOBUS PALLIDUS; HIGH RISK BEHAVIOR; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; MEDIAL ORBITOFRONTAL CORTEX; MENSTRUAL CYCLE; NORMAL HUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROBABILITY; PROPENSITY SCORE; PUBERTY; REWARD; TESTOSTERONE BLOOD LEVEL; WECHSLER INTELLIGENCE SCALE; CHILD; CHILD BEHAVIOR; DIAGNOSTIC IMAGING; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PREFRONTAL CORTEX;

ADOLESCENT; ADOLESCENT BEHAVIOR; CHILD; CHILD BEHAVIOR; DECISION MAKING; ESTRADIOL; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PUBERTY; REWARD; RISK-TAKING; TESTOSTERONE;

EID: 84984856981     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2016.08.013     Document Type: Article

References (63)

1. Achenbach, T.M., Manual for the Child Behavior Checklist/4-18 and 1991 Profile. 1991, University of Vermont, Department of Psychiatry, Burlington (Vermont).
2. Balleine, B.W., Delgado, M.R., Hikosaka, O., The role of the dorsal striatum in reward and decision-making. J. Neurosci. 27 (2007), 8161–8165, 10.1523/JNEUROSCI.1554-07.2007.
3. Biro, F.M., Pinney, S.M., Huang, B., Baker, E.R., Chandler, D.W., Dorn, L.D., Hormone changes in peripubertal girls. J. Clin. Endocrinol. Metabol. 99 (2014), 3829–3835, 10.1210/jc.2013-4528.
4. Bjork, J.M., Knutson, B., Fong, G.W., Caggiano, D.M., Bennett, S.M., Hommer, D.W., Incentive-elicited brain activation in adolescents: similarities and differences from young adults. J. Neurosci. 24 (2004), 1793–1802, 10.1523/JNEUROSCI.4862-03.2004.
5. Bjork, J.M., Smith, A.R., Chen, G., Hommer, D.W., Adolescents, adults and rewards: comparing motivational neurocircuitry recruitment using fMRI. PLoS One, 5, 2010, e11440, 10.1371/journal.pone.0011440.
6. Braams, B.R., Van Duijvenvoorde, A.C.K., Peper, J.S., Crone, E.A., Longitudinal changes in adolescent risk-taking: a comprehensive study of neural responses to rewards, pubertal development and risk-taking behavior. J. Neurosci. 35 (2015), 7226–7238, 10.1523/JNEUROSCI.4764-14.2015.
7. Brett, M.C., Anton, J.L., Valabregue, R., Poline, J.B., Region of interest analysis using an SPM toolbox. NeuroImage, 16, 2002, 497.
8. Chick, C.F., Reward processing in the adolescent brain: individual differences and relation to risk taking. J. Neurosci. 35:40 (2015), 13539–13541, 10.1523/JNEUROSCI.2571-15.2015.
9. Crone, E.A., Dahl, R.E., Understanding adolescence as a period of social-affective engagement and goal flexibility. Nat. Rev. Neurosci. 13 (2012), 636–650, 10.1038/nrn3313.
10. Crone, E.A., Elzinga, B.M., Changing brains: how longitudinal functional magnetic resonance imaging studies can inform us about cognitive and social-affective growth trajectories. WIREs Cogn. Sci. 6 (2015), 53–63, 10.1002/wcs.1327.
11. Crone, E.A., The role of the medial frontal cortex in the development of cognitive and social-affective performance monitoring. Psychophysiology 51 (2014), 943–950, 10.1111/psyp.12252.
12. Dahl, R.E., Adolescent brain development: a period of vulnerabilities and opportunities. Ann. N. Y. Acad. Sci. 1021 (2004), 1–22, 10.1196/annals.1308.001.
13. De Water, E., Braams, B.R., Crone, E.A., Peper, J.S., Pubertal maturation and sex steroids are related to alcohol use in adolescents. Horm. Behav. 63 (2013), 392–397, 10.1016/j.yhbeh.2012.11.018.
14. Delgado, M.R., Reward-related responses in the human striatum. Ann. N. Y. Acad. Sci. 1104 (2007), 70–88.
15. Diekhof, E.K., Falkai, P., Gruber, O., The orbitofrontal cortex and its role in the assignment of behavioural significance. Neuropsychologia 49:5 (2012), 984–991, 10.1016/j.neuropsychologia.2011.01.032.
16. Dorn, L.D., Dahl, R.E., Woodward, H.R., Biro, F., Defining the boundaries of early adolescence: a user's guide to assessing pubertal status and pubertal timing in research with adolescents. Appl. Dev. Sci. 10 (2006), 37–41, 10.1207/s1532480xads1001.
17. Dreher, J.C., Schmidt, P.J., Kohn, P., Furman, D., Rubinow, D., Berman, K.F., Menstrual cycle phase modulates reward-related neural function in women. Proc. Natl. Acad. Sci. U. S. A. 104:7 (2007), 2465–2470.
18. Forbes, E.E., Dahl, R.E., Pubertal development and behavior: hormonal activation of social and motivational tendencies. Brain Cogn. 72 (2010), 66–72.
19. Forbes, E.E., Ryan, N.D., Phillips, M.L., Manuck, S.B., Worthman, C.M., Moyles, D.L., Dahl, R.E., Healthy adolescents’ neural response to reward: associations with puberty, positive affect, and depressive symptoms. J. Am. Acad. Child Adolesc. Psychiatry 49 (2010), 162–172.
20. Galvan, A., Adolescent development of the reward system. Front. Hum. Neurosci. 4 (2010), 1–9, 10.3389/neuro.09.006.2010.
21. Goddings, A.L., Mills, K.L., Clasen, L.S., Giedd, J.N., Viner, R.M., Blakemore, S.J., The influence of puberty on subcortical brain development. NeuroImage 88 (2014), 242–251, 10.1016/j.neuroimage.2013.09.073.
22. Haber, S.N., Knutson, B., The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35 (2010), 4–26, 10.1038/npp.2009.129.
23. Harden, K.P., Mann, F.D., Biological risk for the development of adolescent externalizing: integrating insights from behavioral genetics and neuroscience. Child Dev. Perspect. 9 (2015), 211–216, 10.1111/cdep.12135.
24. Hayes, A.F., An index and test of linear moderated mediation. Multivar. Behav. Res. 50:1 (2015), 1–22, 10.1080/00273171.2014.962683.
25. Hermans, E.J., Bos, P.A., Ossewaarde, L., Ramsey, N.F., Fernández, G., Van Honk, J., Effects of exogenous testosterone on the ventral striatal BOLD response during reward anticipation in healthy women. NeuroImage 52 (2010), 277–283.
26. Herting, M.M., Maxwell, E.C., Irvine, C., Nagel, B.J., The impact of sex, puberty, and hormones on white matter microstructure in adolescents. Cereb. Cortex 22:9 (2011), 1979–1992, 10.1093/cercor/bhr246.
27. Herting, M.M., Gautam, P., Spielberg, J.M., Kan, E., Dahl, R.E., Sowell, E.R., The role of testosterone and estradiol in brain volume changes across adolescence: a longitudinal structural MRI study. Hum. Brain Mapp. 35 (2014), 5633–5645, 10.1002/hbm.22575.
28. Kayser, A.S., Op de Macks, Z.A., Dahl, R.E., Frank, M.J., A neural correlate of exploratory behavior in early adolescence. J. Cogn. Neurosci. 28:2 (2016), 199–209, 10.1162/jocn_a_00896.
29. Koenis, M.M.G., Brouwer, R.M., van Baal, G.C.M., van Soelen, I.L.C., Peper, J.S., van Leeuwen, M., Delemarre-van de Waal, H.A., Boomsma, D.I., Hulshoff Pol, H.E., Longitudinal study of hormonal and physical development in young twins. J. Clin. Endocrinol. Metab. 98:3 (2013), E518–E527.
30. Koolschijn, P.C.M.P., Peper, J.S., Crone, E.A., The influence of sex steroids on structural brain maturation in adolescence. PLoS One, 9, 2014, e83929, 10.1371/journal.pone.0083929.
31. Lamm, C., Benson, B.E., Guyer, A.E., Perez-Edgar, K., Fox, N.A., Pine, D.S., Ernst, M., Longitudinal study of striatal activation to reward and loss anticipation from mid-adolescence into late adolescence/early adulthood. Brain Cogn. 89 (2014), 51–60, 10.1016/j.bandc.2013.12.003.
32. Leotti, L.A., Delgado, M.R., The value of exercising control over monetary gains and losses. Psychol. Sci. 25 (2014), 596–604, 10.1177/0956797613514589.
33. Levy, D.J., Glimcher, P.W., The root of all value: a neural common currency for choice. Curr. Opin. Neurobiol. 22 (2012), 1027–1038, 10.1016/j.conb.2012.06.001.
34. Liening, S.H., Stanton, S.J., Saini, E.K., Schultheiss, O.C., Salivary testosterone, cortisol, and progesterone: two-week stability, interhormone correlations, and effects of time of day, menstrual cycle, and oral contraceptive use on steroid hormone levels. Physiol. Behav. 99 (2010), 8–16, 10.1016/j.physbeh.2009.10.001.
35. Mazaika, P., Hoeft, F., Glover, G.H., Reiss, A.L., Methods and software for fMRI analysis for clinical subjects. Poster Presentation at the Ann. Hum. Brain Mapp. Meeting, San Francisco, CA, USA, 2009.
36. O'Doherty, J.P., Lights, camembert, action! The role of human orbitofrontal cortex in encoding stimuli, rewards, and choices. Ann. N. Y. Acad. Sci. 1121 (2007), 254–272.
37. Op de Macks, Z.A., Gunther Moor, B., Overgaauw, S., Güroğlu, B., Dahl, R.E., Crone, E.A., Testosterone levels correspond with increased ventral striatum activation in response to monetary rewards in adolescents. Dev. Cogn. Neurosci. 1 (2011), 506–516, 10.1016/j.dcn.2011.06.003.
38. Op de Macks, Z.A., Bunge, S.A., Bell, O.N., Kriegsfeld, L.J., Kayser, A.S., Dahl, R.E., under review. The effect of social rank feedback on risk taking and associated reward processes in adolescent girls.
39. Ostatníková, D., Pastor, K., Putz, Z., Dohnányiová, M., Mat'ašeje, A., Hamp, R., 2002. Salivary testosterone levels in preadolescent children. BMC Pediatrics: www.biomedcentral.com/1471-2431/2/5.
40. Peper, J.S., Dahl, R.E., The teenage brain: surging hormones-brain-behavior interactions during puberty. Curr. Dir. Psychol. Sci. 22 (2013), 134–139, 10.1177/0963721412473755.
41. Peper, J.S., Hulshoff Pol, H.E., Crone, E.A., Van Honk, J., Sex steroids and brain structure in pubertal boys and girls: a mini-review of neuroimaging studies. Neuroscience 191 (2011), 28–37, 10.1016/j.neuroscience.2011.02.014.
42. Peper, J.S., Koolschijn, P.C., Crone, E.A., Development of risk taking: contributions from adolescent testosterone and the orbito-frontal cortex. J. Cogn. Neurosci. 25 (2013), 2141–2150, 10.1162/jocn_a_00445.
43. Peters, J., Büchel, C., Neural representations of subjective reward value. Behav. Brain Res. 213 (2010), 135–141, 10.1016/j.bbr.2010.04.031.
44. Petersen, A.C., Crockett, L., Richards, M., Boxer, A., A self-report measure of pubertal status: reliability, validity, and initial norms. J. Youth Adolesc. 17 (1988), 117–133, 10.1007/BF01537962.
45. Schulz, K.M., Molenda-Figueira, H.A., Sisk, C.L., Back to the future: the organizational-activational hypothesis adapted to puberty and adolescence. Horm. Behav. 55 (2009), 597–604, 10.1016/j.yhbeh.2009.03.010.
46. Sescousse, G., Caldú, X., Segura, B., Dreher, J.C., Processing of primary and secondary rewards: a quantitative meta-analysis and review of human functional neuroimaging studies. Neurosci. Biobehav. Rev. 37 (2013), 681–696, 10.1016/j.neubiorev.2013.02.002.
47. Shirtcliff, E.A., Granger, D.A., Schwartz, E., Curran, M.J., Use of salivary biomarkers in biobehavioral research: cotton-based sample collection methods can interfere with salivary immunoassay results. Psychoneuroendocrinology 26 (2001), 165–173.
48. Shirtcliff, E.A., Dahl, R.E., Pollak, S.D., Pubertal development: correspondence between hormonal and physical development. Child Dev. 80 (2009), 327–337, 10.1111/j.1467-8624.2009.01263.x.
49. Shulman, E.P., Cauffman, E., Deciding in the dark: age differences in intuitive risk judgement. Dev. Psychol. 50:1 (2014), 167–177, 10.1037/a0032778.
50. Shulman, E.P., Harden, K.P., Chein, J.M., Steinberg, L., Sex differences in the developmental trajectories of impulse control and sensation-seeking from early adolescence to early adulthood. J. Youth Adolesc. 44 (2015), 1–17, 10.1007/s10964-014-0116-9.
51. Somerville, L.H., Jones, R.M., Casey, B.J., A time of change: behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues. Brain Cogn. 72 (2010), 124–133, 10.1016/j.bandc.2009.07.003.
52. Steinberg, L., Graham, S., O'Brien, L., Woolard, J., Cauffman, E., Banich, M., Age differences in future orientation and delay discounting. Child Dev. 80 (2009), 28–44.
53. Steinberg, L., A dual systems model of adolescent risk-taking. Dev. Psychobiol. 52 (2010), 216–224, 10.1002/dev.20445.
54. Thomas, J., Météreau, E., Déchaud, H., Pugeat, M., Dreher, J.C., Hormonal treatment increases the responseof the reward system at the menopausetransition: a counterbalanced randomized placebo-controlled fMRI study. Psychoneuroendocrinology 50 (2014), 167–180, 10.1016/j.psyneuen.2014.08.012.
55. Tivis, L.J., Richardson, M.D., Peddi, E., Arjmandi, B., Saliva versus serum estradiol: implications for research studies using postmenopausal women. Prog. Neuropsychopharmacol. Biol. Psychiatry. 29:5 (2005), 727–732.
56. Van Duijvenvoorde, A.C.K., Op de Macks, Z.A., Overgaauw, S., Gunther Moor, B., Dahl, R.E., Crone, E.A., A cross-sectional and longitudinal analysis of reward-related brain activation: effects of age, pubertal stage, and reward sensitivity. Brain Cogn. 89 (2014), 3–14, 10.1016/j.bandc.2013.10.005.
57. Van Leijenhorst, L., Westenberg, P.M., Crone, E.A., A developmental study of risky decisions on the cake gambling task: age and gender analyses of probability estimation and reward evaluation. Dev. Neuropsychol. 33:2 (2008), 179–196, 10.1080/87565640701884287.
58. Van Leijenhorst, L., Gunther Moor, B., Op de Macks, Z.A., Rombouts, S.A.R.B., Westenberg, P.M., Crone, E.A., Adolescent risky decision-making: neurocognitive development of reward and control regions. Neuroimage 51 (2010), 345–355, 10.1016/j.neuroimage.2010.02.038.
59. Van Wingen, G.A., Ossewaarde, L., Bäckström, T., Hermans, E.J., Fernández, G., Gonadal hormone regulation of the emotion circuitry in humans. Neuroscience 191 (2011), 38–45, 10.1016/j.neuroscience.2011.04.042.
60. Vermeersch, H., T'sjoen, G., Kaufman, J.M., Vincke, J., Estradiol, testosterone, differential association and aggressive and non-aggressive risk-taking in adolescent girls. Psychoneuroendocrinology 33 (2008), 897–908, 10.1016/j.psyneuen.2008.03.016.
61. Vermeersch, H., T'sjoen, G., Kaufman, J.M., Vincke, J., The role of testosterone in aggressive and non-aggressive risk-taking in adolescent boys. Horm. Behav. 53 (2008), 463–471, 10.1016/j.yhbeh.2007.11.021.
62. Wallis, J.D., Orbitofrontal cortex and its contribution to decision-making. Ann. Rev. Neurosci. 30 (2007), 31–56, 10.1146/annurev.neuro.30.051606.094334.
63. Wechsler, D., Manual for the Wechsler Intelligence Scale for Children. 3rd ed., 1991, The Psychological Corporation, San Antonio (TX).