Regional brain volume reductions relate to facial dysmorphology and neurocognitive function in fetal alcohol spectrum disorders

Human Brain Mapping

Volumn 33, Issue 4, 2012, Pages 920-937

  Roussotte, Florence F ^a,b   Sulik, Kathleen K ^c   Mattson, Sarah N ^d   Riley, Edward P ^d   Jones, Kenneth L ^e   Adnams, Colleen M ^f   May, Philip A ^g   O'Connor, Mary J ^a   Narr, Katherine L ^a   Sowell, Elizabeth R ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d SAN DIEGO STATE UNIVERSITY   (United States)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^f UNIVERSITY OF CAPE TOWN   (South Africa)

^g UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

Brain development; Developmental defects; Facial abnormalities; Prenatal alcohol exposure; Teratogenic effects of alcohol

Indexed keywords

ADOLESCENT; ALCOHOL CONSUMPTION; AMYGDALOID NUCLEUS; ARTICLE; BASAL GANGLION; BRAIN SIZE; CAUDATE NUCLEUS; CHILD; COGNITION; CORRELATIONAL STUDY; DIENCEPHALON; FACE DYSMORPHIA; FEMALE; FETAL ALCOHOL SYNDROME; FIRST TRIMESTER PREGNANCY; GLOBUS PALLIDUS; GRAY MATTER; HIPPOCAMPUS; HUMAN; INTELLIGENCE QUOTIENT; LEFT HEMISPHERE; MAJOR CLINICAL STUDY; MALE; MATERNAL BEHAVIOR; MULTICENTER STUDY; PALPEBRAL FISSURE; PHILTRUM; PRENATAL EXPOSURE; PRIORITY JOURNAL; PUTAMEN; RIGHT HEMISPHERE; SCHOOL CHILD; SOUTH AFRICA; THALAMUS; WHITE MATTER;

ADOLESCENT; BRAIN; CHILD; FACE; FEMALE; FETAL ALCOHOL SYNDROME; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; INTELLECTUAL DISABILITY; INTELLIGENCE TESTS; MAGNETIC RESONANCE IMAGING; MALE; MICROCEPHALY; PREGNANCY;

EID: 84858162583     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.21260     Document Type: Article

References (90)

1. Adnams CM, Kodituwakku PW, Hay A, Molteno CD, Viljoen D, May PA (2001): Patterns of cognitive-motor development in children with fetal alcohol syndrome from a community in South Africa. Alcohol Clin Exp Res 25: 557-562.
2. Adnams CM, Sorour P, Kalberg WO, Kodituwakku P, Perold MD, Kotze A, September S, Castle B, Gossage J, May PA (2007): Language and literacy outcomes from a pilot intervention study for children with fetal alcohol spectrum disorders in South Africa. Alcohol 41: 403-414.
3. Aragon AS, Coriale G, Fiorentino D, Kalberg WO, Buckley D, Gossage JP, Ceccanti M, Mitchell ER, May PA (2008a): Neuropsychological characteristics of Italian children with fetal alcohol spectrum disorders. Alcohol Clin Exp Res 32: 1909-1919.
4. Aragon AS, Kalberg WO, Buckley D, Barela-Scott LM, Tabachnick BG, May PA (2008b): Neuropsychological study of FASD in a sample of American Indian children: processing simple versus complex information. Alcohol Clin Exp Res 32: 2136-2148.
5. Archibald SL, Fennema-Notestine C, Gamst A, Riley EP, Mattson SN, Jernigan TL (2001): Brain dysmorphology in individuals with severe prenatal alcohol exposure. Dev Med Child Neurol 43: 148-154.
6. Astley SJ, Clarren SK (2000): Diagnosing the full spectrum of fetal alcohol-exposed individuals: Introducing the 4-digit diagnostic code. Alcohol Alcohol 35: 400-410.
7. Astley SJ, Clarren SK (2001): Measuring the facial phenotype of individuals with prenatal alcohol exposure: Correlations with brain dysfunction. Alcohol Alcohol 36: 147-159.
8. Astley SJ, Magnuson SI, Omnell LM, Clarren SK (1999): Fetal alcohol syndrome: Changes in craniofacial form with age, cognition, and timing of ethanol exposure in the macaque. Teratology 59: 163-172.
9. Astley SJ, Aylward EH, Carmichael Olson H, Kerns K, Brooks A, Coggins TE, Davies J, Dorn S, Gendler B, Jirikowic T, Kraegel P, Maravilla K, Richards T. (2009a): Functional magnetic resonance imaging outcomes from a comprehensive magnetic resonance study of children with fetal alcohol spectrum disorders. J Neurodev Disord 1: 61-80.
10. Astley SJ, Richards T, Aylward EH, Olson HC, Kerns K, Brooks A, Coggins TE, Davies J, Dorn S, Gendler B, Jirikowic T, Kraegel P, Maravilla K. (2009b): Magnetic resonance spectroscopy outcomes from a comprehensive magnetic resonance study of children with fetal alcohol spectrum disorders. Magn Reson Imaging 27: 760-778.
11. Astley SJ, Aylward EH, Olson HC, Kerns K, Brooks A, Coggins TE, Davies J, Dorn S, Gendler B, Jirikowic T, Kraegel P, Maravilla K, Richards T (2009c): Magnetic resonance imaging outcomes from a comprehensive magnetic resonance study of children with fetal alcohol spectrum disorders. Alcohol Clin Exp Res 33: 1671-1689.
12. Bookstein FL, Sampson PD, Streissguth AP, Connor PD (2001): Geometric morphometrics of corpus callosum and subcortical structures in the fetal-alcohol-affected brain. Teratology 64: 4-32.
13. Buerger AA, Gross CG, Rocha-Miranda CE (1974): Effects of ventral putamen lesions on discrimination learning by monkeys. J Comp Physiol Psychol 86: 440-446.
14. Burden MJ, Jacobson SW, Jacobson JL (2005): Relation of prenatal alcohol exposure to cognitive processing speed and efficiency in childhood. Alcohol Clin Exp Res 29: 1473-1483.
15. Cortese BM, Moore GJ, Bailey BA, Jacobson SW, Delaney-Black V, Hannigan JH (2006): Magnetic resonance and spectroscopic imaging in prenatal alcohol-exposed children: preliminary findings in the caudate nucleus. Neurotoxicol Teratol 28: 597-606.
16. Dale AM, Fischl B, Sereno MI (1999): Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage 9: 179-194.
17. Deacon TW, Pakzaban P, Isacson O (1994): The lateral ganglionic eminence is the origin of cells committed to striatal phenotypes: Neural transplantation and developmental evidence. Brain Res 668: 211-219.
18. Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ. (2006): An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31: 968-980.
19. Dinov ID, Van Horn JD, Lozev KM, Magsipoc R, Petrosyan P, Liu Z, Mackenzie-Graham A, Eggert P, Parker DS, Toga AW (2009): Efficient, distributed and interactive neuroimaging data analysis using the LONI pipeline. Front Neuroinformatics 3: 22.
20. Dodge NC, Jacobson JL, Molteno CD, Meintjes EM, Bangalore S, Diwadkar V, Hoyme EH, Robinson LK, Khaole N, Avison MJ, Jacobson SW. (2009): Prenatal alcohol exposure and interhemispheric transfer of tactile information: Detroit and Cape Town findings. Alcohol Clin Exp Res 33: 1628-1637.
21. Ell SW, Marchant NL, Ivry RB (2006): Focal putamen lesions impair learning in rule-based, but not information-integration categorization tasks. Neuropsychologia 44: 1737-1751.
22. Fagerlund A, Heikkinen S, Autti-Ramo I, Korkman M, Timonen M, Kuusi T, Riley EP, Lundbom N (2006): Brain metabolic alterations in adolescents and young adults with fetal alcohol spectrum disorders. Alcohol Clin Exp Res 30: 2097-2104.
23. Falk DE, Yi HY, Hiller-Sturmhofel S (2006): An epidemiologic analysis of co-occurring alcohol and tobacco use and disorders: findings from the National Epidemiologic Survey on alcohol and related conditions. Alcohol Res Health 29: 162-171.
24. Fischl B, Sereno MI, Dale AM. (1999): Cortical surface-based analysis. II. Inflation, flattening, and a surface-based coordinate system. NeuroImage 9: 195-207.
25. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002): Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron 33: 341-355.
26. Fischl B, van der Kouwe A, Destrieux C, Halgren E, Segonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D, Caviness V, Makris N, Rosen B, Dale AM. (2004): Automatically parcellating the human cerebral cortex. Cereb Cortex 14: 11-22.
27. Flandin P, Kimura S, Rubenstein JL (2010): The progenitor zone of the ventral medial ganglionic eminence requires Nkx2-1 to generate most of the globus pallidus but few neocortical interneurons. J Neurosci 30: 2812-2823.
28. Fryer SL, Tapert SF, Mattson SN, Paulus MP, Spadoni AD, Riley EP (2007): Prenatal alcohol exposure affects frontal-striatal BOLD response during inhibitory control. Alcohol Clin Exp Res 31: 1415-1424.
29. Fryer SL, Schweinsburg BC, Bjorkquist OA, Frank LR, Mattson SN, Spadoni AD, Riley EP (2009): Characterization of white matter microstructure in fetal alcohol spectrum disorders. Alcohol Clin Exp Res 33: 514-521.
30. Godin EA, O'Leary-Moore SK, Khan AA, Parnell SE, Ament JJ, Dehart DB, Johnson BW, Allan Johnson G, Styner MA, Sulik KK (2010): Magnetic resonance microscopy defines ethanol-induced brain abnormalities in prenatal mice: Effects of acute insult on gestational day 7. Alcohol Clin Exp Res 34: 98-111.
31. Hannigan JH, Chiodo LM, Sokol RJ, Janisse J, Ager JW, Greenwald MK, Delaney-Black V (2009): A 14-year retrospective maternal report of alcohol consumption in pregnancy predicts pregnancy and teen outcomes. Alcohol 44: 583-594.
32. Hoyme HE, May PA, Kalberg WO, Kodituwakku P, Gossage JP, Trujillo PM, Buckley DG, Miller JH, Aragon AS, Khaole N, Viljoen DL, Jones KL, Robinson LK. (2005): A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: Clarification of the 1996 institute of medicine criteria. Pediatrics 115: 39-47.
33. Jernigan TL, Trauner DA, Hesselink JR, Tallal PA (1991): Maturation of human cerebrum observed in vivo during adolescence. Brain 114(Part 5): 2037-2049.
34. Jones KL, Smith DW (1973): Recognition of the fetal alcohol syndrome in early infancy. Lancet 302: 999-1001.
35. Jones KL, Smith DW (1975): The fetal alcohol syndrome. Teratology 12: 1-10.
36. Jones KL, Robinson LK, Bakhireva LN, Marintcheva G, Storojev V, Strahova A, Sergeevskaya S, Budantseva S, Mattson SN, Riley EP, Chambers CD (2006). Accuracy of the diagnosis of physical features of fetal alcohol syndrome by pediatricians after specialized training. Pediatrics 118: e1734-e1738.
37. Kodituwakku P, Coriale G, Fiorentino D, Aragon AS, Kalberg WO, Buckley D, Gossage JP, Ceccanti M, May PA (2006): Neurobehavioral characteristics of children with fetal alcohol spectrum disorders in communities from Italy: Preliminary results. Alcohol Clin Exp Res 30: 1551-1561.
38. Lange N, Froimowitz MP, Bigler ED, Lainhart JE (2010): Associations between IQ, total and regional brain volumes, and demography in a large normative sample of healthy children and adolescents. Dev Neuropsychol 35: 296-317.
39. Lebel C, Rasmussen C, Wyper K, Andrew G, Beaulieu C (2010): Brain microstructure is related to math ability in children with fetal alcohol spectrum disorder. Alcohol Clin Exp Res 34: 354-363.
40. Lee KT, Mattson SN, Riley EP (2004): Classifying children with heavy prenatal alcohol exposure using measures of attention. J Int Neuropsychol Soc 10: 271-277.
41. Ma X, Coles CD, Lynch ME, Laconte SM, Zurkiya O, Wang D, Hu X (2005): Evaluation of corpus callosum anisotropy in young adults with fetal alcohol syndrome according to diffusion tensor imaging. Alcohol Clin Exp Res 29: 1214-1222.
42. Malisza KL, Allman AA, Shiloff D, Jakobson L, Longstaffe S, Chudley AE (2005): Evaluation of spatial working memory function in children and adults with fetal alcohol spectrum disorders: A functional magnetic resonance imaging study. Pediatr Res 58: 1150-1157.
43. Mattson SN, Riley EP (1998): A review of the neurobehavioral deficits in children with fetal alcohol syndrome or prenatal exposure to alcohol. Alcohol Clin Exp Res 22: 279-294.
44. Mattson SN, Roebuck TM (2002): Acquisition and retention of verbal and nonverbal information in children with heavy prenatal alcohol exposure. Alcohol Clin Exp Res 26: 875-882.
45. Mattson SN, Riley EP, Sowell ER, Jernigan TL, Sobel DF, Jones KL (1996): A decrease in the size of the basal ganglia in children with fetal alcohol syndrome. Alcohol Clin Exp Res 20: 1088-1093.
46. Mattson SN, Riley EP, Gramling L, Delis DC, Jones KL (1997): Heavy prenatal alcohol exposure with or without physical features of fetal alcohol syndrome leads to IQ deficits. J Pediatr 131: 718-721.
47. Mattson SN, Riley EP, Gramling L, Delis DC, Jones KL (1998): Neuropsychological comparison of alcohol-exposed children with or without physical features of fetal alcohol syndrome. Neuropsychology 12: 146-153.
48. Mattson SN, Goodman AM, Caine C, Delis DC, Riley EP (1999): Executive functioning in children with heavy prenatal alcohol exposure. Alcohol Clin Exp Res 23: 1808-1815.
49. Mattson SN, Schoenfeld AM, Riley EP (2001): Teratogenic effects of alcohol on brain and behavior. Alcohol Res Health 25: 185-191.
50. Mattson SN, Calarco KE, Lang AR (2006): Focused and shifting attention in children with heavy prenatal alcohol exposure. Neuropsychology 20: 361-369.
51. Mattson SN, Foroud T, Sowell ER, Jones KL, Coles CD, Fagerlund A, Autti-Rämö I, May PA, Adnams CM, Konovalova V, Wetherill L, Arenson AD, Barnett WK, Riley EP; CIFASD (2010): Collaborative initiative on fetal alcohol spectrum disorders: Methodology of clinical projects. Alcohol 44: 635-641.
52. May PA (2007): The epidemiology of fetal alcohol syndrome and partial FAS in a South-African community. Drug Alcohol Depend 88: 259-271.
53. May PA, Gossage JP, Brooke LE, Snell CL, Marais AS, Hendricks LS, Croxford JA, Viljoen DL (2005): Maternal risk factors for fetal alcohol syndrome in the Western cape province of South Africa: A population-based study. Am J Public Health 95: 1190-1199.
54. May PA, Fiorentino D, Phillip Gossage J, Kalberg WO, Eugene Hoyme H, Robinson LK, Coriale G, Jones KL, del Campo M, Tarani L, Romeo M, Kodituwakku PW, Deiana L, Buckley D, Ceccanti M (2006): Epidemiology of FASD in a province in Italy: Prevalence and characteristics of children in a random sample of schools. Alcohol Clin Exp Res 30: 1562-1575.
55. May PA, Gossage JP, Marais AS, Adnams CM, Hoyme HE, Jones KL, Robinson LK, Khaole NC, Snell C, Kalberg WO, Hendricks L, Brooke L, Stellavato C, Viljoen DL (2007): The epidemiology of fetal alcohol syndrome and partial FAS in a South African community. Drug Alcohol Depend 88: 259-271.
56. May PA, Gossage JP, Marais AS, Hendricks LS, Snell CL, Tabachnick BG, Stellavato C, Buckley DG, Brooke LE, Viljoen DL (2008): Maternal risk factors for fetal alcohol syndrome and partial fetal alcohol syndrome in South Africa: A third study. Alcohol Clin Exp Res 32: 738-753.
57. May PA, Gossage JP, Smith M, Tabachnick BG, Robinson LK, Manning M, Cecanti M, Jones KL, Khaole N, Buckley D, Kalberg WO, Trujillo PM, Hoyme HE. (2010): Population differences in dysmorphic features among children with fetal alcohol spectrum disorders. J Dev Behav Pediatr 31: 304-316.
58. Meintjes EM, Jacobson JL, Molteno CD, Gatenby JC, Warton C, Cannistraci CJ, Hoyme HE, Robinson LK, Khaole N, Gore JC, Jacobson SW. (2010): An fMRI study of number processing in children with fetal alcohol syndrome. Alcohol Clin Exp Res 34: 1450-1464.
59. Morey RA, Selgrade ES, Wagner HRII, Huettel SA, Wang L, McCarthy G (2010): Scan-rescan reliability of subcortical brain volumes derived from automated segmentation. Hum Brain Mapp 31: 1751-1762.
60. O'Connor MJ, Paley B (2006): The relationship of prenatal alcohol exposure and the postnatal environment to child depressive symptoms. J Pediatr Psychol 31: 50-64.
61. O'Hare ED, Kan E, Yoshii J, Mattson SN, Riley EP, Thompson PM, Toga AW, Sowell ER (2005): Mapping cerebellar vermal morphology and cognitive correlates in prenatal alcohol exposure. Neuroreport 16: 1285-1290.
62. O'Hare ED, Lu LH, Houston SM, Bookheimer SY, Mattson SN, O'Connor MJ, Sowell ER (2009): Altered frontal-parietal functioning during verbal working memory in children and adolescents with heavy prenatal alcohol exposure. Hum Brain Mapp 30: 3200-3208.
63. Packard MG, Knowlton BJ (2002): Learning and memory functions of the Basal Ganglia. Annu Rev Neurosci 25: 563-593.
64. Parnell SE, Dehart DB, Wills TA, Chen SY, Hodge CW, Besheer J, Waage-Baudet HG, Charness ME, Sulik KK (2006): Maternal oral intake mouse model for fetal alcohol spectrum disorders: Ocular defects as a measure of effect. Alcohol Clin Exp Res 30: 1791-1798.
65. Parnell SE, O'Leary-Moore SK, Godin EA, Dehart DB, Johnson BW, Allan Johnson G, Styner MA, Sulik KK (2009): Magnetic resonance microscopy defines ethanol-induced brain abnormalities in prenatal mice: Effects of acute insult on gestational day 8. Alcohol Clin Exp Res 33: 1001-1011.
66. Pollard I (2007): Neuropharmacology of drugs and alcohol in mother and fetus. Semin Fetal Neonatal Med 12: 106-113.
67. Reiss AL, Abrams MT, Singer HS, Ross JL, Denckla MB (1996): Brain development, gender and IQ in children. A volumetric imaging study. Brain 119 (Part 5): 1763-1774.
68. Rex DE, Ma JQ, Toga AW (2003): The LONI pipeline processing environment. Neuroimage 19: 1033-1048.
69. Rex DE, Shattuck DW, Woods RP, Narr KL, Luders E, Rehm K, Stoltzner SE, Rottenberg DA, Toga AW (2004): A meta-algorithm for brain extraction in MRI. Neuroimage 23: 625-637.
70. Riley EP, Mattson SN, Sowell ER, Jernigan TL, Sobel DF, Jones KL (1995): Abnormalities of the corpus callosum in children prenatally exposed to alcohol. Alcohol Clin Exp Res 19: 1198-1202.
71. Roebuck-Spencer TM, Mattson SN, Marion SD, Brown WS, Riley EP (2004): Bimanual coordination in alcohol-exposed children: Role of the corpus callosum. J Int Neuropsychol Soc 10: 536-548.
72. Schambra UB, Lauder JM, Petrusz P, Sulik KK (1990): Development of neurotransmitter systems in the mouse embryo following acute ethanol exposure: a histological and immunocytochemical study. Int J Dev Neurosci 8: 507-522.
73. Seger CA, Peterson EJ, Cincotta CM, Lopez-Paniagua D, Anderson CW (2010): Dissociating the contributions of independent corticostriatal systems to visual categorization learning through the use of reinforcement learning modeling and Granger causality modeling. Neuroimage 50: 644-656.
74. Shattuck DW, Leahy RM (2002): BrainSuite: An automated cortical surface identification tool. Med Image Anal 6: 129-142.
75. Slotkin TA (1998): Fetal nicotine or cocaine exposure: Which one is worse? J Pharmacol Exp Ther 285: 931-945.
76. Sowell ER, Jernigan TL, Mattson SN, Riley EP, Sobel DF, Jones KL (1996): Abnormal development of the cerebellar vermis in children prenatally exposed to alcohol: size reduction in lobules I-V. Alcohol Clin Exp Res 20: 31-34.
77. Sowell ER, Mattson SN, Thompson PM, Jernigan TL, Riley EP, Toga AW (2001a): Mapping callosal morphology and cognitive correlates: effects of heavy prenatal alcohol exposure. Neurology 57: 235-244.
78. Sowell ER, Thompson PM, Mattson SN, Tessner KD, Jernigan TL, Riley EP, Toga AW (2001b): Voxel-based morphometric analyses of the brain in children and adolescents prenatally exposed to alcohol. Neuroreport 12: 515-523.
79. Sowell ER, Thompson PM, Mattson SN, Tessner KD, Jernigan TL, Riley EP, Toga AW (2002a): Regional brain shape abnormalities persist into adolescence after heavy prenatal alcohol exposure. Cerebral Cortex 12: 856-865.
80. Sowell ER, Thompson PM, Peterson BS, Mattson SN, Welcome SE, Henkenius AL, Riley EP, Jernigan TL, Toga AW (2002b): Mapping cortical gray matter asymmetry patterns in adolescents with heavy prenatal alcohol exposure. Neuroimage 17: 1807-1819.
81. Sowell ER, Trauner DA, Gamst A, Jernigan TL (2002c): Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study. Dev Med Child Neurol 44: 4-16.
82. Sowell ER, Lu LH, O'Hare ED, McCourt ST, Mattson SN, O'Connor MJ, Bookheimer SY (2007): Functional magnetic resonance imaging of verbal learning in children with heavy prenatal alcohol exposure. Neuroreport 18: 635-639.
83. Sowell ER, Mattson SN, Kan E, Thompson PM, Riley EP, Toga AW (2008a): Abnormal cortical thickness and brain-behavior correlation patterns in individuals with heavy prenatal alcohol exposure. Cereb Cortex 18: 136-144.
84. Sowell ER, Johnson A, Kan E, Lu LH, Van Horn JD, Toga AW, O'Connor MJ, Bookheimer SY (2008b): Mapping white matter integrity and neurobehavioral correlates in children with fetal alcohol spectrum disorders. J Neurosci 28: 1313-1319.
85. Sulik KK (1984): Critical periods for alcohol teratogenesis in mice, with special reference to the gastrulation stage of embryogenesis. Ciba Found Symp 105: 124-141.
86. Sulik KK (2005): Genesis of alcohol-induced craniofacial dysmorphism. Exp Biol Med (Maywood) 230: 366-375.
87. Swayze VWII, Johnson VP, Hanson JW, Piven J, Sato Y, Giedd JN, Mosnik D, Andreasen NC (1997): Magnetic resonance imaging of brain anomalies in fetal alcohol syndrome. Pediatrics 99: 232-240.
88. Tae WS, Kim SS, Lee KU, Nam EC, Kim KW. (2008): Validation of hippocampal volumes measured using a manual method and two automated methods (FreeSurfer and IBASPM) in chronic major depressive disorder. Neuroradiology 50: 569-581.
89. Wechsler D (2003): The Wechsler Intelligence Scale for Children, 4th ed. San Antonio, TX: The Psychological Corporation.
90. Wozniak JR, Mueller BA, Chang PN, Muetzel RL, Caros L, Lim KO (2006): Diffusion tensor imaging in children with fetal alcohol spectrum disorders. Alcohol Clin Exp Res 30: 1799-1806.