Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-24T18:41:46.830Z Has data issue: false hasContentIssue false

Hippocampal Abnormalities in Youth with Alcohol-Related Neurodevelopmental Disorder

Published online by Cambridge University Press:  11 February 2014

Joanna Dudek
Affiliation:
Department of Psychology, University of Toronto, Toronto, Ontario
Jovanka Skocic
Affiliation:
Neuroscience and Mental Health Research Program, The Hospital for Sick Children, Toronto, Ontario
Erin Sheard
Affiliation:
Neuroscience and Mental Health Research Program, The Hospital for Sick Children, Toronto, Ontario
Joanne Rovet*
Affiliation:
Department of Psychology, University of Toronto, Toronto, Ontario Neuroscience and Mental Health Research Program, The Hospital for Sick Children, Toronto, Ontario Department of Pediatrics, University of Toronto, Toronto, Ontario
*
Correspondence and reprint requests to: Joanne Rovet, The Hospital for Sick Children, 555 University Avenue, Toronto, Ontario, Canada, M5G1X8. E-mail: [email protected]

Abstract

Individuals diagnosed with alcohol-related neurodevelopmental disorder (ARND) exhibit difficulty on hippocampally mediated memory tasks and show reduced hippocampal size. However inconsistencies exist regarding the affected memory functions and where within the hippocampi effects occur. Given recent studies showing anterior and posterior segments support distinct memory functions and sex dimorphisms in hippocampal function, we asked whether these factors influence memory performance in youth with ARND (n = 18) and typically developing controls (n = 17). Participants received a battery of memory tests and a structural MRI scan. Right and left hippocampi were manually traced; anterior and posterior segments were delineated at the uncus. Measured were intracranial volumes (ICV) and right and left hippocampi and hippocampal segments. Volumes were adjusted for ICV. Relative to controls, the ARND group had lower IQs and memory performance on most tasks and marginally smaller ICVs. Left and right hippocampal volumes and posterior segments were smaller in the ARND group. Although no sex differences were observed between groups, females overall had larger anterior hippocampi than males. Positive and negative associations between hippocampal and selective memory indices were found in the ARND group only. These findings are the first to suggest that posterior hippocampal development may be compromised in youth with ARND. (JINS, 2014, 20, 181–191)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2014 

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.)

References

Agnihotri, S., Sheard, E., Keightley, M., Rovet, J. (2012, September). Everyday memory impairments in children and adolescents with fetal alcohol spectrum disorder. FACE Roundtable Annual Meeting, Saskatoon SK.Google Scholar
Archibald, S.L., Fennema-Notestine, C., Gamst, A., Riley, E.P., Mattson, S.N., Jernigan, T.L. (2001). Brain dysmorphology in individuals with severe prenatal alcohol exposure. Developmental Medicine & Child Neurology, 43, 148154.Google Scholar
Astley, S.J., Aylward, E.H., Carmichael Olson, H.C., Kerns, K., Brooks, A., Coggins, T.E., Richards, T. (2009). Magnetic resonance imaging outcomes from a comprehensive magnetic resonance study of children with fetal alcohol spectrum disorders. Alcoholism, Clinical and Experimental Research, 33, 16711689.Google Scholar
Astley, S.J., Carmichael Olson, H., Kerns, K., Brooks, A., Aylward, E.H., Coggins, T.E., Richards, T. (2009). Neuropsychological and behavioral outcomes from a comprehensive magnetic resonance study of children with fetal alcohol spectrum disords. Canadian Journal Clinical Pharmacology, 16, e178e201.Google Scholar
Autti-Rämö, I., Autti, T., Korkman, M., Kettunen, S., Salonen, O., Valanne, L. (2002). MRI findings in children with school problems who had been exposed prenatally to alcohol. Developmental Medicine and Child Neurology, 44, 98106.CrossRefGoogle ScholarPubMed
Autti-Rämö, I., Granstrom, M.L. (1991). The effect of intrauterine alcohol exposition in various durations on early cognitive development. Neuropediatrics, 22, 203210.Google Scholar
Berman, R.F., Hannigan, J.H. (2000). Effects of prenatal alcohol exposure on the hippocampus: Spatial behavior, electrophysiology and neuroanatomy. Hippocampus, 10, 94110.Google Scholar
Bernstein, J.H., Waber, D.P. (1999). Developmental scoring system for the Rey-Osterrieth complex figure: Professional manual. Lutz, FL: Psychological Assessment Resources, Inc.Google Scholar
Bishop, S., Gahagan, S., Lord, C. (2007). Re-examining the core features of autism: A comparison of autism spectrum disorder and fetal alcohol spectrum disorder. Journal of Child Psychology and Psychiatry, 48, 11111121.Google Scholar
Brickman, A.M., Stern, Y., Small, S.A. (2011). Hippocampal subregions differentially associate with standardized memory tests. Hippocampus, 20, 923928.Google Scholar
Burd, L., Klung, M.G., Martsolf, J.T., Kerbeshian, J. (2003). Fetal alcohol syndrome: neuropsychiatric phenomics. Neurotoxicology and Teratology, 25, 697705.CrossRefGoogle ScholarPubMed
Cambridge Neuropsychological Test Automated Battery. (1998). Cambridge UK: CeNeS, V2: 35, Cognition.Google Scholar
Chudley, A.E., Conry, J., Cook, J.L., Loock, C., Rosales, T., LeBlanc, N. (2005). Fetal alcohol spectrum disorder: Canadian guidelines for diagnosis. Canadian Medical Association Journal, 172, 121.CrossRefGoogle ScholarPubMed
Chudley, A.E., Kilgour, A.R., Cranston, M., Edwards, M. (2007). Challenges of diagnosis in fetal alcohol syndrome and fetal alcohol spectrum disorder in the adult. American Journal of Medical Genetics Part C, 145C, 261272.Google Scholar
Clarren, S.K., Smith, D.W. (1978). The fetal alcohol syndrome. New England Journal of Medicine, 298, 10631067.Google Scholar
Cohen, M.J. (1997). Children's Memory Scale Manual. San Antonio: The Psychological Corporation.Google Scholar
Coles, C.D., Goldstein, F.C., Lynch, E.M., Chen, X., Kable, J.A., Johnson, K.C., Hu, X. (2011). Memory and brain volume in adults prenatally exposed to alcohol. Brain and Cognition, 75, 6777.CrossRefGoogle ScholarPubMed
Cortese, B.M., Moore, G.J., Bailey, B.A., Jacobson, S.W., Delaney-Black, V., Hannigan, J.H. (2006). Magnetic resonance and spectroscopic imaging in prenatal alcohol-exposed children: Preliminary findings in the caudate nucleus. Neurotoxicology and Teratology, 28, 597606.Google Scholar
Dennis, M., Francis, D.J., Cirino, P.T., Schachar, R., Barnes, M.A., Fletcher, J.M. (2009). Why IQ is not a covariate in cognitive studies of neurodevelopmental disorders. Journal of International Neuropsychological Society, 15, 331343.Google Scholar
Donaldson, T., Coles, C.D., Hagan, J.F., Evans, S.W., Klain, E.J., Kosofsy, B., Yolton, K. (2011, November). Recognizing alcohol-related neurodevelopmental disorder (ARND) in primary health care of children. NIAAA ICCFASD Consensus Statement, Rockville MD. exposure. Pediatrics, 119, 733741.Google Scholar
Duvernoy, H.M. (2005). The human hippocampus: Functional anatomy, vascularization and serial sections with MRI (3rd ed.). Berlin: Springer-Verlag.Google Scholar
Fanselow, M.S., Dong, H. (2010). Are the dorsal and ventral hippocampus functionally distinct structures? Neuron, 65, 125.CrossRefGoogle ScholarPubMed
Fast, D.K., Conry, J. (2009). Fetal alcohol spectrum disorders and the criminal justice system. Developmental Disabilities Research Reviews, 15, 250257.CrossRefGoogle ScholarPubMed
Filipek, P.A., Richelme, C., Kennedy, D.N., Caviness, V.S. Jr. (1994). The young adult human brain: An MRI-based morphometric analysis. Cerebral Cortex, 4, 344360.Google Scholar
Fryer, S.L., McGee, C.L., Matt, G.E., Riley, E.P., Mattson, S.N. (2007). Evaluation of psychopathological conditions in children with heavy prenatal alcohol exposure. Pediatrics, 119, 733741.Google Scholar
Giedd, J.N., Castellanos, F.X., Rajapakse, J.C., Vaituzis, A.C., Rapoport, J.L. (1997). Sexual dimorphism of the developing human brain. Progress in Neuropsychopharmacology & Biological Psychiatry, 21, 11851201.Google Scholar
Giedd, J.N., Vaituzis, A.C., Hamburger, S.D., Lange, N., Rajapakse, J.C., Kaysen, D., Rapoport, J.L. (1996). Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: Ages 4–18 years. Journal of Comparative Neurology, 366, 223230.Google Scholar
Gogtay, N., Nugent, T.F., Herman, D.H., Ordonez, A., Greenstein, D., Hayashi, K.M., Thompson, P.N. (2006). Dynamic mapping of normal human hippocampal development. Hippocampus, 16, 664672.Google Scholar
Goodlett, C.R., Peterson, S.D. (1995). Sex differences in vulnerability to developmental spatial learning deficits induced by limited binge alcohol exposure in neonatal rats. Neurobiology of Learning and Memory, 64, 265275.Google Scholar
Hamilton, D.A., Kodituwakku, P., Sutherland, R.J., Savage, D.D. (2003). Children with Fetal Alcohol Syndrome are impaired at place learning but not cued-navigation in a virtual Morris water task. Behavioural Brain Research, 143, 8594.Google Scholar
Kelly, S.J., Leggett, D.C., Cronise, K. (2009). Sexually dimorphic effects of alcohol exposure during development on the processing of social cues. Alcohol & Alcoholism, 44, 555560.Google Scholar
Klintsova, A.Y., Helfer, J.L., Calizo, L.H., Dong, W.K., Goodlett, C.R., Greenough, W.T. (2007). Persistent impairment of hippocampal neurogenesis in young adult rats following early postnatal alcohol exposure. Alcoholism: Clinical and Experimental Research, 31, 20732082.Google Scholar
Kodituwakku, P.W. (2007). Defining the behavioral phenotype in children with fetal alcohol spectrum disorders: A review. Neuroscience and Biobehavioral Reviews, 31, 192201.Google Scholar
Lebel, C., Rasmussen, C., Wyper, K., Walker, L., Andrew, G., Yager, J., Beaulieu, C. (2008). Brain diffusion abnormalities in children with fetal alcohol spectrum disorder. Alcohol: Clinical and Experimental Research, 32, 19.Google Scholar
Lebel, C., Roussotte, F., Sowell, E.R. (2011). Imaging the impact of prenatal alcohol exposure on the structure of the developing brain. Neuropsychology Review, 21, 102118.Google Scholar
Lipinski, R.J., Hammond, P., O'Leary-Moore, S.K., Ament, J.J., Pecevich, S.J., Jang, Y., Sulik, K.K. (2012). Ethanol-induced face-brain dysmophology patterns are correlative and exposure-stage dependent. PLOS One, 7, e43067.Google Scholar
Livy, D., Miller, E.K., Maier, S.E., West, J.R. (2003). Fetal alcohol exposure and temporal vulnerability: Effects of binge like alcohol exposure on the developing rat hippocampus. Neurotoxicology & Teratology, 25, 447458.CrossRefGoogle ScholarPubMed
Lord, C., Buss, C., Lupien, S.J., Preussner, J.C. (2008). Hippocampal volumes are larger in postmenopausal women using estrogen therapy compared to past users, never users and men: A possible window of opportunity effect. Neurobiology of Aging, 29, 95101.Google Scholar
Lupton, C., Burd, L., Harwood, R. (2004). Cost of fetal alcohol spectrum disorders. American Journal of Medical Genetics Part C, 127C, 4250.Google Scholar
Maguire, E.A., Gadian, D.G., Johnsrude, I.S., Good, C.D., Ashburner, J., Frackowiak, R.S., Frith, C.D. (2000). Navigation-related structural change in the hippocampi of taxi drivers. Proceedings of the National Academy of Sciences of the United States of America, 97, 43984403.Google Scholar
Malisza, K.L., Allman, A., Chiloff, D., Jakobson, L., Longstaffe, S., Chudley, A.E. (2005). Evaluation of spatial working memory function in children and adults with fetal alcohol spectrum disorders: A functional magnetic resonance imaging study. Pediatric Research, 58, 11501157.Google Scholar
Mattson, S.N., Riley, E.P., Delis, D.C., Stern, C., Lyons, K. (1996). Verbal learning and memory in children with Fetal Alcohol Syndrome. Alcoholism: Clinical and Experimental Research, 20, 810816.Google Scholar
May, P.A., Gossage, J.P. (2011). Maternal risk factors for fetal alcohol spectrum disorders. Alcohol Research & Health, 34, 1526.Google Scholar
May, P.A., Gossage, J.P., Kalberg, W.O., Robinson, L.K., Buckley, D., Manning, M., Hoyme, H.E. (2009). Prevalence and epidemiologic characteristics of FASD from various research methods with an emphasis on recent in-school studies. Developmental Disability Research Revised, 15, 176192.Google Scholar
May, P.A., Gossage, J.P., Marais, A.S., Hendricks, L.S., Snell, C.L., Tabachnick, B.G., Viljoen, D.L. (2008). Maternal risk factors for fetal alcohol syndrome and partial fetal alcohol syndrome in South Africa: A third study. Alcoholism: Clinical and Experimental Research, 32, 738753.CrossRefGoogle ScholarPubMed
Minetti, A., Arolfo, M.P., Virgolini, M.B., Brioni, J.D., Fulginiti, S. (1996). Spatial learning in rats exposed to acute ethanol intoxication on gestational day 8. Pharmacology Biochemistry and Behavior, 53, 361367.Google Scholar
Moser, M.B., Moser, E.I. (1998). Functional differentiation in the hippocampus. Hippocampus, 8, 608619.Google Scholar
Nardelli, A., Lebel, C., Rasmussen, C., Andrew, G., Beaulieu, C. (2011). Extensive deep gray matter volume reductions in children and adolescents with fetal alcohol spectrum disorder. Alcoholism: Clinical and Experimental Research, 8, 14041417.Google Scholar
Nash, K., Koren, G., Rovet, J. (2011). A differential approach for examining the behavioural phenotype of fetal alcohol spectrum disorders. Journal of Population Therapeutics and Clinical Pharmacology, 18, 440453.Google Scholar
Nash, K., Rovet, J., Greenbaum, R., Fantus, E., Nulman, I., Koren, G. (2006). Identifying the behavioural phenotype in fetal alcohol spectrum disorder: Sensitivity, specificity and screening potential. Archives Women's Mental Health, 9, 181186.Google Scholar
Nash, K., Stevens, S., Rovet, J., Fantus, E., Nulman, I., Sorbara, D., Koren, G. (2013). Towards identifying a characteristic neuropsychological profile for fetal alcohol spectrum disorders. Analysis of the Motherrisk FASD Clinic. Journal of Population Therapeutics and Clinical Pharmacology, 20, 4452.Google Scholar
Neufang, S., Specht, K., Hausmann, M., Gunturkun, O., Herpertz-Dahlmann, B., Fink, G.R., Konrad, K. (2009). Sex differences and the impact of steroid hormones on the developing human brain. Cerebral Cortex, 19, 464473.Google Scholar
O'Malley, K., Huggins, J. (2005). Suicidality in adolescents and adults with fetal alcohol spectrum disorders. Canadian Journal Psychiatry, 50, 125.Google Scholar
O'Malley, K., Nanson, J. (2002). Clinical implications of a link between fetal alcohol spectrum disorder and attention-deficit hyperactivity disorder. Canadian Journal of Psychiatry, 47, 349354.Google Scholar
Osterrieth, P., Rey, A. (1944). Le test de copie d'une figure complex. Archives de Psychologie, 30, 205221.Google Scholar
Parnell, S.E., O'Leary-Moore, S.K., Godin, E.A., Dehart, D.B., Johnson, B.W., Johnson, G.A., Sulik, K.K. (2009). Magenetic resonance microscopy defines ethanol-induced brain abnormalities in prenatal mice: Effects of acute insult on gestational day 8. Alcoholism: Clinical and Experimental Research, 33, 10011011.Google Scholar
Pei, J.R., Rinaldi, C.M., Rasmussen, C., Massey, V., Massey, D. (2008). Memory patterns of acquisition and retention of verbal and nonverbal information in children with fetal alcohol spectrum disorders. The Canadian Journal of Clinical Pharmacology, 15, 4456.Google Scholar
Poppenk, J., Evensmoen, H.R., Moscovtch, M., Nadel, L. (2013). Long-axis specialization of the human hippocampus. Trends in Cognitive Sciences, 17, 230240.Google Scholar
Poppenk, J., Moscovitch, M. (2011). A hippocampal marker of recollection memory ability among healthy young adults: Contributions of posterior and anterior segments. Neuron, 72, 931937.Google Scholar
Pruessner, J.C., Li, L.M., Serles, W., Pruessner, M., Collins, D.L., Kabani, N., Evans, A.C. (2000). Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: Minimizing the discrepancies between laboratories. Cerebral Cortex, 10, 433442.Google Scholar
Rajaprakash, M., Chakravarty, M.M., Lerch, J.P., Rovet, J. (2014). Cortical morphology in children with alcohol-related neurodevelopment disorder. Brain and Behavior, 4, 4150.Google Scholar
Rasmussen, C., Andrew, G., Zwaigenbaum, L., Tough, S. (2008). Neurobehavioral outcomes of children with fetal alcohol spectrum disorders: A Canadian perspective. Paediatrics & Child Health, 13, 185191.Google Scholar
Rasmussen, C., Benz, J., Pei, J., Andrew, G., Schuller, G., Abele-Wester, L., Lord, L. (2010). The impact of an ADHD co-morbidity on the diagnosis of FASD. Canadian Journal Clinical Pharmacology, 17, e165e176.Google Scholar
Rasmussen, C., Horne, K., Witol, A. (2008). Neurobehavioral functioning in children with Fetal Alcohol Spectrum Disorder. Child Neuropsychology, 12, 453468.Google Scholar
Rasmussen, C., McAuley, R., Andrew, G. (2008). Parental ratings of children with Fetal Alcohol Spectrum Disorder on the behavioral rating inventory of executive function (BRIEF). Journal of Fetal Alcohol Syndrome International, 5, 18.Google Scholar
Reynolds, C.R., Bigler, E.D. (2007). Test of memory and learning (2nd ed.). Circle Pines, MN: Pearson American Guidance Service.Google Scholar
Richardson, G.A., Ryan, C., Willford, J., Day, N.L., Goldschmidt, L. (2002). Prenatal alcohol and marijuana exposure: Effects on neuropsychological outcomes at 10 years. Neurotoxicology and Teratology, 24, 309320.Google Scholar
Riikonen, R.S., Salonen, I., Partanen, K., Verho, S. (1999). Brain perfusion SPECT and MRI in fetal alcohol syndrome. Developmental Medicine & Child Neurology, 41, 652659.Google Scholar
Riley, E.P., Mattson, S.N., Sowell, E.R., Jernigan, T.L., Sobel, D.F., Jones, K.L. (1995). Abnormalities of the corpus callosum in children prenatally exposed to alcohol. Alcoholism, Clinical and Experimental Research, 19, 11981202.Google Scholar
Riley, E.P., McGee, C.L. (2005). Fetal alcohol spectrum disorders: An overview with emphasis on changes in brain and behavior. Experimental Biology and Medicine, 230, 357365.Google Scholar
Robinson, G.C., Conry, J.L., Conry, R.F. (1987). Clinical profile and prevalence of fetal alcohol syndrome in an isolated community in British Columbia. Canadian Medical Association Journal, 127, 203307.Google Scholar
Rovet, J., Sheard, E., Wheeler, S., Skocic, J. (2010, November). Children with fetal alcohol spectrum disorder show atypical fMRI activitation of the hippocampus on memory tasks. Fetal Alcohol Spectrum Disorders: Growing Awareness in Europe, FASD-EU Conference Proceesings, Rolduc, The Netherlands.Google Scholar
Sowell, E.R., Jernigan, T.L., Mattson, S.N., Riley, E.P., Sobel, D.F., Jones, K.L. (1996). Abnormal development of the cerebellar vermis in children prenatally exposed to alcohol: Size reduction in lobules I-V. Alcoholism, Clinical and Experimental Research, 20, 3134.Google Scholar
Sowell, E.R., Lu, L.H., O'Hare, E.D., McCourt, S.T., Mattson, S.N., O'Connor, M.J., Bookheimer, S.Y. (2007). Functional magnetic resonance imaging of verbal learning in children with heavy prenatal alcohol exposure. Neuroreport, 18, 635639.Google Scholar
Sowell, E.R., Mattson, S.N., Kan, E., Thompson, P.M., Riley, E.P., Toga, A.W. (2008). Abnormal cortical thickness and brain behavior correlation patterns in individuals with heavy prenatal alcohol exposure. Cerebral Cortex, 18, 136144.Google Scholar
Sowell, E.R., Thompson, P.M., Mattson, S.N., Tessner, K.D., Jernigan, T.L., Riley, E.P., Toga, A.W. (2002). Regional brain shape abnormalities persist into adolescence after heavy prenatal alcohol exposure. Cerebral Cortex, 12, 856865.Google Scholar
Spadoni, A.D., McGee, C.L., Fryer, S.L., Riley, E.P. (2007). Neuroimaging and Fetal Alcohol Spectrum Disorders. Neuroscience and Biobehavioral Reviews, 31, 239245.Google Scholar
Stade, B., Ali, A., Bennett, D., Campbell, D., Johnston, M., Lens, C., Koren, G. (2009). The burden of prenatal exposure to alcohol: Revised measurement of cost. Canadian Journal Clinical Pharmacology, 16, e91e102.Google Scholar
Stade, B., Ungar, W., Stevens, B., Beyene, J., Koren, G. (2006). The burden of prenatal exposure to alcohol: Measurement of costs. Journal of Fetal Alcohol Syndrome International, 4, e5.Google Scholar
Stevens, S.A., Nash, K., Fantus, E., Nulman, I., Rovet, J., Koren, G. (2013). Towards identifying a characteristic neuropsychological profile for fetal alcohol spectrum disorder. Specific caregiver- and teach-rating. Journal of Population Therapeutics & Clinical Pharmacology, 20, 5362.Google Scholar
Stevens, S.A., Nash, K., Koren, G., Rovet, J. (2012). Autism characteristics in children with fetal alcohol spectrum disorders. Child Neuropsychology, 1, 19.Google Scholar
Stoler, M., Holmes, L.B. (1999). Under recognition of prenatal alcohol effects in infants of known alcohol abusing women. Journal of Pediatrics, 135, 430436.Google Scholar
Stratton, K.R., Howe, C.J., Battaglia, F.C. (1996). Fetal Alcohol Syndrome: Diagnosis, Epidemiology, Prevention, and Treatment. Institute of Medicine, Washington, DC: National Academy Press.Google Scholar
Streissguth, A.P., Bookstein, F.L., Barr, H.M., Sampson, P.D., O'Malley, K., Kogan Young, J. (2004). Risk factors for adverse life outcomes in fetal alcohol syndrome and fetal alcohol effects. Journal of Developmental and Behavioral Pediatrics, 25, 228238.Google Scholar
Taylor, L.B. (1991). Scoring criteria for the ROCF. In O. Spreen, & E. Strauss (Eds.), A compendium of neuropsychological tests: Administration, norms, and commentary. New York: Oxford University Press.Google Scholar
Uecker, A., Nadel, L. (1996). Spatial locations gone awry: Object and spatial memory deficits in children with fetal alcohol syndrome. Neuropsychologia, 34, 209223.Google Scholar
Wechsler, D. (1999). Wechsler Abbreviated Scale of Intelligence. New York: Psychological Corporation.Google Scholar
Willford, J.A., Richardson, G.A., Leech, S.L., Day, N.L. (2004). Verbal and visuospatial learning and memory function in children with moderate prenatal alcohol exposure. Alcoholism: Clinical and Experimental Research, 38, 497507.Google Scholar
Willoughby, K.A., Sheard, E.D., Nash, K., Rovet, J. (2008). Effects of prenatal exposure on hippocampal volume, verbal learning, and verbal and spatial recall in late childhood. Journal of the International Neuropsychological Society, 14, 10221033.Google Scholar
Wozniak, J.R., Muetzel, R.L., Mueller, B.A., McGee, C.L., Feerks, M.A., Ward, E.E., Lim, K.O. (2009). Microstructural corpus callosum anomalies in children with prenatal alcohol exposure: An extension of previous diffusion tensor imaging findings. Alcohol: Clinical and Experimental Research, 33, 18251835.Google Scholar
Yang, Y., Roussotte, F., Kan, E., Sulik, K., Mattson, S., Riley, E., Sowell, E.B. (2012). Abnormal cortical thickness alterations in Fetal Alcohol Spectrum Disorders and their relationships with facial dysmorphology. Cerebral Cortex, 22, 11701179.Google Scholar
Zhou, D., Lebel, C., Lepage, C., Rasmussen, C., Evans, A., Wyper, K., Beaulieu, C. (2011). Developmental cortical thinning in fetal alcohol spectrum disorders. Neuroimage, 58, 1625.CrossRefGoogle ScholarPubMed
Zimmerman, M.E., Pan, J.W., Hetherington, H.P., Katz, M.J., Verghese, J., Buschke, H., Lipton, R.B. (2008). Hippocampal neurochemistry, neuromorphometry, and verbal memory in nondemented older adults. Neurology, 70, 15941600.Google Scholar