Hostname: page-component-669899f699-tpknm Total loading time: 0 Render date: 2025-04-26T13:16:34.578Z Has data issue: false hasContentIssue false
  • English
  • Français

Neuroimaging effects of prenatal alcohol exposure on the developing human brain: a magnetic resonance imaging review

Published online by Cambridge University Press:  17 March 2015

Kirsten Ann Donald ,
Emma Eastman ,
Fleur Margaret Howells ,
Colleen Adnams ,
Edward Patrick Riley ,
Roger Paul Woods ,
Katherine Louise Narr  and
Dan Joseph Stein
Kirsten Ann Donald*
Affiliation:
Division of Developmental Paediatrics, Department of Paediatrics and Child Health, Red Cross War Memorial Children’s Hospital, University of Cape Town, Cape Town, South Africa
Emma Eastman
Affiliation:
Division of Developmental Paediatrics, Department of Paediatrics and Child Health, Red Cross War Memorial Children’s Hospital, University of Cape Town, Cape Town, South Africa
Fleur Margaret Howells
Affiliation:
Department of Psychiatry and Mental Health, University of Cape Town, Cape Town, South Africa
Colleen Adnams
Affiliation:
Department of Psychiatry and Mental Health, University of Cape Town, Cape Town, South Africa
Edward Patrick Riley
Affiliation:
Department of Psychology, San Diego State University, San Diego, CA, USA
Roger Paul Woods
Affiliation:
Department of Neurology, David Geffen School of Medicine, University of California, Los Angeles, CA, USA
Katherine Louise Narr
Affiliation:
Department of Neurology, David Geffen School of Medicine, University of California, Los Angeles, CA, USA
Dan Joseph Stein
Affiliation:
Department of Psychiatry and Mental Health, University of Cape Town, Cape Town, South Africa
*
Kirsten Ann Donald, Division of Developmental Paeditrics, Department of Paediatrics and Child Health, Red Cross War Memorial Children’s Hospital, University of Cape Town, Cape Town, South Africa. Tel: +27 21 658 5535 Fax: +27 21 658 5530 E-mail: kirsty.donald@uct.ac.za
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective

This paper reviews the magnetic resonance imaging (MRI) literature on the effects of prenatal alcohol exposure on the developing human brain.

Method

A literature search was conducted through the following databases: PubMed, PsycINFO and Google Scholar. Combinations of the following search terms and keywords were used to identify relevant studies: ‘alcohol’, ‘fetal alcohol spectrum disorders’, ‘fetal alcohol syndrome’, ‘FAS’, ‘FASD’, ‘MRI’, ‘DTI’, ‘MRS’, ‘neuroimaging’, ‘children’ and ‘infants’.

Results

A total of 64 relevant articles were identified across all modalities. Overall, studies reported smaller total brain volume as well as smaller volume of both the white and grey matter in specific cortical regions. The most consistently reported structural MRI findings were alterations in the shape and volume of the corpus callosum, as well as smaller volume in the basal ganglia and hippocampi. The most consistent finding from diffusion tensor imaging studies was lower fractional anisotropy in the corpus callosum. Proton magnetic resonance spectroscopy studies are few to date, but showed altered neurometabolic profiles in the frontal and parietal cortex, thalamus and dentate nuclei. Resting-state functional MRI studies reported reduced functional connectivity between cortical and deep grey matter structures.

Discussion

There is a critical gap in the literature of MRI studies in alcohol-exposed children under 5 years of age across all MRI modalities. The dynamic nature of brain maturation and appreciation of the effects of alcohol exposure on the developing trajectory of the structural and functional network argue for the prioritisation of studies that include a longitudinal approach to understanding this spectrum of effects and potential therapeutic time points.

Keywords

foetal alcohol spectrum disorders (FASD)foetal alcohol syndrome (FAS)magnetic resonance imaging (MRI)neuroimaging
Type
Review Article
Information
Acta Neuropsychiatrica , Volume 27 , Issue 5 , October 2015 , pp. 251 - 269
Check for updates
Copyright
© Scandinavian College of Neuropsychopharmacology 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

1. Jones, K, Smith, D. Recognition of the fetal alcohol syndrome in early infancy. Lancet 1973;302:999–1001.Google Scholar
2. May, PA, Gossage, JP, White‐Country, M et al. Alcohol consumption and other maternal risk factors for fetal alcohol syndrome among three distinct samples of women before, during, and after pregnancy: the risk is relative. Am J Med Genet 2004;127:10–20.CrossRefGoogle Scholar
3. World Health Organisation. Global status report on alcohol and health WHO Press, World Health Organization, Geneva, Switzerland, 2014.Google Scholar
4. Lupton, C, Burd, L, Harwood, R. Cost of fetal alcohol spectrum disorders. Am J Med Genet 2004;127:42–50.CrossRefGoogle Scholar
5. Popova, S, Stade, B, Bekmuradov, D, Lange, S, Rehm, J. What do we know about the economic impact of fetal alcohol spectrum disorder? A systematic literature review. Alcohol Alcohol 2011;46:490–497.Google Scholar
6. Navarro, HJ, Doran, CM, Shakeshaft, AP. Measuring costs of alcohol harm to others: a review of the literature. Drug Alcohol Depen 2011;114:87–99.Google ScholarPubMed
7. May, PA, Blankenship, J, Marais, AS et al. Maternal alcohol consumption producing fetal alcohol spectrum disorders (FASD): quantity, frequency, and timing of drinking. Drug Alcohol Depen 2013;133:502–512.CrossRefGoogle ScholarPubMed
8. May, PA, Fiorentino, D, Gossage, JP et al. Epidemiology of FASD in a province in Italy: prevalence and characteristics of children in a random sample of schools. Alcohol Clin Exp Res 2006:1562–1575.Google Scholar
9. May, PA, Gossage, JP, Kalberg, WO et al. The prevalence and epidemiologic characteristics of FASD from various research methods with an emphasis on in-school studies. Dev Disabil Res Revs 2009:176–192.Google Scholar
10. Viljoen, DL, Gossage, JP, Brooke, L et al. Fetal alcohol syndrome epidemiology in a South African community: a second study of a very high prevalence area. J Stud Alcohol 2005;66:593.Google Scholar
11. May, PA, Gossage, JP, Marais, AS et al. The epidemiology of fetal alcohol syndrome and partial FAS in a South African community. Drug Alcohol Depen 2007;88:259–271.CrossRefGoogle Scholar
12. May, PA, Fiorentino, D, Coriale, G et al. Prevalence of children with severe fetal alcohol spectrum disorders in communities near Rome, Italy: new estimated rates are higher than previous estimates. Int J Environ Res Public Health 2011;8:2331–2351.Google Scholar
13. May, PA, Blankenship, J, Marais, A et al. Approaching the prevalence of the full spectrum of fetal alcohol spectrum disorders in a South African population-based study. Alcohol Clin Exp Res 2013;37:818–830.Google Scholar
14. May, PA, Baete, A, Russo, J et al. Prevalence and characteristics of fetal alcohol spectrum disorders. Pediatrics 2014;134:855–866.Google Scholar
15. O’Leary-Moore, S, Parnell, S, Lipinski, R. Magnetic resonance-based imaging in animal models of fetal alcohol spectrum disorder. Neuropsychol Rev 2011;21:167–185.CrossRefGoogle ScholarPubMed
16. Mattson, SN, Riley, EP, Jernigan, TL et al. A decrease in the size of the basal ganglia following prenatal alcohol exposure: a preliminary report. Neurotoxicol Teratol 1994;16:283–289.Google Scholar
17. O’Leary-Moore, SK, Parnell, SE, Godin, EA et al. Magnetic resonance microscopy-based analyses of the brains of normal and ethanol-exposed fetal mice. Birth Defects Res A 2010;88:953–964.CrossRefGoogle ScholarPubMed
18. Coleman, LG Jr, Oguz, I, Lee, J, Styner, M, Crews, FT. Postnatal day 7 ethanol treatment causes persistent reductions in adult mouse brain volume and cortical neurons with sex specific effects on neurogenesis. Alcohol 2012;46:603–612.Google Scholar
19. Leigland, LA, Ford, MM, Lerch, JP, Kroenke, CD. The influence of fetal ethanol exposure on subsequent development of the cerebral cortex as revealed by magnetic resonance imaging. Alcohol Clin Exp Res 2013;37:924–932.CrossRefGoogle ScholarPubMed
20. Parnell, SE, O’Leary-Moore, SK, Godin, EA et al. Magnetic resonance microscopy defines ethanol-induced brain abnormalities in prenatal mice: effects of acute insult on gestational day 8. Alcohol Clin Exp Res 2009;33:1001–1011.CrossRefGoogle ScholarPubMed
21. Lipinski, RJ, Hammond, P, O’Leary-Moore, SK et al. Ethanol-induced face-brain dysmorphology patterns are correlative and exposure-stage dependent. PLoS One 2012;7:e43067. doi: 10.1371/journal.pone.0043067.Google Scholar
22. Leigland, LA, Budde, MD, Cornea, A, Kroenke, CD. Diffusion MRI of the developing cerebral cortical gray matter can be used to detect abnormalities in tissue microstructure associated with fetal ethanol exposure. NeuroImage 2013;83:1081–1087.CrossRefGoogle ScholarPubMed
23. O’Leary-Moore, SK, McMechan, AP, Galloway, MP, Hannigan, JH. Neonatal alcohol-induced region-dependent changes in rat brain neurochemistry measured by high-resolution magnetic resonance spectroscopy. Alcohol Clin Exp Res 2008;32:1697–1707.CrossRefGoogle ScholarPubMed
24. Jones, KL, Smith, DW, Ulleland, CN, Streissguth, AP. Pattern of malformation in offspring of chronic alcoholic mothers. Lancet 1973;1:1267–1271.CrossRefGoogle ScholarPubMed
25. Coulter, CL, Leech, RW, Schaefer, G, Scheithauer, BW, Brumback, RA. MIdline cerebral dysgenesis, dysfunction of the hypothalamic-pituitary axis, and fetal alcohol effects. Arch Neurol 1993;50:771–775.Google Scholar
26. Archibald, SL, Fennema-Notestine, C, Gamst, A, Riley, EP, Mattson, SN, Jernigan, TL. Brain dysmorphology in individuals with severe prenatal alcohol exposure. Dev Med Child Neurol 2001;43:148–154.CrossRefGoogle ScholarPubMed
27. Astley, SJ, Aylward, EH, Olson, HC et al. Magnetic resonance imaging outcomes from a comprehensive magnetic resonance study of children with fetal alcohol spectrum disorders. Alcohol Clin Exp Res 2009;33:1671–1689.Google Scholar
28. Autti-Rämö, I, Autti, T, Korkman, M, Kettunen, S, Salonen, O, Valanne, L. MRI findings in children with school problems who had been exposed prenatally to alcohol. Dev Med Child Neurol 2002;44:98–106.CrossRefGoogle ScholarPubMed
29. Bookstein, FL, Connor, PD, Huggins, JE, Barr, HM, Pimentel, KD, Streissguth, AP. Many infants prenatally exposed to high levels of alcohol show one particular anomaly of the corpus callosum. Alcohol Clin Exp Res 2007;31:868–879.Google Scholar
30. Bookstein, FL, Streissguth, AP, Sampson, PD, Connor, PD, Barr, HM. Corpus callosum shape and neuropsychological deficits in adult males with heavy fetal alcohol exposure. NeuroImage 2002;15:233–251.Google Scholar
31. Bookstein, FL, Sampson, PD, Connor, PD, Streissguth, AP. Midline corpus callosum is a neuroanatomical focus of fetal alcohol damage. Anat Rec 2002;269:162–174.CrossRefGoogle ScholarPubMed
32. Chen, X, Coles, CD, Lynch, ME, Hu, X. Understanding specific effects of prenatal alcohol exposure on brain structure in young adults. Hum Brain Mapp 2012;33:1663–1676.Google Scholar
33. Cortese, BM, Moore, GJ, Bailey, BA, Jacobson, SW, Delaney-Black, V, Hannigan, JH. Magnetic resonance and spectroscopic imaging in prenatal alcohol-exposed children: preliminary findings in the caudate nucleus. Neurotoxicol Teratol 2006;28:597–606.CrossRefGoogle ScholarPubMed
34. Johnson, VP, Swayze, VW, Sato, Y, Andreasen, NC. Fetal alcohol syndrome: craniofacial and central nervous system manifestations. Am J Med Genet 1996;61:329–339.Google Scholar
35. Joseph, J, Warton, C, Jacobson, SW et al. Three‐dimensional surface deformation‐based shape analysis of hippocampus and caudate nucleus in children with fetal alcohol spectrum disorders. Hum Brain Mapp 2014;35:659–672.CrossRefGoogle ScholarPubMed
36. Lebel, C, Rasmussen, C, Wyper, K, Walker, L, Andrew, G, Yager, J. Brain diffusion abnormalities in children with fetal alcohol spectrum disorder. Alcohol Clin Exp Res 2008;32:1732–1740.Google Scholar
37. Lebel, C, Mattson, SN, Riley, EP et al. A longitudinal study of the long-term consequences of drinking during pregnancy: heavy in utero alcohol exposure disrupts the normal processes of brain development. J Neurosci 2012;32:15243–15251.Google Scholar
38. Li, Z, Coles, CD, Lynch, ME, Ma, X, Peltier, S, Hu, X. Occipital-temporal reduction and sustained visual attention deficit in prenatal alcohol exposed adults. Brain Imaging Behav 2008;2:39–48.Google Scholar
39. Mattson, SN, Riley, EP, Jernigan, TL et al. Fetal alcohol syndrome: a case report of neuropsychological, MRI, and EEG assessment of two children. Alcohol Clin Exp Res 1992;16:1001–1003.Google Scholar
40. Mattson, SN, Riley, EP, Sowell, ER, Jernigan, TL, Sobel, DF, Jones, KL. A decrease in the size of the basal ganglia in children with fetal alcohol syndrome. Alcohol Clin Exp Res 1996;20:1088–1093.Google Scholar
41. Meintjes, EM, Narr, KL, van der Kouwe, AJ et al. A tensor-based morphometry analysis of regional differences in brain volume in relation to prenatal alcohol exposure. NeuroImage Clin 2014;5:152–160.Google Scholar
42. Nardelli, A, Lebel, C, Rasmussen, C, Andrew, G, Beaulieu, C. Extensive deep gray matter volume reductions in children and adolescents with fetal alcohol spectrum disorders. Alcohol Clin Exp Res 2011;35:1404–1417.Google ScholarPubMed
43. O’Hare, ED, Kan, E, Yoshii, J et al. Mapping cerebellar vermal morphology and cognitive correlates in prenatal alcohol exposure. Neuroreport 2005;16:1285–1290.Google Scholar
44. Rajaprakash, M, Chakravarty, MM, Lerch, JP, Rovet, J. Cortical morphology in children with alcohol-related neurodevelopmental disorder. Brain Imaging Behav 2014;4:41–50.Google Scholar
45. Riikonen, R, Salonen, I, Partanen, K, Verho, S. Brain perfusion SPECT and MRI in foetal alcohol syndrome. Dev Med Child Neurol 1999;41:652–659.CrossRefGoogle ScholarPubMed
46. Riikonen, RS, Nokelainen, P, Valkonen, K et al. Deep serotonergic and dopaminergic structures in fetal alcoholic syndrome: a study with nor-β-CIT-single-photon emission computed tomography and magnetic resonance imaging volumetry. Biol Psychiatry 2005;57:1565–1572.CrossRefGoogle ScholarPubMed
47. Riley, EP, Mattson, SN, Sowell, ER, Jernigan, TL, Sobel, DF, Jones, KL. Abnormalities of the corpus callosum in children prenatally exposed to alcohol. Alcohol Clin Exp Res 1995;19:1198–1202.Google Scholar
48. Roussotte, FF, Sulik, KK, Mattson, SN et al. Regional brain volume reductions relate to facial dysmorphology and neurocognitive function in fetal alcohol spectrum disorders. Hum Brain Mapp 2012;33:920–937.CrossRefGoogle ScholarPubMed
49. Sowell, ER, Jernigan, TL, Mattson, SN, Riley, EP, Sobel, DF, Jones, KL. Abnormal development of the cerebellar vermis in children prenatally exposed to alcohol: size reduction in lobules I-V. Alcohol Clin Exp Res 1996;20:31–34.Google Scholar
50. Sowell, ER, Thompson, PM, Mattson, SN et al. Voxel-based morphometric analyses of the brain in children and adolescents prenatally exposed to alcohol. Neuroreport 2001;12:515–523.CrossRefGoogle ScholarPubMed
51. Sowell, ER, Thompson, PM, Peterson, BS et al. Mapping cortical gray matter asymmetry patterns in adolescents with heavy prenatal alcohol exposure. NeuroImage 2002;17:1807–1819.Google Scholar
52. Sowell, ER, Mattson, SN, Kan, E, Thompson, PM, Riley, EP, Toga, AW. Abnormal cortical thickness and brain–behavior correlation patterns in individuals with heavy prenatal alcohol exposure. Cereb Cortex 2008;18:136–144.Google Scholar
53. Swayze, VW, Johnson, VP, Hanson, JW et al. Magnetic resonance imaging of brain anomalies in fetal alcohol syndrome. Pediatrics 1997;99:232–240.Google Scholar
54. Treit, S, Lebel, C, Baugh, L, Rasmussen, C, Andrew, G, Beaulieu, C. Longitudinal MRI reveals altered trajectory of brain development during childhood and adolescence in fetal alcohol spectrum disorders. J Neurosci 2013;33:10098–10109.CrossRefGoogle ScholarPubMed
55. Willoughby, KA, Sheard, ED, Nash, K, Rovet, J. Effects of prenatal alcohol exposure on hippocampal volume, verbal learning, and verbal and spatial recall in late childhood. J Int Neuropsychol Soc 2008;14:1022–1033.CrossRefGoogle ScholarPubMed
56. Yang, Y, Phillips, OR, Kan, E et al. Callosal thickness reductions relate to facial dysmorphology in fetal alcohol spectrum disorders. Alcohol Clin Exp Res 2012;36:798–806.Google Scholar
57. Yang, Y, Roussotte, F, Kan, E et al. Abnormal cortical thickness alterations in fetal alcohol spectrum disorders and their relationships with facial dysmorphology. Cereb Cortex 2012;22:1170–1179.Google Scholar
58. Zhou, D, Lebel, C, Lepage, C et al. Developmental cortical thinning in fetal alcohol spectrum disorders. NeuroImage 2011;58:16–25.Google Scholar
59. Wozniak, JR, Mueller, BA, Chang, PN, Muetzel, RL, Caros, L, Lim, KO. Diffusion tensor imaging in children with fetal alcohol spectrum disorders. Alcohol Clin Exp Res 2006;30:1799–1806.CrossRefGoogle ScholarPubMed
60. Sowell, ER, Johnson, A, Kan, E et al. Mapping white matter integrity and neurobehavioral correlates in children with fetal alcohol spectrum disorders. J Neurosci 2008;28:1313–1319.Google Scholar
61. Hermoye, L, Saint-Martin, C, Cosnard, G et al. Pediatric diffusion tensor imaging: normal database and observation of the white matter maturation in early childhood. NeuroImage 2006;29:493–504.CrossRefGoogle ScholarPubMed
62. Pannek, K, Guzzetta, A, Colditz, P, Rose, S. Diffusion MRI of the neonate brain: acquisition, processing and analysis techniques. Pediatr Radiol 2012;42:1169–1182.Google Scholar
63. Beaulieu, C. The basis of anisotropic water diffusion in the nervous system – a technical review. NMR Biomed 2002;15:435–436–455.Google Scholar
64. Dubois, J, Dehaene-Lambertz, G, Kulikova, S, Poupon, C, Hüppi, PS, Hertz-Pannier, L. The early development of brain white matter: a review of imaging studies in fetuses, newborns and infants. Neuroscience 2014;276:48–71.Google Scholar
65. Geng, X, Gouttard, S, Sharma, A et al. Quantitative tract-based white matter development from birth to age 2 years. NeuroImage 2012;61:542–557.CrossRefGoogle Scholar
66. Paus, T, Pesaresi, M, French, L. White matter as a transport system. Neuroscience 2014;276:117–125.CrossRefGoogle ScholarPubMed
67. Fryer, S, Schweinsburg, BC, Bjorkquist, OA, Frank, LK, Mattson, SM, Spadoni, AD. Characterisation of white matter microstructure in fetal alcohol spectrum disorders. Alcohol Clin Exp Res 2009;33:514–521.CrossRefGoogle ScholarPubMed
68. Li, L, Coles, CD, Lynch, ME, Hu, X. Voxelwise and skeleton-based region of interest analysis of fetal alcohol syndrome and fetal alcohol spectrum disorders in young adults. Hum Brain Mapp 2009;30:3265–3274.Google Scholar
69. Ma, X, Coles, CD, Lynch, ME et al. Evaluation of corpus callosum anisotropy in young adults with fetal alcohol syndrome according to diffusion tensor imaging. Alcohol Clin Exp Res 2005;29:1214–1222.CrossRefGoogle ScholarPubMed
70. Spottiswoode, BS, Meintjes, EM, Anderson, AW et al. Diffusion tensor imaging of the cerebellum and eyeblink conditioning in fetal alcohol spectrum disorder. Alcohol Clin Exp Res 2011;35:2174–2183.Google Scholar
71. Wozniak, JR, Muetzel, RL, Mueller, BA et al. Microstructural corpus callosum anomalies in children with prenatal alcohol exposure: an extension of previous diffusion tensor imaging findings. Alcohol Clin Exp Res 2009;33:1825–1835.Google Scholar
72. Ikonomidou, C, Bittigau, P, Ishimaru, MJ et al. Ethanol induced apoptotic neurodegeneration and fetal alcohol syndrome. Science 2000;287:1056–1060.Google Scholar
73. Roussotte, FF, Soderberg, L, Sowell, ER. Structural, metabolic and functional brain abnormalities as a result of prenatal exposure to drugs of abuse: evidence from neuroimaging. Neuropsychol Rev 2010;20:376–397.Google Scholar
74. Blüml, S, Wisnowski, JL, Nelson, MD et al. Metabolic maturation of the human brain from birth through adolescence: insights from in vivo magnetic resonance spectroscopy. Cereb Cortex 2012;23:2944–2955.Google Scholar
75. Ross, BD, Colletti, P, Lin, A. MR spectroscopy of the brain: neurospectroscopy. In Robert R. Edelman, John R. Hesselink, Michael B. Zlatkin, John V. Crues, editors. Clinical magnetic resonance imaging, 3rd edn. Philadelphia: Saunders-Elsevier, 2006; p. 1840–1910.Google Scholar
76. Astley, SJ, Richards, T, Aylward, EH et al. Magnetic resonance spectroscopy outcomes from a comprehensive magnetic resonance study of children with fetal alcohol spectrum disorders. J Magn Reson 2009;27:760–778.Google Scholar
77. Fagerlund, Å, Heikkinen, S, Autti-Rämö, I et al. Brain metabolic alterations in adolescents and young adults with fetal alcohol spectrum disorders. Alcohol Clin Exp Res 2006;30:2097–2104.CrossRefGoogle Scholar
78. du Plessis, L, Jacobson, JL, Jacobson, SW et al. An in vivo 1H magnetic resonance spectroscopy study of the deep cerebellar nuclei in children with fetal alcohol spectrum disorders. Alcohol Clin Exp Res 2014;38:1330–1338.Google Scholar
79. Burke, MW, Palmour, RM, Ervin, FR, Ptito, M. Neuronal reduction in frontal cortex of primates after prenatal alcohol exposure. Neuroreport 2009;20:13–17.Google Scholar
80. An, L, Zhang, T. Spatial cognition and sexually dimorphic synaptic plasticity balance impairment in rats with chronic prenatal ethanol exposure. Behav Brain Res 2013;256:564–574.Google Scholar
81. Sowell, ER, Johnson, A, Kan, E et al. Mapping white matter integrity and neurobehavioral correlates in children with fetal alcohol spectrum disorders. J Neurosci 2008;28:1313–1319.Google Scholar
82. Lebel, C, Roussotte, F, Sowell, ER. Imaging the impact of prenatal alcohol exposure on the structure of the developing human brain. Neuropsychol Rev 2011;21:102–118.Google Scholar
83. Wozniak, JR, Muetzel, RL. What does diffusion tensor imaging reveal about the brain and cognition in fetal alcohol spectrum disorders? Neuropsychol Rev 2011;21:133–147.Google Scholar
84. Lebel, C, Rasmussen, C, Wyper, K, Andrew, G, Beaulieu, C. Brain microstructure is related to math ability in children with fetal alcohol spectrum disorder. Alcohol Clin Exp Res 2010;34:354–363.CrossRefGoogle ScholarPubMed
85. Leigland, LA, Ford, MM, Lerch, JP, Kroenke, CD. The influence of fetal ethanol exposure on subsequent development of the cerebral cortex as revealed by magnetic resonance imaging. Alcohol Clin Exp Res 2013;37:924–932.CrossRefGoogle ScholarPubMed
86. Biswal, B, Zerrin Yetkin, F, Haughton, VM, Hyde, JS. Functional connectivity in the motor cortex of resting human brain using echo-planar mri. Magn Reson Med 1995;34:537–541.Google Scholar
87. Hagmann, P, Grant, PE, Fair, DA. MR connectomics: a conceptual framework for studying the developing brain. Front Sys Neurosci 2012;6:43.Google Scholar
88. Norman, AL, O’Brien, JW, Spadoni, AD et al. A functional magnetic resonance imaging study of spatial working memory in children with prenatal alcohol exposure: contribution of familial history of alcohol use disorders. Alcohol Clin Exp Res 2013;37:132–140.Google Scholar
89. Spadoni, AD, Bazinet, AD, Fryer, SL, Tapert, SF, Mattson, SN, Riley, EP. BOLD response during spatial working memory in youth with heavy prenatal alcohol exposure. Alcohol Clin Exp Res 2009;33:2067–2076.CrossRefGoogle ScholarPubMed
90. Malisza, KL, Allman, AA, Shiloff, D, Jakobson, L, Longstaffe, S, Chudley, AE. Evaluation of spatial working memory function in children and adults with fetal alcohol spectrum disorders: a functional magnetic resonance imaging study. Pediatr Res 2005;58:1150–1157.Google Scholar
91. Roussotte, FF, Bramen, JE, Nunez, SC et al. Abnormal brain activation during working memory in children with prenatal exposure to drugs of abuse: the effects of methamphetamine, alcohol, and polydrug exposure. NeuroImage 2011;54:3067–3075.CrossRefGoogle ScholarPubMed
92. Roussotte, FF, Rudie, JD, Smith, L et al. Frontostriatal connectivity in children during working memory and the effects of prenatal methamphetamine, alcohol and polydrug exposure. Dev Neurosci 2012;34:43–57.CrossRefGoogle ScholarPubMed
93. Diwadkar, VA, Meintjes, EM, Goradia, D et al. Differences in cortico-striatal-cerebellar activation during working memory in syndromal and nonsyndromal children with prenatal alcohol exposure. Hum Brain Mapp 2013;34:1931–1945.Google Scholar
94. Astley, SJ, Aylward, EH, Olson, HC et al. Functional magnetic resonance imaging outcomes from a comprehensive magnetic resonance study of children with fetal alcohol spectrum disorders. J Neurodev Disord 2009;1:61–80.Google Scholar
95. O’Hare, ED, Lu, LH, Houston, SM et al. Altered frontal-parietal functioning during verbal working memory in children and adolescents with heavy prenatal alcohol exposure. Hum Brain Mapp 2009;30:3200–3208.Google Scholar
96. O’Brien, JW, Norman, AL, Fryer, SL et al. Effect of predictive cuing on response inhibition in children with heavy prenatal alcohol exposure. Alcohol Clin Exp Res 2013;37:644–654.Google Scholar
97. Fryer, SL, Tapert, SF, Mattson, SN, Paulus, MP, Spadoni, AD, Riley, EP. Prenatal alcohol exposure affects frontal–striatal BOLD response during inhibitory control. Alcohol Clin Exp Res 2007;31:1415–1424.Google Scholar
98. Sowell, ER, Lu, LH, O’Hare, ED et al. Functional magnetic resonance imaging of verbal learning in children with heavy prenatal alcohol exposure. Neuroreport 2007;18:635–639.Google Scholar
99. Meintjes, EM, Jacobson, JL, Molteno, CD et al. An FMRI study of number processing in children with fetal alcohol syndrome. Alcohol Clin Exp Res 2010;34:1450–1464.Google Scholar
100. Santhanam, P, Coles, CD, Li, Z, Li, L, Lynch, ME, Hu, X. Default mode network dysfunction in adults with prenatal alcohol exposure. Psychiatry Res 2011;194:354–362.Google Scholar
101. Wozniak, JR, Mueller, BA, Bell, CJ et al. Global functional connectivity abnormalities in children with fetal alcohol spectrum disorders. Alcohol Clin Exp Res 2013;37:748–756.Google Scholar
102. Wozniak, JR, Mueller, BA, Muetzel, RL et al. Inter-hemispheric functional connectivity disruption in children with prenatal alcohol exposure. Alcohol Clin Exp Res 2011;35:849–861.Google Scholar
103. Sowell, ER, Mattson, SN, Thompson, PM, Jernigan, TL, Riley, EP, Toga, AW. Mapping callosal morphology and cognitive correlates: effects of heavy prenatal alcohol exposure. Neurology 2001;57:235–244.Google Scholar
104. Fix, JD. Basal ganglia and the striatal motor system. Neuroanatomy (Board Review Series), 4th edn. Baltimore: Wolters Kluwer; Lippincott Wiliams & Wilkins, 2008; p. 274–281.Google Scholar
105. Gilmore, JH, Shi, F, Woolson, SL et al. Longitudinal development of cortical and subcortical gray matter from birth to 2 years. Cereb Cortex 2012;22:2478–2485.CrossRefGoogle ScholarPubMed
106. Shaw, P, Kabani, NJ, Lerch, JP et al. Neurodevelopmental trajectories of the human cerebral cortex. J Neurosci 2008;28:3586–3594.Google Scholar
107. Norman, AL, Crocker, N, Mattson, SN, Riley, EP. Neuroimaging and fetal alcohol spectrum disorders. Dev Disabil Res Revs 2009;15:209–217.Google Scholar
108. Wozniak, JR, Muetzel, RL. What does diffusion tensor imaging reveal about the brain and cognition in fetal alcohol spectrum disorders. Neuropsychol Rev 2011;21:133–147.Google Scholar
109. Gonçalves, R, de, C, Vasconcelos, MM et al. Proton magnetic resonance spectroscopy in children with fetal alcohol spectrum disorders. Arq Neuropsiquiatr 2009;67:254–261.Google Scholar
110. Karadottir, R, Attwell, D. Combining patch-clamping of cells in brain slices with immunocytochemical labeling to define cell type and developmental stage. Nat Protoc 2006;1:1977–1986.Google Scholar
111. Rodier, PM. Vulnerable periods and processes during central nervous system development. Environ Health Perspect 1994;102(Suppl. 2):121–124.Google Scholar
112. Rodier, PM. Environmental causes of central nervous system maldevelopment. Pediatrics 2004;113:1076–1083.Google Scholar
113. Doria, V, Beckmann, CF, Arichi, T et al. Emergence of resting state networks in the preterm human brain. Proc Natl Acad Sci 2010;107:20015–20020.Google Scholar