Review: Magnetic resonance imaging of male/female differences in human adolescent brain anatomy

Biology of Sex Differences

Volumn 3, Issue 1, 2012, Pages

  Giedd, Jay N ^a   Raznahan, Armin ^a   Mills, Kathryn L ^a,c   Lenroot, Rhoshel K ^b  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Brain; Development; MRI; Sex differences

Indexed keywords

EID: 84872708573     PISSN: None     EISSN: 20426410     Source Type: Journal    
DOI: 10.1186/2042-6410-3-19     Document Type: Review

References (105)

1. Baron Cohen S, Lombardo M, Auyeung B, Ashwin E, Chakrabarti B, Knickmeyer R: Why are autism spectrum conditions more prevalent in males? PLoS Biology 2011, 9:e1001081-e1001081.
2. Kim Y, Leventhal B, Koh Y-J, Fombonne E, Laska E, Lim E-C, Cheon K-A, Kim S-J, Lee H, Song D-H, Grinker R: Prevalence of autism spectrum disorders in a total population sample. The American journal of psychiatry 2011, 168:904-912.
3. Munkvold LH, Lundervold AJ, Manger T: Oppositional defiant disordergender differences in co-occurring symptoms of mental health problems in a general population of children. Journal of abnormal child psychology 2011, 39:577-587.
4. Loeber R, Burke JD, Lahey BB, Winters A, Zera M: Oppositional defiant and conduct disorder: a review of the past 10 years, part I. J Am Acad Child Adolesc Psychiatry 2000, 39:1468-1484.
5. Novik TS, Hervas A, Ralston SJ, Dalsgaard S: Rodrigues Pereira R, Lorenzo MJ: Influence of gender on attention-deficit/hyperactivity disorder in Europe-ADORE. European child & adolescent psychiatry 2006, 15(Suppl 1): I15-24.
6. Scahill L, Schwab-Stone M: Epidemiology of ADHD in school-age children. Child and adolescent psychiatric clinics of North America 2000, 9:541-555. (Pubitemid 30620543)
7. Hayward C, Sanborn K: Puberty and the emergence of gender differences in psychopathology. J Adolesc Health 2002, 30:49-58. (Pubitemid 34275453)
8. Angold A, Costello E, Worthman C: Puberty and depression: the roles of age, pubertal status and pubertal timing. Psychological medicine 1998, 28:51-61. (Pubitemid 28043568)
9. Swanson SA, Crow SJ, Le Grange D, Swendsen J, Merikangas KR: Prevalence and correlates of eating disorders in adolescents. Results from the national comorbidity survey replication adolescent supplement. Arch Gen Psychiatry 2011, 68:714-723.
10. Currin L, Schmidt U, Treasure J, Jick H: Time trends in eating disorder incidence. Br J Psychiatry 2005, 186:132-135. (Pubitemid 40193782)
11. Halpern DF: Sex differences in cognitive abilities. 4th edition. New York: Psychology Press; 2012.
12. Dekaban AS: Tables of cranial and orbital measurements, cranial volume, and derived indexes in males and females from 7 days to 20 years of age. Ann Neurol 1977, 2:485-491. (Pubitemid 8401020)
13. Pakkenberg H, Voight J: Brain weight of the Danes. Acta Anat 1964, 56:604-606.
14. Witelson SF, Beresh H, Kigar DL: Intelligence and brain size in 100 postmortem brains: Sex, lateralization and age factors. Brain 2006, 129:386-398. (Pubitemid 43164363)
15. Andreasen NC, Flaum M, Swayze V, O'Leary DS, Alliger R, Cohen G, Ehrhardt J, Yuh WT: Intelligence and brain structure in normal individuals [see comments]. Am J Psychiatry 1993, 150:130-134. (Pubitemid 23059177)
16. Nopoulos P, Flaum M, O'Leary D, Andreasen NC: Sexual dimorphism in the human brain: evaluation of tissue volume, tissue composition and surface anatomy using magnetic resonance imaging. Psychiatry Res 2000, 98:1-13. (Pubitemid 30119884)
17. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RSJ: A voxel-based morphometric study of aging in 465 normal adult human brains. Neuro Image 2001, 14:21-36. (Pubitemid 32552740)
18. Allen JS, Damasio H, Grabowski TJ, Bruss J, Zhang W: Sexual dimorphism and asymmetries in the gray-white composition of the human cerebrum. Neuroimage 2003, 18:880-894. (Pubitemid 36513462)
19. Goldstein JM, Seidman LJ, Horton NJ, Makris N, Kennedy DN, Caviness VS Jr, Faraone SV, Tsuang MT: Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cereb Cortex 2011, 11:490-497.
20. Reiss AL, Abrams MT, Singer HS, Ross JL, Denckla MB: Brain development, gender and IQ in children. A volumetric imaging study. Brain 1996, 119:1763-1774. (Pubitemid 26375742)
21. Giedd JN, Castellanos FX, Rajapakse JC, Vaituzis AC, Rapoport JL: Sexual dimorphism of the developing human brain. Prog Neuropsychopharmacol Biol Psychiatry 1997, 21:1185-1201. (Pubitemid 28046695)
22. Jerison H: Evolution of the Brain and Intelligence. New York: Academic; 1973.
23. Lenroot RK, Gogtay N, Greenstein DK, Wells EM, Wallace GL, Clasen LS, Blumenthal JD, Lerch J, Zijdenbos AP, Evans AC, et al: Sexual dimorphism of brain developmental trajectories during childhood and adolescence. Neuroimage 2007, 36:1065-1073. (Pubitemid 47001725)
24. CDC: Centers for Disease Control and Prevention, National Center for Health Statistics. CDC growth charts: United States. In Book Centers for Disease Control and Prevention, National Center for Health Statistics. CDC growth charts: United States 2000. (Editor ed.eds.), May 30, 2000 edition. City; 2000.
25. Ho KC, Roessmann U, Straumfjord JV, Monroe G: Analysis of brain weight. I. Adult brain weight in relation to sex, age, and race. Arch Pathol Lab Med 1980, 104:635-639. (Pubitemid 11240928)
26. Ankney CD: Differences in brain size [letter; comment]. Nature 1992, 358:532.
27. O'Brien LM, Ziegler DA, Deutsch CK, Kennedy DN, Goldstein JM, Seidman LJ, Hodge S, Makris N, Caviness V, Frazier JA, Herbert MR: Adjustment for whole brain and cranial size in volumetric brain studies: A review of common adjustment factors and statistical methods. Harvard Review of Psychiatry 2006, 14:141-151. (Pubitemid 43995123)
28. Finlay BL, Darlington RB: Linked regularities in the development and evolution of mammalian brains. Science 1995, 268:1578-1584.
29. Zhang K, Sejnowski TJ: A universal scaling law between gray matter and white matter of cerebral cortex. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:5621-5626. (Pubitemid 30313768)
30. Gur RC, Gunning-Dixon F, Bilker WB, Gur RE: Sex differences in temporolimbic and frontal brain volumes of healthy adults. Cerebral Cortex 2002, 12:998-1003.
31. Leonard CM, Towler S, Welcome S, Halderman LK, Otto R, Eckert MA, Chiarello C: Size matters: Cerebral volume influences sex differences in neuroanatomy. Cerebral Cortex 2008, 18:2920-2931.
32. Brun CC, Lepore N, Luders E, Chou YY, Madsen SK, Toga AW, Thompson PM: Sex differences in brain structure in auditory and cingulate regions. Neuroreport 2009, 20:930-935.
33. Shaw P, Eckstrand K, Sharp W, Blumenthal J, Lerch JP, Greenstein D, Clasen L, Evans A, Giedd J, Rapoport JL: Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation. Proc Natl Acad Sci U S A 2007, 104:19649-19654.
34. Mackie S, Shaw P, Lenroot R, Pierson R, Greenstein DK, Nugent TF, Sharp WS, Giedd JN, Rapoport JL: Cerebellar development and clinical outcome in attention deficit hyperactivity disorder. American Journal of Psychiatry 2007, 164:647-655. (Pubitemid 46650197)
35. Paus T: Sex differences in the human brain: a developmental perspective. Prog Brain Res 2010, 186:13-28.
36. Raznahan A, Shaw P, Lalonde F, Stockman M, Wallace GL, Greenstein D, Clasen L, Gogtay N, Giedd JN: How does your cortex grow? The Journal of neuroscience: the official journal of the Society for Neuroscience 2011, 31:7174-7177.
37. Salat DH, Buckner RL, Snyder AZ, Greve DN, Desikan RSR, Busa E, Morris JC, Dale AM, Fischl B: Thinning of the cerebral cortex in aging. Cerebral Cortex 2004, 14:721-730. (Pubitemid 38856947)
38. O'Donnell S, Noseworthy MD, Levine B, Dennis M: Cortical thickness of the frontopolar area in typically developing children and adolescents. Neuroimage 2005, 24:948-954. (Pubitemid 40164496)
39. Luders E, Narr KL, Thompson PM, Rex DE, Woods RP, Deluca H, Jancke L, Toga AW: Gender effects on cortical thickness and the influence of scaling. Human brain mapping 2006, 27:314-324.
40. Sowell ER, Peterson BS, Kan E, Woods RP, Yoshii J, Bansal R, Xu D, Zhu H, Thompson PM, Toga AW: Sex differences in cortical thickness mapped in 176 healthy individuals between 7 and 87 years of age. Cereb Cortex 2007, 17:1550-1560.
41. Salinas J, Mills E, Conrad A, Koscik T, Andreasen N, Nopoulos P: Sex differences in parietal lobe structure and development. Gender Medicine 2012, 9:44-55.
42. Pakkenberg B, Gundersen HJ: Neocortical neuron number in humans: effect of sex and age. J Comp Neurol 1997, 384:312-320. (Pubitemid 27282046)
43. Luders E, Gaser C, Narr KL, Toga AW: Why sex matters: brain size independent differences in gray matter distributions between men and women. The Journal of neuroscience: the official journal of the Society for Neuroscience 2009, 29:14265-14270.
44. Filipek PA, Richelme C, Kennedy DN, Caviness VS Jr: The young adult human brain: an MRI-based morphometric analysis. Cereb Cortex 1994, 4:344-360. (Pubitemid 24228840)
45. Sowell ER, Trauner DA, Gamst A, Jernigan TL: Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study. Dev Med Child Neurol 2002, 44:4-16. (Pubitemid 34051455)
46. Giedd JN, Shaw P, Wallace G, Gogtay N, Lenroot RK: Anatomic brain imaging studies of normal and abnormal brain development in children and adolescents. In Developmental Psychopathology. Volume 2. 2nd edition. Edited by Cicchetti D, Cohen DJ. Hoboken, N.J: John Wiley & Sons; 2006:127-194.
47. Rijpkema M, Everaerd D, van der Pol C, Franke B, Tendolkar I, Fernndez G: Normal sexual dimorphism in the human basal ganglia. Human Brain Mapping 2012, 33:1246-1252.
48. Clark AS, MacLusky NJ, Goldman-Rakic PS: Androgen binding and metabolism in the cerebral cortex of the deveoping rhesus monkey. Endocrinology 1988, 123:932-940.
49. Morse JK, Scheff SW, DeKosky ST: Gonadal steroids influence axonal sprouting in the hippocampal dentate gyrus: a sexually dimorphic response. Experimental Neurology 1986, 94:649-658. (Pubitemid 17223467)
50. Wilke M: Krägeloh-Mann I, Holland SK: Global and local development of gray and white matter volume in normal children and adolescents. Experimental Brain Research 2007, 178:296-307. (Pubitemid 46440574)
51. Suzuki M, Hagino H, Nohara S, Zhou SY, Kawasaki Y, Takahashi T, Matsui M, Seto H, Ono T, Kurachi M: Male-specific volume expansion of the human hippocampus during adolescence. Cerebral Cortex 2005, 15:187-193. (Pubitemid 40111079)
52. Giedd JN, Vaituzis AC, Hamburger SD, Lange N, Rajapakse JC, Kaysen D, Vauss YC, Rapoport JL: Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: ages 4-18 years. J Comp Neurol 1996, 366:223-230. (Pubitemid 26070596)
53. Neufang S, Specht K, Hausmann M, Herpertz-Dahlmann B, G√̊nt√̊rk√̊n O, Fink GR, Konrad K: Sex differences and the impact of steroid hormones on the developing human brain. Cerebral Cortex 2009, 19:464-473.
54. Romeo RD, Waters E, McEwen B: Steroid-induced hippocampal synaptic plasticity: sex differences and similarities. NGB 2004, 1:11.
55. McEwen BS: Genome and hormones: gender differences in physiology. Journal of Applied Physiology 2001, 18:2785-2801.
56. Becker JB, Monteggia LM, Perrot-Sinal TS, Romeo RD, Taylor JR, Yehuda R, Bale TL: Stress and disease: is being female a predisposing factor? Journal of Neuroscience 2007, 27:11851-11855. (Pubitemid 350072096)
57. De Bellis MD, Keshavan MS, Beers SR, Hall J, Frustaci K, Masalehdan A, Noll J, Boring AM: Sex differences in brain maturation during childhood and adolescence. Cereb Cortex 2001, 11:552-557. (Pubitemid 32488382)
58. de Lacoste MC, Holloway RL, Woodward DJ: Sex differences in the fetal human corpus callosum. Human Neurobiology 1986, 5:93-96. (Pubitemid 16093814)
59. Witelson SF: Hand and Sex Differences in the Isthmus and Genu of the Human Corpus Callosum. Brain 1989, 112:799-835. (Pubitemid 19151171)
60. Sullivan EV, Rosenbloom MJ, Desmond JE, Pfefferbaum A: Sex differences in corpus callosum size: relationship to age and intracranial size. Neurobiology of Aging 2001, 22:603-611. (Pubitemid 32607745)
61. Luders E, Rex DE, Narr KL, Woods RP, Jancke L, Thompson PM, Mazziotta JC, Toga AW: Relationships between sulcal asymmetries and corpus callosum size: gender and handedness effects. Cereb Cortex 2003, 13:1084-1093. (Pubitemid 37163207)
62. Driesen NR, Raz N: The influence of sex, age, and handedness on corpuscallosum morphology-a meta-analysis. Psychobiology 1995, 23:240-247.
63. Bishop KM, Wahlsten D: Sex differences in the human corpus callosum: Myth or reality? Neuroscience And Biobehavioral Reviews 1997, 21:581-601. (Pubitemid 27458801)
64. Jancke L, Staiger JF, Schlaug G, Huang Y, Steinmetz H: The relationship between corpus callosum size and forebrain volume. Cereb Cortex 1997, 7:48-56. (Pubitemid 27081870)
65. Luders E, Toga AW: Sex differences in brain anatomy. Prog Brain Res 2010, 186:3-12.
66. Mori S, Zhang J: Principles of diffusion tensor imaging and its applications to Basic Neuroscience Research. Neuron 2006, 51:527-539. (Pubitemid 44301829)
67. Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, Chabriat H: Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 2001, 13:534-546. (Pubitemid 32231507)
68. Snook L, Paulson LA, Roy D, Phillips L, Beaulieu C: Diffusion tensor imaging of neurodevelopment in children and young adults. Neuroimage 2005, 26:1164-1173. (Pubitemid 40806495)
69. Barnea-Goraly N, Menon V, Eckert M, Tamm L, Bammer R, Karchemskiy A, Dant CC, Reiss AL: White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study. Cereb Cortex 2005, 15:1848-1854. (Pubitemid 41628326)
70. Mukherjee P, Miller JH, Shimony JS, Philip JV, Nehra D, Snyder AZ, Conturo TE, Neil JJ, McKinstry RC: Diffusion-tensor MR imaging of gray and white matter development during normal human brain maturation. AJNR Am J Neuroradiol 2002, 23:1445-1456. (Pubitemid 35154982)
71. Schmithorst VJ, Holland SK: Sex differences in the development of neuroanatomical functional connectivity underlying intelligence found using Bayesian connectivity analysis. Neuroimage 2007, 35:406-419. (Pubitemid 46240936)
72. Schmithorst VJ, Holland SK, Dardzinski BJ: Developmental differences in white matter architecture between boys and girls. Human Brain Mapping 2008, 29:696-710. (Pubitemid 351794124)
73. Bava S, Boucquey V, Goldenberg D, Thayer RE, Ward M, Jacobus J, Tapert SF: Sex differences in adolescent white matter architecture. Brain Research 2011, 1375:41-48.
74. Beaulieu C, Allen PS: Determinants of anisotropic water diffusion in nerves. Magnetic resonance in medicine 1994, 31:394-400. (Pubitemid 24108269)
75. Glenn O, Henry R, Berman J, Chang P, Miller S, Vigneron D, Barkovich AJ: DTI-based three-dimensional tractography detects differences in the pyramidal tracts of infants and children with congenital hemiparesis. Journal of Magnetic Resonance Imaging 2003, 18:641-648. (Pubitemid 37467264)
76. Song S-K, Sun S-W, Ramsbottom MJ, Chang C, Russell J, Cross AH: Dysmyelination Revealed through MRI as Increased Radial (but Unchanged Axial) Diffusion of Water. Neuroimage 2002, 17:1429-1436. (Pubitemid 35333862)
77. Song S-K, Sun S-W, Ju W-K, Lin S-J, Cross AH, Neufeld AH: Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 2003, 20:1714-1722. (Pubitemid 37468277)
78. Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, Armstrong RC: Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuro Image 2005, 26:132-140. (Pubitemid 40602893)
79. Herting MM, Maxwell EC, Irvine C, Nagel BJ: The Impact of Sex, Puberty, and Hormones on White Matter Microstructure in Adolescents. Cerebral Cortex 2011.
80. Menzler K, Belke M, Wehrmann E, Krakow K, Lengler U, Jansen A, Hamer HM, Oertel WH, Rosenow F, Knake S: Men and women are different: Diffusion tensor imaging reveals sexual dimorphism in the microstructure of the thalamus, corpus callosum and cingulum. Neuroimage 2011, 54(4):2557-2562.
81. Andersen BB, Korbo L, Pakkenberg B: A quantitative study of the human cerebellum with unbiased stereological techniques. Journal of Comparative Neurology 1992, 326:549-560. (Pubitemid 23001429)
82. Riva D, Giorgi C: The cerebellum contributes to higher functions during development: evidence from a series of children surgically treated for posterior fossa tumours. Brain 2000, 123(Pt 5):1051-1061. (Pubitemid 30224200)
83. Schmahmann JD: Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J Neuropsychiatry Clin Neurosci 2004, 16:367-378. (Pubitemid 39244566)
84. Tiemeier H, Lenroot RK, Greenstein DK, Tran L, Pierson R, Giedd JN: Cerebellum development during childhood and adolescence: a longitudinal morphometric MRI study. Neuroimage 2010, 49:63-70.
85. Sowell ER, Peterson BS, Kan E, Woods RP, Yoshii J, Bansal R, Xu D, Zhu H, Thompson PM, Toga AW: Sex differences in cortical thickness mapped in 176 healthy individuals between 7 and 87 years of age. Cerebral Cortex 2007, 17:1550-1560.
86. Lenroot RK, Giedd JN: Sex differences in the adolescent brain. Brain Cogn 2010, 72:46-55.
87. Raznahan A, Lee Y, Stidd R, Long R, Greenstein D, Clasen L, Addington A, Gogtay N, Rapoport JL, Giedd JN: Longitudinally mapping the influence of sex and androgen signaling on the dynamics of human cortical maturation in adolescence. Proc Natl Acad Sci U S A 2010, 107: 16988-16993.
88. Simerly RB, Chang C, Muramatsu M, Swanson LW: Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. Journal of Comparative Neurology 1990, 294:76-95. (Pubitemid 20104631)
89. Cameron JL: Effects of sex hormones on brain development. Handbook of Developmental Cognitive Neuroscience 2001, 1:59-78.
90. Guerriero G: Vertebrate sex steroid receptors: evolution, ligands, and neurodistribution. Ann N Y Acad Sci 2009, 1163:154-168.
91. Sarkey S, Azcoitia I, Garcia-Segura LM, Garcia-Ovejero D, DonCarlos LL: Classical androgen receptors in non-classical sites in the brain. Hormones and Behavior 2008, 53:753-764.
92. Weickert CS, Miranda-angulo AL, Wong J, Perlman WR, Ward SE, Radhakrishna V, Straub RE, Weinberger DR, Kleinman JE: Variants in the estrogen receptor alpha gene and its mRNA contribute to risk for schizophrenia. Human Molecular Genetics 2008, 17:2293-2309.
93. Weiser MJ, Foradori CD, Handa RJ: Estrogen receptor beta in the brain: from form to function. Brain Research Reviews 2008, 57:309-320. (Pubitemid 351381766)
94. Sugiyama N, Andersson S, Lathe R, Fan X, Alonso-Magdalena P, Schwend T, Nalvarte I, Warner M, Gustafsson JÖ: Spatiotemporal dynamics of the expression of estrogen receptors in the postnatal mouse brain. Molecular Psychiatry 2009, 14:223-232.
95. Garagorri J, Rodríguez G, Lario-Elboj Á, Olivares J, Lario-Muñoz Á, Orden I: Reference levels for 17- hydroxyprogesterone, 11-desoxycortisol, cortisol, testosterone, dehydroepiandrosterone sulfate and androstenedione in infants from birth to six months of age. European Journal of Pediatrics 2008, 167:647-653. (Pubitemid 351503500)
96. Garces C, de Oya I, Lopez-Simon L, Cano B, Schoppen S, Gil A, de Oya M: Hormone levels in 12-to 15-year-old boys and girls in Spain and their relationship with anthropometric variables. Clinical Biochemistry 2008, 41:621-624.
97. Lombardo M, Ashwin E, Auyeung B, Chakrabarti B, Taylor K, Hackett G, Bullmore E: Baron Cohen S: Fetal testosterone influences sexually dimorphic gray matter in the human brain. The Journal of neuroscience 2012, 32:674-680.
98. Perrin JS, Hervé PY, Leonard G, Perron M, Pike GB, Pitiot A, Richer L, Veillette S, Pausova Z, Paus T: Growth of white matter in the adolescent brain: Role of testosterone and androgen receptor. Journal of Neuroscience 2008, 28:9519-9524.
99. Peper JS, Brouwer RM, Schnack HG, van Baal GCM, van Leeuwen M, van den Berg SM, de Waal HA D-V, Janke AL, Collins DL, Evans AC, et al: Cerebral white matter in early puberty is associated with luteinizing hormone concentrations. Psychoneuroendocrinology 2008, 33:909-915.
100. Peper JS, Brouwer RM, Schnack HG, van Baal GC, van Leeuwen M, van den Berg SM, de Waal HA D-V, Boomsma DI, Kahn RS, Hulshoff Pol HE: Sex steroids and brain structure in pubertal boys and girls. Psychoneuroendocrinology 2009, 34:332-342.
101. Peper JS, Schnack HG, Brouwer RM, Van Baal GC, Pjetri E, Szekely E, van Leeuwen M, van den Berg SM, Collins DL, Evans AC, et al: Heritability of regional and global brain structure at the onset of puberty: a magnetic resonance imaging study in 9-year-old twin pairs. Hum Brain Mapp 2009, 30:2184-2196.
102. Benes FM, Turtle M, Khan Y, Farol P: Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. Archives of General Psychiatry 1994, 51: 477-484. (Pubitemid 24180494)
103. Im K, Lee JM, Lyttelton O, Kim SH, Evans AC, Kim SI: Brain size and cortical structure in the adult human brain. Cerebral Cortex 2008, 18:2181-2191.
104. Dahl RE: Adolescent brain development: a period of vulnerabilities and opportunities. Keynote address. Ann N Y Acad Sci 2004, 1021:1-22. (Pubitemid 38879605)
105. Casey BJ, Jones RM, Hare TA: The adolescent brain. Ann N Y Acad Sci 2008, 1124:111-126. (Pubitemid 351506787)