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Published in: Neuropsychology Review 2/2011

01-06-2011 | Review

Biobehavioral Markers of Adverse Effect in Fetal Alcohol Spectrum Disorders

Authors: Sandra W. Jacobson, Joseph L. Jacobson, Mark E. Stanton, Ernesta M. Meintjes, Christopher D. Molteno

Published in: Neuropsychology Review | Issue 2/2011

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Abstract

Identification of children with fetal alcohol spectrum disorders (FASD) is difficult because information regarding prenatal exposure is often lacking, a large proportion of affected children do not exhibit facial anomalies, and no distinctive behavioral phenotype has been identified. Castellanos and Tannock have advocated going beyond descriptive symptom-based approaches to diagnosis to identify biomarkers derived from cognitive neuroscience. Classical eyeblink conditioning and magnitude comparison are particularly promising biobehavioral markers of FASD—eyeblink conditioning because a deficit in this elemental form of learning characterizes a very large proportion of alcohol-exposed children; magnitude comparison because it is a domain of higher order cognitive function that is among the most sensitive to fetal alcohol exposure. Because the neural circuitry mediating both these biobehavioral markers is well understood, they have considerable potential for advancing understanding of the pathophysiology of FASD, which can contribute to development of treatments targeted to the specific deficits that characterize this disorder.
Literature
go back to reference Abel, E. L. (1995). An update on the general incidence of FAS: FAS is not an equal opportunity deficit. Neurotoxicology and Teratology, 17, 437–443.PubMedCrossRef Abel, E. L. (1995). An update on the general incidence of FAS: FAS is not an equal opportunity deficit. Neurotoxicology and Teratology, 17, 437–443.PubMedCrossRef
go back to reference Anderson, C. M., Polcari, A., Lowen, S. B., Renshaw, P. F., & Teicher, M. H. (2002). Effects of methylphenidate on functional magnetic resonance relaxometry of the cerebellar vermis in boys with ADHD. The American Journal of Psychiatry, 159, 1322–1328.PubMedCrossRef Anderson, C. M., Polcari, A., Lowen, S. B., Renshaw, P. F., & Teicher, M. H. (2002). Effects of methylphenidate on functional magnetic resonance relaxometry of the cerebellar vermis in boys with ADHD. The American Journal of Psychiatry, 159, 1322–1328.PubMedCrossRef
go back to reference 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 and Child Neurology, 43, 148–154.PubMed 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 and Child Neurology, 43, 148–154.PubMed
go back to reference Astley, S. J., & Clarren, S. K. (2001). Measuring the facial phenotype of individuals with prenatal alcohol exposure: correlations with brain dysfunction. Alcohol and Alcoholism, 36, 147–159.PubMedCrossRef Astley, S. J., & Clarren, S. K. (2001). Measuring the facial phenotype of individuals with prenatal alcohol exposure: correlations with brain dysfunction. Alcohol and Alcoholism, 36, 147–159.PubMedCrossRef
go back to reference Bauer-Moffett, C., & Altman, J. (1977). The effect of ethanol chronically administered to preweanling rats on cerebellar development: a morphological study. Brain Research, 119, 249–268.PubMedCrossRef Bauer-Moffett, C., & Altman, J. (1977). The effect of ethanol chronically administered to preweanling rats on cerebellar development: a morphological study. Brain Research, 119, 249–268.PubMedCrossRef
go back to reference Bearer, C. F., Lee, S., Salvator, A. E., Minnes, S., Swick, A., Yamashita, T., et al. (1999). Ethyl linoleate in meconium: a biomarker for prenatal ethanol exposure. Alcoholism, Clinical and Experimental Research, 23, 487–493.PubMed Bearer, C. F., Lee, S., Salvator, A. E., Minnes, S., Swick, A., Yamashita, T., et al. (1999). Ethyl linoleate in meconium: a biomarker for prenatal ethanol exposure. Alcoholism, Clinical and Experimental Research, 23, 487–493.PubMed
go back to reference Bearer, C. F., Jacobson, J. L., Jacobson, S. W., Barr, D., Croxford, J., Molteno, C. D., et al. (2003). Validation of a new biomarker of fetal exposure to alcohol. The Journal of Pediatrics, 143, 463–469.PubMedCrossRef Bearer, C. F., Jacobson, J. L., Jacobson, S. W., Barr, D., Croxford, J., Molteno, C. D., et al. (2003). Validation of a new biomarker of fetal exposure to alcohol. The Journal of Pediatrics, 143, 463–469.PubMedCrossRef
go back to reference Berquin, P. C., Giedd, J. N., Jacobsen, L. K., Hamburger, S. D., Krain, A. L., Rapoport, J. L., et al. (1998). Cerebellum in attention-deficit hyperactivity disorder: a morphometric MRI study. Neurology, 50, 1087–1093.PubMed Berquin, P. C., Giedd, J. N., Jacobsen, L. K., Hamburger, S. D., Krain, A. L., Rapoport, J. L., et al. (1998). Cerebellum in attention-deficit hyperactivity disorder: a morphometric MRI study. Neurology, 50, 1087–1093.PubMed
go back to reference Bichenkov, E., & Ellingson, J. S. (2001). Ethanol exerts different effects on myelin basic protein and 2′,3′-cyclic nucleotide 3′-phosphodiesterase expression in differentiating CG-4 oligodendrocytes. Brain Research. Developmental Brain Research, 128, 9–16.PubMedCrossRef Bichenkov, E., & Ellingson, J. S. (2001). Ethanol exerts different effects on myelin basic protein and 2′,3′-cyclic nucleotide 3′-phosphodiesterase expression in differentiating CG-4 oligodendrocytes. Brain Research. Developmental Brain Research, 128, 9–16.PubMedCrossRef
go back to reference Bonthius, D. J., & West, J. R. (1991). Permanent neuronal deficits in rats exposed to alcohol during the brain growth spurt. Teratology, 44, 147–163.PubMedCrossRef Bonthius, D. J., & West, J. R. (1991). Permanent neuronal deficits in rats exposed to alcohol during the brain growth spurt. Teratology, 44, 147–163.PubMedCrossRef
go back to reference Brown, K. L., Calizo, L. H., & Stanton, M. E. (2008). Dose-dependent deficits in dual interstimulus interval classical eyeblink conditioning tasks following neonatal binge alcohol exposure in rats. Alcoholism, Clinical and Experimental Research, 32, 277–293.PubMedCrossRef Brown, K. L., Calizo, L. H., & Stanton, M. E. (2008). Dose-dependent deficits in dual interstimulus interval classical eyeblink conditioning tasks following neonatal binge alcohol exposure in rats. Alcoholism, Clinical and Experimental Research, 32, 277–293.PubMedCrossRef
go back to reference Burden, M. J., Jacobson, S. W., Sokol, R. J., & Jacobson, J. L. (2005a). Effects of prenatal alcohol exposure on attention and working memory at 7.5 years of age. Alcoholism, Clinical and Experimental Research, 29, 443–452.CrossRef Burden, M. J., Jacobson, S. W., Sokol, R. J., & Jacobson, J. L. (2005a). Effects of prenatal alcohol exposure on attention and working memory at 7.5 years of age. Alcoholism, Clinical and Experimental Research, 29, 443–452.CrossRef
go back to reference Burden, M. J., Jacobson, S. W., & Jacobson, J. L. (2005b). The relation of prenatal alcohol exposure to cognitive processing speed and efficiency in childhood. Alcoholism, Clinical and Experimental Research, 29, 1473–1483.CrossRef Burden, M. J., Jacobson, S. W., & Jacobson, J. L. (2005b). The relation of prenatal alcohol exposure to cognitive processing speed and efficiency in childhood. Alcoholism, Clinical and Experimental Research, 29, 1473–1483.CrossRef
go back to reference Burden, M. J., Jacobson, J. L., Westerlund, A. J., Lundahl, L. H., Klorman, R., Nelson, C. A., et al. (2010). An event-related potential study of response inhibition in ADHD with and without prenatal alcohol exposure. Alcoholism, Clinical and Experimental Research, 34, 617–627.PubMedCrossRef Burden, M. J., Jacobson, J. L., Westerlund, A. J., Lundahl, L. H., Klorman, R., Nelson, C. A., et al. (2010). An event-related potential study of response inhibition in ADHD with and without prenatal alcohol exposure. Alcoholism, Clinical and Experimental Research, 34, 617–627.PubMedCrossRef
go back to reference Butterworth, B. (1999). The mathematical brain. London: Macmillan. Butterworth, B. (1999). The mathematical brain. London: Macmillan.
go back to reference Butterworth, B. (2005). The development of arithmetical abilities. Journal of Child Psychology and Psychiatry, 46, 3–18.PubMedCrossRef Butterworth, B. (2005). The development of arithmetical abilities. Journal of Child Psychology and Psychiatry, 46, 3–18.PubMedCrossRef
go back to reference Cantlon, J. F., Brannon, E. M., Carter, E. J., & Pelphrey, K. A. (2006). Functional imaging of numerical processing in adults and 4-yr-old children. PLoS Biology, 4, e125.PubMedCrossRef Cantlon, J. F., Brannon, E. M., Carter, E. J., & Pelphrey, K. A. (2006). Functional imaging of numerical processing in adults and 4-yr-old children. PLoS Biology, 4, e125.PubMedCrossRef
go back to reference Carmichael-Olson, H., Feldman, J. J., Streissguth, A. P., Sampson, P. D., & Bookstein, F. L. (1998). Neuropsychological deficits in adolescents with fetal alcohol syndrome: clinical findings. Alcoholism, Clinical and Experimental Research, 22, 1998–2012. Carmichael-Olson, H., Feldman, J. J., Streissguth, A. P., Sampson, P. D., & Bookstein, F. L. (1998). Neuropsychological deficits in adolescents with fetal alcohol syndrome: clinical findings. Alcoholism, Clinical and Experimental Research, 22, 1998–2012.
go back to reference Castellanos, F. X., & Tannock, R. (2002). Neuroscience of attention-deficit/hyperactivity disorder: the search for endophenotypes. Nature Reviews. Neuroscience, 3, 617–628.PubMed Castellanos, F. X., & Tannock, R. (2002). Neuroscience of attention-deficit/hyperactivity disorder: the search for endophenotypes. Nature Reviews. Neuroscience, 3, 617–628.PubMed
go back to reference Castellanos, F. X., Lee, P. P., Sharp, W., Jeffries, N. O., Greenstein, D. K., Clasen, L. S., et al. (2002). Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder. JAMA, 288, 1740–1748.PubMedCrossRef Castellanos, F. X., Lee, P. P., Sharp, W., Jeffries, N. O., Greenstein, D. K., Clasen, L. S., et al. (2002). Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder. JAMA, 288, 1740–1748.PubMedCrossRef
go back to reference Chambers, C. D., et al. (2008). Predictors of binge drinking during pregnancy among women in Ukraine. Abstract poster presented at American Public Health Association meeting, October, 2008. Chambers, C. D., et al. (2008). Predictors of binge drinking during pregnancy among women in Ukraine. Abstract poster presented at American Public Health Association meeting, October, 2008.
go back to reference Cheng, D. T., Disterhoft, J. F., Power, J. M., Ellis, D. A., & Desmond, J. E. (2008). Neural substrates underlying human delay and trace eyeblink conditioning. Proceedings of the National Academy of Sciences of the United States of America, 105, 8108–8113.PubMedCrossRef Cheng, D. T., Disterhoft, J. F., Power, J. M., Ellis, D. A., & Desmond, J. E. (2008). Neural substrates underlying human delay and trace eyeblink conditioning. Proceedings of the National Academy of Sciences of the United States of America, 105, 8108–8113.PubMedCrossRef
go back to reference Chiappelli, F., Taylor, A. N., Espinosa de los Monteros, A., & de Vellis, J. (1991). Fetal alcohol delays the development expression of myelin basic protein and transferring in rat primary oligodendrocyte cultures. International Journal of Developmental Neuroscience, 9, 67–75.PubMedCrossRef Chiappelli, F., Taylor, A. N., Espinosa de los Monteros, A., & de Vellis, J. (1991). Fetal alcohol delays the development expression of myelin basic protein and transferring in rat primary oligodendrocyte cultures. International Journal of Developmental Neuroscience, 9, 67–75.PubMedCrossRef
go back to reference Chochon, F., Cohen, L., van de Moortele, P. F., & Dehaene, S. (1999). Differential contributions of the left and right inferior parietal lobules to number processing. Journal of Cognitive Neuroscience, 11, 617–630.PubMedCrossRef Chochon, F., Cohen, L., van de Moortele, P. F., & Dehaene, S. (1999). Differential contributions of the left and right inferior parietal lobules to number processing. Journal of Cognitive Neuroscience, 11, 617–630.PubMedCrossRef
go back to reference Christian, K. M., & Thompson, R. F. (2003). Neural substrates of eyeblink conditioning: acquisition and retention. Learning & Memory, 10, 427–455.CrossRef Christian, K. M., & Thompson, R. F. (2003). Neural substrates of eyeblink conditioning: acquisition and retention. Learning & Memory, 10, 427–455.CrossRef
go back to reference Clark, R. E., & Lavond, D. G. (1993). Reversible lesions of the red nucleus during acquisition and retention of a classically conditioned behavior in rabbits. Behavioral Neuroscience, 107, 264–270.PubMedCrossRef Clark, R. E., & Lavond, D. G. (1993). Reversible lesions of the red nucleus during acquisition and retention of a classically conditioned behavior in rabbits. Behavioral Neuroscience, 107, 264–270.PubMedCrossRef
go back to reference Clark, R. E., & Squire, L. R. (1998). Classical conditioning and brain systems: the role of awareness. Science, 280, 77–81.PubMedCrossRef Clark, R. E., & Squire, L. R. (1998). Classical conditioning and brain systems: the role of awareness. Science, 280, 77–81.PubMedCrossRef
go back to reference Clark, R. E., Zhang, A. A., & Lavond, D. G. (1992). Reversible lesions of the cerebellar interpositus nucleus during acquisition and retention of a classically conditioned behavior. Behavioral Neuroscience, 106, 879–888.PubMedCrossRef Clark, R. E., Zhang, A. A., & Lavond, D. G. (1992). Reversible lesions of the cerebellar interpositus nucleus during acquisition and retention of a classically conditioned behavior. Behavioral Neuroscience, 106, 879–888.PubMedCrossRef
go back to reference Clarren, S. K. (1977). Central nervous system malformations in two offspring of alcoholic women. Birth Defects Original Article Series, 13, 151–153.PubMed Clarren, S. K. (1977). Central nervous system malformations in two offspring of alcoholic women. Birth Defects Original Article Series, 13, 151–153.PubMed
go back to reference Clarren, S. K. (1986). Neuropathology and fetal alcohol syndrome. In J. R. West (Ed.), Alcohol and brain development. New York: Oxford University Press. Clarren, S. K. (1986). Neuropathology and fetal alcohol syndrome. In J. R. West (Ed.), Alcohol and brain development. New York: Oxford University Press.
go back to reference Clarren, S. K., & Smith, D. W. (1978). The fetal alcohol syndrome. The New England Journal of Medicine, 298, 1063–1067.PubMedCrossRef Clarren, S. K., & Smith, D. W. (1978). The fetal alcohol syndrome. The New England Journal of Medicine, 298, 1063–1067.PubMedCrossRef
go back to reference Coffin, J. M., & Boegle, A. (2000). Failure of dyslexics to achieve eyeblink conditioning following five days of training. Society for Neuroscience Abstracts, 26. Coffin, J. M., & Boegle, A. (2000). Failure of dyslexics to achieve eyeblink conditioning following five days of training. Society for Neuroscience Abstracts, 26.
go back to reference Coffin, J. M., Baroody, S., Schneider, K., & O’Neill, J. (2005). Impaired cerebellar learning in children with prenatal alcohol exposure: a comparative study of eyeblink conditioning in children with ADHD and dyslexia. Cortex, 41, 389–398.PubMedCrossRef Coffin, J. M., Baroody, S., Schneider, K., & O’Neill, J. (2005). Impaired cerebellar learning in children with prenatal alcohol exposure: a comparative study of eyeblink conditioning in children with ADHD and dyslexia. Cortex, 41, 389–398.PubMedCrossRef
go back to reference Coles, C. D., Brown, R. T., Smith, I. E., Platzman, K. A., Erickson, S., & Falek, A. (1991). Effects of prenatal alcohol exposure at school age. I. Physical and cognitive development. Neurotoxicology and Teratology, 13, 357–367.PubMedCrossRef Coles, C. D., Brown, R. T., Smith, I. E., Platzman, K. A., Erickson, S., & Falek, A. (1991). Effects of prenatal alcohol exposure at school age. I. Physical and cognitive development. Neurotoxicology and Teratology, 13, 357–367.PubMedCrossRef
go back to reference Coles, C. D., Platzman, K. A., Raskind-Hood, C. L., Brown, R. T., Falek, A., & Smith, I. E. (1997). A comparison of children affected by prenatal alcohol exposure and attention deficit, hyperactivity disorder. Alcoholism, Clinical and Experimental Research, 20, 150–161.CrossRef Coles, C. D., Platzman, K. A., Raskind-Hood, C. L., Brown, R. T., Falek, A., & Smith, I. E. (1997). A comparison of children affected by prenatal alcohol exposure and attention deficit, hyperactivity disorder. Alcoholism, Clinical and Experimental Research, 20, 150–161.CrossRef
go back to reference Coles, C. D., Platzman, K. A., Lynch, M. E., & Freides, D. (2002). Auditory and visual sustained attention in adolescents prenatally exposed to alcohol. Alcoholism, Clinical and Experimental Research, 26, 263–271.PubMedCrossRef Coles, C. D., Platzman, K. A., Lynch, M. E., & Freides, D. (2002). Auditory and visual sustained attention in adolescents prenatally exposed to alcohol. Alcoholism, Clinical and Experimental Research, 26, 263–271.PubMedCrossRef
go back to reference Coles, C. D., Lynch, M. E., Kable, J. A., Johnson, K. C., & Goldstein, F. C. (2010). Verbal and nonverbal memory in adults prenatally exposed to alcohol. Alcoholism, Clinical and Experimental Research, 34(5), 897–906.PubMedCrossRef Coles, C. D., Lynch, M. E., Kable, J. A., Johnson, K. C., & Goldstein, F. C. (2010). Verbal and nonverbal memory in adults prenatally exposed to alcohol. Alcoholism, Clinical and Experimental Research, 34(5), 897–906.PubMedCrossRef
go back to reference Croxford, J., & Viljoen, D. (1999). Alcohol consumption by pregnant women in the Western Cape. South African Medical Journal, 89, 962–965.PubMed Croxford, J., & Viljoen, D. (1999). Alcohol consumption by pregnant women in the Western Cape. South African Medical Journal, 89, 962–965.PubMed
go back to reference Dehaene, S., & Cohen, L. (1995). Towards an anatomical and functional model of number processing. Mathematical Cognition, 1, 83–120. Dehaene, S., & Cohen, L. (1995). Towards an anatomical and functional model of number processing. Mathematical Cognition, 1, 83–120.
go back to reference Dehaene, S., Piazza, M., Pinel, P., & Cohen, L. (2003). Three parietal circuits for number processing. Cognitive Neuropsychology, 20, 487–506.PubMedCrossRef Dehaene, S., Piazza, M., Pinel, P., & Cohen, L. (2003). Three parietal circuits for number processing. Cognitive Neuropsychology, 20, 487–506.PubMedCrossRef
go back to reference Dehaene, S., Molko, N., Cohen, L., & Wilson, A. J. (2004). Arithmetic and the brain. Current Opinion in Neurobiology, 14, 218–224.PubMedCrossRef Dehaene, S., Molko, N., Cohen, L., & Wilson, A. J. (2004). Arithmetic and the brain. Current Opinion in Neurobiology, 14, 218–224.PubMedCrossRef
go back to reference Dikranian, K., Qin, Y. Q., Labruyere, J., Nemmers, B., & Olney, J. W. (2005). Ethanol-induced neuroapoptosis in the developing rodent cerebellum and related brain structures. Developmental Brain Research, 155, 1–13.PubMedCrossRef Dikranian, K., Qin, Y. Q., Labruyere, J., Nemmers, B., & Olney, J. W. (2005). Ethanol-induced neuroapoptosis in the developing rodent cerebellum and related brain structures. Developmental Brain Research, 155, 1–13.PubMedCrossRef
go back to reference Diwadkar, V., Meintjes, E. M., Goradia, D., Dodge, N. C., Warton, C., Molteno, C., et al. (in press). Children with FAS and PFAS recruit different working memory brain regions than alcohol-exposed nonsyndromal children. Alcoholism: Clinical and Experimental Research, 35. Diwadkar, V., Meintjes, E. M., Goradia, D., Dodge, N. C., Warton, C., Molteno, C., et al. (in press). Children with FAS and PFAS recruit different working memory brain regions than alcohol-exposed nonsyndromal children. Alcoholism: Clinical and Experimental Research, 35.
go back to reference Dunty, W. C., Chen, S.-Y., Zucker, R. M., Dehart, D. B., & Sulik, K. K. (2001). Selective vulnerability of embryonic cell populations to ethanol-induced apoptosis: implications for alcohol-related birth defects and neurodevelopmental disorder. Alcoholism, Clinical and Experimental Research, 25, 1523–1535.PubMedCrossRef Dunty, W. C., Chen, S.-Y., Zucker, R. M., Dehart, D. B., & Sulik, K. K. (2001). Selective vulnerability of embryonic cell populations to ethanol-induced apoptosis: implications for alcohol-related birth defects and neurodevelopmental disorder. Alcoholism, Clinical and Experimental Research, 25, 1523–1535.PubMedCrossRef
go back to reference Eger, E., Sterzer, P., Russ, M. O., Giraud, A. L., & Kleinschmidt, A. (2003). A supramodal number representation in human intraparietal cortex. Neuron, 37, 719–725.PubMedCrossRef Eger, E., Sterzer, P., Russ, M. O., Giraud, A. L., & Kleinschmidt, A. (2003). A supramodal number representation in human intraparietal cortex. Neuron, 37, 719–725.PubMedCrossRef
go back to reference Fletcher, P. C., Shallice, T., Frith, C. D., Frackowiak, R. S. J., & Dolan, R. J. (1996). Brain activity during memory retrieval—the influence of imagery and semantic cueing. Brain, 119, 1587–1596.PubMedCrossRef Fletcher, P. C., Shallice, T., Frith, C. D., Frackowiak, R. S. J., & Dolan, R. J. (1996). Brain activity during memory retrieval—the influence of imagery and semantic cueing. Brain, 119, 1587–1596.PubMedCrossRef
go back to reference Frings, M., Gaertner, K., Buderath, P., Gerwig, M., Christiansen, H., Schoch, B., et al. (2010). Timing of conditioned eyeblink responses is impaired in children with attention-deficit/hyperactivity disorder. Experimental Brain Research, 201, 167–176.CrossRef Frings, M., Gaertner, K., Buderath, P., Gerwig, M., Christiansen, H., Schoch, B., et al. (2010). Timing of conditioned eyeblink responses is impaired in children with attention-deficit/hyperactivity disorder. Experimental Brain Research, 201, 167–176.CrossRef
go back to reference Fryer, S. L., Tapert, S. F., Mattson, S. N., Paulus, M. P., Spadoni, A. D., & Riley, E. P. (2007). Prenatal alcohol exposure affects frontal-striatal BOLD response during inhibitory control. Alcoholism, Clinical and Experimental Research, 31, 1415–1424.PubMedCrossRef Fryer, S. L., Tapert, S. F., Mattson, S. N., Paulus, M. P., Spadoni, A. D., & Riley, E. P. (2007). Prenatal alcohol exposure affects frontal-striatal BOLD response during inhibitory control. Alcoholism, Clinical and Experimental Research, 31, 1415–1424.PubMedCrossRef
go back to reference Fryer, S. L., Schweinsburg, B. C., Bjorkquist, O. A., Frank, L. R., Mattson, S. N., Spadoni, A. D., et al. (2009). Characterization of white matter microstructure in fetal alcohol spectrum disorders. Alcoholism, Clinical and Experimental Research, 33, 514–521.PubMedCrossRef Fryer, S. L., Schweinsburg, B. C., Bjorkquist, O. A., Frank, L. R., Mattson, S. N., Spadoni, A. D., et al. (2009). Characterization of white matter microstructure in fetal alcohol spectrum disorders. Alcoholism, Clinical and Experimental Research, 33, 514–521.PubMedCrossRef
go back to reference Geinisman, Y., Berry, R. W., Disterhoft, J. F., Power, J. M., & Van der Zee, E. A. (2001). Associative learning elicits the formation of multiple-synapse boutons. The Journal of Neuroscience, 21, 5568–5573.PubMed Geinisman, Y., Berry, R. W., Disterhoft, J. F., Power, J. M., & Van der Zee, E. A. (2001). Associative learning elicits the formation of multiple-synapse boutons. The Journal of Neuroscience, 21, 5568–5573.PubMed
go back to reference Goldschmidt, L., Richardson, G. A., Stoffer, D. S., Geva, D., & Day, N. L. (1996). Prenatal alcohol exposure and academic achievement at age six: a nonlinear fit. Alcoholism, Clinical and Experimental Research, 20, 763–770.PubMedCrossRef Goldschmidt, L., Richardson, G. A., Stoffer, D. S., Geva, D., & Day, N. L. (1996). Prenatal alcohol exposure and academic achievement at age six: a nonlinear fit. Alcoholism, Clinical and Experimental Research, 20, 763–770.PubMedCrossRef
go back to reference Goodlett, C. R., Marcussen, B. L., & West, J. R. (1990). A single day of alcohol exposure during the brain growth spurt induces brain weight restriction and cerebellar Purkinje loss. Alcohol, 7, 107–114.PubMedCrossRef Goodlett, C. R., Marcussen, B. L., & West, J. R. (1990). A single day of alcohol exposure during the brain growth spurt induces brain weight restriction and cerebellar Purkinje loss. Alcohol, 7, 107–114.PubMedCrossRef
go back to reference Gottesman, I. I., & Gould, T. D. (2003). The endophenotype concept in psychiatry: etymology and strategic intentions. The American Journal of Psychiatry, 160, 636–645.PubMedCrossRef Gottesman, I. I., & Gould, T. D. (2003). The endophenotype concept in psychiatry: etymology and strategic intentions. The American Journal of Psychiatry, 160, 636–645.PubMedCrossRef
go back to reference Gould, E., Beylin, A., Tanapat, P., Reeves, A., & Shors, T. J. (1999). Learning enhances adult neurogenesis in the hippocampal formation. Nature Neuroscience, 2, 260–265.PubMedCrossRef Gould, E., Beylin, A., Tanapat, P., Reeves, A., & Shors, T. J. (1999). Learning enhances adult neurogenesis in the hippocampal formation. Nature Neuroscience, 2, 260–265.PubMedCrossRef
go back to reference Green, J. T., Rogers, R. F., Goodlett, C. R., & Steinmetz, J. E. (2000). Impairment in eyeblink classical conditioning in adult rats exposed to ethanol as neonates. Alcoholism, Clinical and Experimental Research, 24, 438–447.PubMedCrossRef Green, J. T., Rogers, R. F., Goodlett, C. R., & Steinmetz, J. E. (2000). Impairment in eyeblink classical conditioning in adult rats exposed to ethanol as neonates. Alcoholism, Clinical and Experimental Research, 24, 438–447.PubMedCrossRef
go back to reference Green, J. T., Johnson, T. B., Goodlett, C. R., & Steinmetz, J. E. (2002a). Eyeblink classical conditioning and interpositus nucleus activity are disrupted in adult rats exposed to ethanol as neonates. Learning & Memory, 9, 304–320.CrossRef Green, J. T., Johnson, T. B., Goodlett, C. R., & Steinmetz, J. E. (2002a). Eyeblink classical conditioning and interpositus nucleus activity are disrupted in adult rats exposed to ethanol as neonates. Learning & Memory, 9, 304–320.CrossRef
go back to reference Green, J. T., Tran, T., Steinmetz, J. E., & Goodlett, C. R. (2002b). Neonatal ethanol produces cerebellar deep nuclear loss and correlated disruption of eyeblink conditioning in adult rats. Brain Research, 956, 302–311.CrossRef Green, J. T., Tran, T., Steinmetz, J. E., & Goodlett, C. R. (2002b). Neonatal ethanol produces cerebellar deep nuclear loss and correlated disruption of eyeblink conditioning in adult rats. Brain Research, 956, 302–311.CrossRef
go back to reference Gruber, O., Indefrey, P., Steinmetz, H., & Kleinschmidt, A. (2001). Dissociating neural correlates of cognitive components in mental calculation. Cerebral Cortex, 11, 350–359.PubMedCrossRef Gruber, O., Indefrey, P., Steinmetz, H., & Kleinschmidt, A. (2001). Dissociating neural correlates of cognitive components in mental calculation. Cerebral Cortex, 11, 350–359.PubMedCrossRef
go back to reference Guerri, C., Pascual, M., & Renau-Piqueras, J. (2001). Glia and fetal alcohol syndrome. Neurotoxicology, 22, 593–599.PubMedCrossRef Guerri, C., Pascual, M., & Renau-Piqueras, J. (2001). Glia and fetal alcohol syndrome. Neurotoxicology, 22, 593–599.PubMedCrossRef
go back to reference Hamre, K. M., & West, J. R. (1993). The effects of the timing of ethanol exposure during the brain growth spurt on the number of cerebellar Purkinje and granule cell nuclear profiles. Alcoholism, Clinical and Experimental Research, 17, 610–622.PubMedCrossRef Hamre, K. M., & West, J. R. (1993). The effects of the timing of ethanol exposure during the brain growth spurt on the number of cerebellar Purkinje and granule cell nuclear profiles. Alcoholism, Clinical and Experimental Research, 17, 610–622.PubMedCrossRef
go back to reference Herbert, J. S., Eckerman, C. O., & Stanton, M. E. (2003). The ontogeny of human learning in delay, long-delay, and trace eyeblink conditioning. Behavioral Neuroscience, 117, 1196–1210.PubMedCrossRef Herbert, J. S., Eckerman, C. O., & Stanton, M. E. (2003). The ontogeny of human learning in delay, long-delay, and trace eyeblink conditioning. Behavioral Neuroscience, 117, 1196–1210.PubMedCrossRef
go back to reference Holzman, C., Paneth, N., Little, R., & Pinto-Martin, J. (1995). Perinatal brain injury in premature infants born to mothers using alcohol in pregnancy. Pediatrics, 95, 66–73.PubMed Holzman, C., Paneth, N., Little, R., & Pinto-Martin, J. (1995). Perinatal brain injury in premature infants born to mothers using alcohol in pregnancy. Pediatrics, 95, 66–73.PubMed
go back to reference Howell, K. K., Lynch, M. E., Platzman, K. A., Smith, G. H., & Coles, C. D. (2006). Prenatal alcohol exposure and ability, academic achievement, and school functioning in adolescence: a longitudinal follow-up. Journal of Pediatric Psychology, 311, 16–126. Howell, K. K., Lynch, M. E., Platzman, K. A., Smith, G. H., & Coles, C. D. (2006). Prenatal alcohol exposure and ability, academic achievement, and school functioning in adolescence: a longitudinal follow-up. Journal of Pediatric Psychology, 311, 16–126.
go back to reference Hoyme, H. E., May, P. A., Kalberg, W. O., Kodituwakku, P., Gossage, J. P., Trujillo, P. M., et al. (2005). A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: clarification of the 1996 Institute of Medicine criteria. Pediatrics, 115, 39–47.PubMedCrossRef Hoyme, H. E., May, P. A., Kalberg, W. O., Kodituwakku, P., Gossage, J. P., Trujillo, P. M., et al. (2005). A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: clarification of the 1996 Institute of Medicine criteria. Pediatrics, 115, 39–47.PubMedCrossRef
go back to reference Ivkovich, D., & Stanton, M. E. (2001). Effects of early hippocampal lesions on trace, delay, and long-delay eyeblink conditioning in developing rats. Neurobiology of Learning and Memory, 76, 426–446.PubMedCrossRef Ivkovich, D., & Stanton, M. E. (2001). Effects of early hippocampal lesions on trace, delay, and long-delay eyeblink conditioning in developing rats. Neurobiology of Learning and Memory, 76, 426–446.PubMedCrossRef
go back to reference Ivkovich, D., Paczkowski, C. M., & Stanton, M. E. (2000). Ontogeny of delay versus trace eyeblink conditioning in the rat. Developmental Psychobiology, 36, 148–160.PubMedCrossRef Ivkovich, D., Paczkowski, C. M., & Stanton, M. E. (2000). Ontogeny of delay versus trace eyeblink conditioning in the rat. Developmental Psychobiology, 36, 148–160.PubMedCrossRef
go back to reference Ivry, R. B., Justus, T. C., & Middleton, C. (2001). The cerebellum, timing, and language: Implications for the study of dyslexia. In M. Wolf (Ed.), Dyslexia, fluency, and the brain (pp. 189–211). Timonium: York Press. Ivry, R. B., Justus, T. C., & Middleton, C. (2001). The cerebellum, timing, and language: Implications for the study of dyslexia. In M. Wolf (Ed.), Dyslexia, fluency, and the brain (pp. 189–211). Timonium: York Press.
go back to reference Jacobson, S. W., Jacobson, J. L., Sokol, R. J., & Ager, J. W. (1993). Prenatal alcohol exposure and infant information processing ability. Child Development, 64, 1706–1721.PubMedCrossRef Jacobson, S. W., Jacobson, J. L., Sokol, R. J., & Ager, J. W. (1993). Prenatal alcohol exposure and infant information processing ability. Child Development, 64, 1706–1721.PubMedCrossRef
go back to reference Jacobson, S. W., Jacobson, J. L., & Sokol, R. J. (1994). Effects of fetal alcohol exposure on infant reaction time. Alcoholism, Clinical and Experimental Research, 18, 1125–1132.PubMedCrossRef Jacobson, S. W., Jacobson, J. L., & Sokol, R. J. (1994). Effects of fetal alcohol exposure on infant reaction time. Alcoholism, Clinical and Experimental Research, 18, 1125–1132.PubMedCrossRef
go back to reference Jacobson, S. W., Chiodo, L. M., Sokol, R. J., & Jacobson, J. L. (2002a). Validity of maternal report of prenatal alcohol, cocaine, and smoking in relation to neurobehavioral outcome. Pediatrics, 109, 815–825.CrossRef Jacobson, S. W., Chiodo, L. M., Sokol, R. J., & Jacobson, J. L. (2002a). Validity of maternal report of prenatal alcohol, cocaine, and smoking in relation to neurobehavioral outcome. Pediatrics, 109, 815–825.CrossRef
go back to reference Jacobson, S. W., Hay, A., Molteno, C., Marais, A. S., Carter, R. C., September, M., et al. (2002b). FAS and neurobehavioral deficits in alcohol-exposed South African infants. Alcoholism, Clinical and Experimental Research, 26, 175A. Jacobson, S. W., Hay, A., Molteno, C., Marais, A. S., Carter, R. C., September, M., et al. (2002b). FAS and neurobehavioral deficits in alcohol-exposed South African infants. Alcoholism, Clinical and Experimental Research, 26, 175A.
go back to reference Jacobson, S. W., Jacobson, J. L., Sokol, R. J., Chiodo, L. M., & Corobana, R. (2004). Maternal age, alcohol abuse history, and quality of parenting as moderators of the effects of prenatal alcohol exposure on 7.5-year intellectual function. Alcoholism, Clinical and Experimental Research, 28, 1732–1745.PubMedCrossRef Jacobson, S. W., Jacobson, J. L., Sokol, R. J., Chiodo, L. M., & Corobana, R. (2004). Maternal age, alcohol abuse history, and quality of parenting as moderators of the effects of prenatal alcohol exposure on 7.5-year intellectual function. Alcoholism, Clinical and Experimental Research, 28, 1732–1745.PubMedCrossRef
go back to reference Jacobson, J. L., Jacobson, S. W., Molteno, C. D., & Odendaal, H. (2006a). A prospective examination of the incidence of heavy drinking during pregnancy among Cape Coloured South African women. Alcoholism, Clinical and Experimental Research, 30, 233A.CrossRef Jacobson, J. L., Jacobson, S. W., Molteno, C. D., & Odendaal, H. (2006a). A prospective examination of the incidence of heavy drinking during pregnancy among Cape Coloured South African women. Alcoholism, Clinical and Experimental Research, 30, 233A.CrossRef
go back to reference Jacobson, S. W., Carr, L. G., Croxford, J., Sokol, R. J., Li, T.-K., & Jacobson, J. L. (2006b). Protective effects of the alcohol dehydrogenase-ADH1B allele in African American children exposed to alcohol during pregnancy. The Journal of Pediatrics, 148, 30–37.CrossRef Jacobson, S. W., Carr, L. G., Croxford, J., Sokol, R. J., Li, T.-K., & Jacobson, J. L. (2006b). Protective effects of the alcohol dehydrogenase-ADH1B allele in African American children exposed to alcohol during pregnancy. The Journal of Pediatrics, 148, 30–37.CrossRef
go back to reference Jacobson, S. W., Stanton, M. E., Molteno, C. D., Burden, M. J., Fuller, D. S., Hoyme, H. E., et al. (2008). Impaired eyeblink conditioning in children with fetal alcohol syndrome. Alcoholism, Clinical and Experimental Research, 32, 365–372.PubMedCrossRef Jacobson, S. W., Stanton, M. E., Molteno, C. D., Burden, M. J., Fuller, D. S., Hoyme, H. E., et al. (2008). Impaired eyeblink conditioning in children with fetal alcohol syndrome. Alcoholism, Clinical and Experimental Research, 32, 365–372.PubMedCrossRef
go back to reference Jacobson, J. L., Jacobson, S. W., Dodge, N. C., Klorman, R., & Burden, M. J. (2011a). Number processing in adolescents with prenatal alcohol exposure and ADHD: differences in the neurobehavioral phenotype. Alcoholism, Clinical and Experimental Research, 35, 431–442.CrossRef Jacobson, J. L., Jacobson, S. W., Dodge, N. C., Klorman, R., & Burden, M. J. (2011a). Number processing in adolescents with prenatal alcohol exposure and ADHD: differences in the neurobehavioral phenotype. Alcoholism, Clinical and Experimental Research, 35, 431–442.CrossRef
go back to reference Jacobson, S. W., Stanton, M. E., Dodge, N. C., Fuller, D. S., Molteno, C. D., Meintjes, E. M., et al. (2011b). Impaired short delay and trace eyeblink conditioning in school-age children with fetal alcohol syndrome. Alcoholism, Clinical and Experimental Research, 35, 250–264.CrossRef Jacobson, S. W., Stanton, M. E., Dodge, N. C., Fuller, D. S., Molteno, C. D., Meintjes, E. M., et al. (2011b). Impaired short delay and trace eyeblink conditioning in school-age children with fetal alcohol syndrome. Alcoholism, Clinical and Experimental Research, 35, 250–264.CrossRef
go back to reference Jirikowic, T. L., McCoy, S. W., Price, R., Dellon, B., Vilnai, A. L., Ciol, M., et al. (2010). Sensorimotor Training to Affect Balance Engagement and Learning (STABEL). Taking the new step: Innovative interventions for fetal alcohol spectrum disorders, Emory University, Atlanta, GA. Jirikowic, T. L., McCoy, S. W., Price, R., Dellon, B., Vilnai, A. L., Ciol, M., et al. (2010). Sensorimotor Training to Affect Balance Engagement and Learning (STABEL). Taking the new step: Innovative interventions for fetal alcohol spectrum disorders, Emory University, Atlanta, GA.
go back to reference Jones, K. L., & Smith, D. W. (1973). Recognition of the fetal alcohol syndrome in early infancy. Lancet, 2, 999–1001.CrossRef Jones, K. L., & Smith, D. W. (1973). Recognition of the fetal alcohol syndrome in early infancy. Lancet, 2, 999–1001.CrossRef
go back to reference Kable, J. A., Coles, C. D., & Taddeo, E. (2007). Socio-cognitive habilitation using the math interactive learning experience program for alcohol-affected children. Alcoholism, Clinical and Experimental Research, 31, 1425–1434.PubMedCrossRef Kable, J. A., Coles, C. D., & Taddeo, E. (2007). Socio-cognitive habilitation using the math interactive learning experience program for alcohol-affected children. Alcoholism, Clinical and Experimental Research, 31, 1425–1434.PubMedCrossRef
go back to reference Kaemingk, K. L., Mulvaney, S., & Halverson, P. T. (2003). Learning following prenatal alcohol exposure: performance on verbal and visual multitrial tasks. Archives of Clinical Neuropsychology, 18, 33–47.PubMed Kaemingk, K. L., Mulvaney, S., & Halverson, P. T. (2003). Learning following prenatal alcohol exposure: performance on verbal and visual multitrial tasks. Archives of Clinical Neuropsychology, 18, 33–47.PubMed
go back to reference Kaufman, L., Koppelstaetter, F., Siedentopf, C., Haala, I., Haberlandt, E., Zimmerhackl, L., et al. (2006). Neural correlates of the number-size interference task in children. Neuroreport, 17, 587–591.CrossRef Kaufman, L., Koppelstaetter, F., Siedentopf, C., Haala, I., Haberlandt, E., Zimmerhackl, L., et al. (2006). Neural correlates of the number-size interference task in children. Neuroreport, 17, 587–591.CrossRef
go back to reference Kawashima, R., Taira, M., Okita, K., Inoue, K., Tajima, N., Yoshida, H., et al. (2004). A functional MRI study of simple arithmetic—a comparison between children and adults. Cognitive Brain Research, 18, 225–231.CrossRef Kawashima, R., Taira, M., Okita, K., Inoue, K., Tajima, N., Yoshida, H., et al. (2004). A functional MRI study of simple arithmetic—a comparison between children and adults. Cognitive Brain Research, 18, 225–231.CrossRef
go back to reference Kerns, K. A., Don, A., Mateer, C. A., & Streissguth, A. P. (1997). Cognitive deficits in nonretarded adults with Fetal Alcohol Syndrome. Journal of Learning Disabilities, 30, 685–693.PubMedCrossRef Kerns, K. A., Don, A., Mateer, C. A., & Streissguth, A. P. (1997). Cognitive deficits in nonretarded adults with Fetal Alcohol Syndrome. Journal of Learning Disabilities, 30, 685–693.PubMedCrossRef
go back to reference Kim, J. J., & Thompson, R. F. (1997). Cerebellar circuits and synaptic mechanisms involved in classical eyeblink conditioning. Trends in Neuroscience, 20, 177–181.CrossRef Kim, J. J., & Thompson, R. F. (1997). Cerebellar circuits and synaptic mechanisms involved in classical eyeblink conditioning. Trends in Neuroscience, 20, 177–181.CrossRef
go back to reference Kim, J. J., Clark, R. E., & Thompson, R. F. (1995). Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behavioral Neuroscience, 109, 195–203.PubMedCrossRef Kim, J. J., Clark, R. E., & Thompson, R. F. (1995). Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behavioral Neuroscience, 109, 195–203.PubMedCrossRef
go back to reference Kirschen, M. P., Chen, S. H. A., Schraedley-Desmond, P., & Desmond, J. E. (2005). Load- and practice-dependent increases in cerebro-cerebellar activation in verbal working memory: an fMRI study. Neuroimage, 24, 462–472.PubMedCrossRef Kirschen, M. P., Chen, S. H. A., Schraedley-Desmond, P., & Desmond, J. E. (2005). Load- and practice-dependent increases in cerebro-cerebellar activation in verbal working memory: an fMRI study. Neuroimage, 24, 462–472.PubMedCrossRef
go back to reference Klingenberg, C. P., Wetherill, L., Rogers, J., Moore, E., Ward, R., Autti-Ramo, I., et al. (2010). Prenatal alcohol exposure alters the patterns of facial asymmetry. Alcohol, 44, 649–657.PubMedCrossRef Klingenberg, C. P., Wetherill, L., Rogers, J., Moore, E., Ward, R., Autti-Ramo, I., et al. (2010). Prenatal alcohol exposure alters the patterns of facial asymmetry. Alcohol, 44, 649–657.PubMedCrossRef
go back to reference Klintsova, A. Y., Cowell, R. M., Swain, R. A., Napper, R. M. A., Goodlett, C. R., & Greenough, W. T. (1998). Therapeutic effects of complex motor training on motor performance deficits induced by neonatal binge-like alcohol exposure in rats: I. Behavioral results. Brain Research, 800, 48–61.PubMedCrossRef Klintsova, A. Y., Cowell, R. M., Swain, R. A., Napper, R. M. A., Goodlett, C. R., & Greenough, W. T. (1998). Therapeutic effects of complex motor training on motor performance deficits induced by neonatal binge-like alcohol exposure in rats: I. Behavioral results. Brain Research, 800, 48–61.PubMedCrossRef
go back to reference Kodituwakku, P. W., & Kodituwakku, E. L. (2011). From research to practice: An integrative framework for the development of interventions for children with fetal alcohol spectrum disorders. Neuropsychology Review, 21. Kodituwakku, P. W., & Kodituwakku, E. L. (2011). From research to practice: An integrative framework for the development of interventions for children with fetal alcohol spectrum disorders. Neuropsychology Review, 21.
go back to reference Kodituwakku, P. W., Handmaker, N. S., Cutler, S. K., Weathersby, E. K., & Handmaker, S. D. (1995). Specific impairments in self-regulation in children exposed to alcohol prenatally. Alcoholism, Clinical and Experimental Research, 19, 1558–1564.PubMedCrossRef Kodituwakku, P. W., Handmaker, N. S., Cutler, S. K., Weathersby, E. K., & Handmaker, S. D. (1995). Specific impairments in self-regulation in children exposed to alcohol prenatally. Alcoholism, Clinical and Experimental Research, 19, 1558–1564.PubMedCrossRef
go back to reference Koekkoek, S. K. E., Hulscher, H. C., Dortland, B. R., Hensbroek, R. A., Elgersma, Y., Ruigrok, T. J. H., et al. (2003). Cerebellar LTD and learning-dependent timing of conditioned eyelid responses. Science, 301, 1736–1739.PubMedCrossRef Koekkoek, S. K. E., Hulscher, H. C., Dortland, B. R., Hensbroek, R. A., Elgersma, Y., Ruigrok, T. J. H., et al. (2003). Cerebellar LTD and learning-dependent timing of conditioned eyelid responses. Science, 301, 1736–1739.PubMedCrossRef
go back to reference Kooistra, L., Crawford, S., Gibbard, B., Ramage, B., & Kaplan, B. J. (2010). Differentiating attention deficits in children with fetal alcohol spectrum disorder or attention-deficit–hyperactivity disorder. Developmental Medicine and Child Neurology, 52, 205–211.PubMedCrossRef Kooistra, L., Crawford, S., Gibbard, B., Ramage, B., & Kaplan, B. J. (2010). Differentiating attention deficits in children with fetal alcohol spectrum disorder or attention-deficit–hyperactivity disorder. Developmental Medicine and Child Neurology, 52, 205–211.PubMedCrossRef
go back to reference Kopera-Frye, K., Dehaene, S., & Streissguth, A. P. (1996). Impairments of number processing induced by prenatal alcohol exposure. Neuropsychologia, 34, 1187–1196.PubMedCrossRef Kopera-Frye, K., Dehaene, S., & Streissguth, A. P. (1996). Impairments of number processing induced by prenatal alcohol exposure. Neuropsychologia, 34, 1187–1196.PubMedCrossRef
go back to reference Krupa, D. J., Thompson, J. K., & Thompson, R. F. (1993). Localization of a memory trace in the mammalian brain. Science, 260, 989–991.PubMedCrossRef Krupa, D. J., Thompson, J. K., & Thompson, R. F. (1993). Localization of a memory trace in the mammalian brain. Science, 260, 989–991.PubMedCrossRef
go back to reference Kucian, K., Loenneker, T., Dietrich, T., Dosch, M., Martin, E., & von Aster, M. (2006). Impaired neural networks for approximate calculation in dyscalculic children: a functional MRI study. Behavioral Brain Functions, 2, 31–48.CrossRef Kucian, K., Loenneker, T., Dietrich, T., Dosch, M., Martin, E., & von Aster, M. (2006). Impaired neural networks for approximate calculation in dyscalculic children: a functional MRI study. Behavioral Brain Functions, 2, 31–48.CrossRef
go back to reference Lavond, D. G., & Steinmetz, J. E. (1989). Acquisition of classical conditioning without cerebellar cortex. Behavioral Brain Research, 33, 113–164.CrossRef Lavond, D. G., & Steinmetz, J. E. (1989). Acquisition of classical conditioning without cerebellar cortex. Behavioral Brain Research, 33, 113–164.CrossRef
go back to reference Lavond, D. G., Kim, J. J., & Thompson, R. F. (1993). Mammalian brain substrates of aversive classical conditioning. Annual Reviews in Psychology, 44, 317–342.CrossRef Lavond, D. G., Kim, J. J., & Thompson, R. F. (1993). Mammalian brain substrates of aversive classical conditioning. Annual Reviews in Psychology, 44, 317–342.CrossRef
go back to reference Lebel, C., Rasmussen, C., Wyper, K., Walker, L., Andrew, G., Yager, J., et al. (2008). Brain diffusion abnormalities in children with fetal alcohol spectrum disorder. Alcoholism, Clinical and Experimental Research, 22, 1–9. Lebel, C., Rasmussen, C., Wyper, K., Walker, L., Andrew, G., Yager, J., et al. (2008). Brain diffusion abnormalities in children with fetal alcohol spectrum disorder. Alcoholism, Clinical and Experimental Research, 22, 1–9.
go back to reference 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. Alcoholism, Clinical and Experimental Research, 34, 354–363.PubMedCrossRef 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. Alcoholism, Clinical and Experimental Research, 34, 354–363.PubMedCrossRef
go back to reference 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. 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.
go back to reference Lemoine, P., Harousseau, H., Borteyru, J. P., & Menuet, J. C. (1968). Les enfants de parents alcooliques: anomalies observées. A propos de 127 cas [Children of alcoholic parents: abnormalities observed in 127 cases]. Ouest Medical, 21, 476–482. Lemoine, P., Harousseau, H., Borteyru, J. P., & Menuet, J. C. (1968). Les enfants de parents alcooliques: anomalies observées. A propos de 127 cas [Children of alcoholic parents: abnormalities observed in 127 cases]. Ouest Medical, 21, 476–482.
go back to reference Li, L., Coles, C. D., Lynch, M. E., & Hu, X. (2009). Voxelwise and skeleton-based region of interest analysis of fetal alcohol syndrome and fetal alcohol spectrum disorders in young adults. Human Brain Mapping, 30, 3265–3274.PubMedCrossRef Li, L., Coles, C. D., Lynch, M. E., & Hu, X. (2009). Voxelwise and skeleton-based region of interest analysis of fetal alcohol syndrome and fetal alcohol spectrum disorders in young adults. Human Brain Mapping, 30, 3265–3274.PubMedCrossRef
go back to reference Logan, C. G., & Grafton, S. T. (1995). Functional anatomy of human eyeblink conditioning determined with regional cerebral glucose metabolism and positron-emission tomography. Proceedings of the National Academy of Sciences of the United States of America, 92, 7500–7504.PubMedCrossRef Logan, C. G., & Grafton, S. T. (1995). Functional anatomy of human eyeblink conditioning determined with regional cerebral glucose metabolism and positron-emission tomography. Proceedings of the National Academy of Sciences of the United States of America, 92, 7500–7504.PubMedCrossRef
go back to reference Ma, X., Coles, C. D., Lynch, M. E., LaConte, S. M., Zurkiya, O., Wang, D., et al. (2005). Evaluation of corpus callosum anisotropy in young adults with fetal alcohol syndrome according to diffusion tensor imaging. Alcoholism, Clinical and Experimental Research, 29, 1214–1222.PubMedCrossRef Ma, X., Coles, C. D., Lynch, M. E., LaConte, S. M., Zurkiya, O., Wang, D., et al. (2005). Evaluation of corpus callosum anisotropy in young adults with fetal alcohol syndrome according to diffusion tensor imaging. Alcoholism, Clinical and Experimental Research, 29, 1214–1222.PubMedCrossRef
go back to reference Maier, S. E., & West, J. R. (2001). Regional differences in cell loss associated with binge-like alcohol exposure during the first two trimesters equivalent in the rat. Alcohol, 23, 49–57.PubMedCrossRef Maier, S. E., & West, J. R. (2001). Regional differences in cell loss associated with binge-like alcohol exposure during the first two trimesters equivalent in the rat. Alcohol, 23, 49–57.PubMedCrossRef
go back to reference Maier, S. E., Miller, J. A., Blackwell, J. M., & West, J. R. (1999). Fetal alcohol exposure and temporal vulnerability: regional differences in cell loss as a function of the timing of binge-like alcohol exposure during brain development. Alcoholism, Clinical and Experimental Research, 23, 726–734.PubMed Maier, S. E., Miller, J. A., Blackwell, J. M., & West, J. R. (1999). Fetal alcohol exposure and temporal vulnerability: regional differences in cell loss as a function of the timing of binge-like alcohol exposure during brain development. Alcoholism, Clinical and Experimental Research, 23, 726–734.PubMed
go back to reference Marcussen, B. L., Goodlett, C. R., Mahoney, J. C., & West, J. R. (1994). Developing rat Purkinje cells are more vulnerable to alcohol-induced depletion during differentiation than during neurogenesis. Alcohol, 11, 147–156.PubMedCrossRef Marcussen, B. L., Goodlett, C. R., Mahoney, J. C., & West, J. R. (1994). Developing rat Purkinje cells are more vulnerable to alcohol-induced depletion during differentiation than during neurogenesis. Alcohol, 11, 147–156.PubMedCrossRef
go back to reference Markham, M. R., Miller, W. R., & Arciniega, L. (1993). BaCCus 2.01 computer software for quantifying alcohol consumption. Behavioral Research Methods: Instruments and Computers, 25, 420–421.CrossRef Markham, M. R., Miller, W. R., & Arciniega, L. (1993). BaCCus 2.01 computer software for quantifying alcohol consumption. Behavioral Research Methods: Instruments and Computers, 25, 420–421.CrossRef
go back to reference Mattson, S. N., & Roebuck, T. M. (2002). Acquisition and retention of verbal and nonverbal information in children with heavy prenatal alcohol exposure. Alcoholism, Clinical and Experimental Research, 26, 875–882.PubMedCrossRef Mattson, S. N., & Roebuck, T. M. (2002). Acquisition and retention of verbal and nonverbal information in children with heavy prenatal alcohol exposure. Alcoholism, Clinical and Experimental Research, 26, 875–882.PubMedCrossRef
go back to reference Mattson, S. N., Riley, E. P., Delis, D. C., Stern, C., & Jones, K. L. (1996). Verbal learning and memory in children with fetal alcohol syndrome. Alcoholism, Clinical and Experimental Research, 20, 810–816.PubMedCrossRef Mattson, S. N., Riley, E. P., Delis, D. C., Stern, C., & Jones, K. L. (1996). Verbal learning and memory in children with fetal alcohol syndrome. Alcoholism, Clinical and Experimental Research, 20, 810–816.PubMedCrossRef
go back to reference Mattson, S. N., Goodman, A. M., Caine, C., Delis, D. C., & Riley, E. P. (1999). Executive functioning in children with heavy prenatal alcohol exposure. Alcoholism, Clinical and Experimental Research, 23, 1808–1815.PubMedCrossRef Mattson, S. N., Goodman, A. M., Caine, C., Delis, D. C., & Riley, E. P. (1999). Executive functioning in children with heavy prenatal alcohol exposure. Alcoholism, Clinical and Experimental Research, 23, 1808–1815.PubMedCrossRef
go back to reference Mattson, S. N., Crocker, N., & Nguyen, T. T. (2011). Fetal alcohol spectrum disorders: Neuropsychological and behavioral features. Neuropsychology Review, 21 doi:10.1007/s11065-011-9167-9. Mattson, S. N., Crocker, N., & Nguyen, T. T. (2011). Fetal alcohol spectrum disorders: Neuropsychological and behavioral features. Neuropsychology Review, 21 doi:10.​1007/​s11065-011-9167-9.
go back to reference May, P. A., Brooke, L., Gossage, J. P., Croxford, J., Adnams, C., Jones, K. L., et al. (2000). Epidemiology of fetal alcohol syndrome in a South African community in the Western Cape Province. American Journal of Public Health, 90, 1905–1912.PubMedCrossRef May, P. A., Brooke, L., Gossage, J. P., Croxford, J., Adnams, C., Jones, K. L., et al. (2000). Epidemiology of fetal alcohol syndrome in a South African community in the Western Cape Province. American Journal of Public Health, 90, 1905–1912.PubMedCrossRef
go back to reference McCormick, D. A., & Thompson, R. F. (1984). Neuronal responses of the rabbit cerebellum during acquisition and performance of a classically conditioned nictitating membrane-eyelid response. The Journal of Neuroscience, 4, 2811–2822.PubMed McCormick, D. A., & Thompson, R. F. (1984). Neuronal responses of the rabbit cerebellum during acquisition and performance of a classically conditioned nictitating membrane-eyelid response. The Journal of Neuroscience, 4, 2811–2822.PubMed
go back to reference McEchron, M. D., & Disterhoft, J. F. (1997). Sequence of single neuron changes in CA1 hippocampus of rabbits during acquisition of trace eyeblink conditioned responses. Journal of Neurophysiology, 78, 1030–1044.PubMed McEchron, M. D., & Disterhoft, J. F. (1997). Sequence of single neuron changes in CA1 hippocampus of rabbits during acquisition of trace eyeblink conditioned responses. Journal of Neurophysiology, 78, 1030–1044.PubMed
go back to reference McGlinchey-Berroth, R., Carillo, M. C., Gabrieli, J. D. E., Brawn, C. M., & Disterhoft, J. F. (1997). Impaired trace eyeblink conditioning in bilateral, medial-temporal lobe amnesia. Behavioral Neuroscience, 111, 873–882.PubMedCrossRef McGlinchey-Berroth, R., Carillo, M. C., Gabrieli, J. D. E., Brawn, C. M., & Disterhoft, J. F. (1997). Impaired trace eyeblink conditioning in bilateral, medial-temporal lobe amnesia. Behavioral Neuroscience, 111, 873–882.PubMedCrossRef
go back to reference McGlinchey-Berroth, R., Brawn, C., & Disterhoft, J. F. (1999). Temporal discrimination learning in severe amnesic patients reveals an alteration in the timing of eyeblink conditioned responses. Behavioral Neuroscience, 113, 10–18.PubMedCrossRef McGlinchey-Berroth, R., Brawn, C., & Disterhoft, J. F. (1999). Temporal discrimination learning in severe amnesic patients reveals an alteration in the timing of eyeblink conditioned responses. Behavioral Neuroscience, 113, 10–18.PubMedCrossRef
go back to reference Meintjes, E. M., Jacobson, S. W., Molteno, C. D., Gatenby, J. C., Warton, C., Cannistraci, C. J., et al. (2010a). An fMRI study of number processing in children. Magnetic Resonance Imaging, 28, 351–362.PubMedCrossRef Meintjes, E. M., Jacobson, S. W., Molteno, C. D., Gatenby, J. C., Warton, C., Cannistraci, C. J., et al. (2010a). An fMRI study of number processing in children. Magnetic Resonance Imaging, 28, 351–362.PubMedCrossRef
go back to reference Meintjes, E. M., Jacobson, S. W., Molteno, C. D., Gatenby, J. C., Warton, C., Cannistraci, C. J., et al. (2010b). An fMRI study of number processing in children with fetal alcohol syndrome. Alcoholism, Clinical and Experimental Research, 34, 1450–1464.PubMed Meintjes, E. M., Jacobson, S. W., Molteno, C. D., Gatenby, J. C., Warton, C., Cannistraci, C. J., et al. (2010b). An fMRI study of number processing in children with fetal alcohol syndrome. Alcoholism, Clinical and Experimental Research, 34, 1450–1464.PubMed
go back to reference Menon, V., Rivera, S. M., White, C. D., Glover, G. H., & Reiss, A. L. (2000). Dissociating prefrontal and parietal cortex activation during arithmetic processing. Neuroimage, 12, 357–365.PubMedCrossRef Menon, V., Rivera, S. M., White, C. D., Glover, G. H., & Reiss, A. L. (2000). Dissociating prefrontal and parietal cortex activation during arithmetic processing. Neuroimage, 12, 357–365.PubMedCrossRef
go back to reference Mick, E., Biederman, J., Faraone, S. V., Sayer, J., & Kleinman, S. (2002). Case-control study of attention-deficit hyperactivity disorder and maternal smoking, alcohol use, and drug use during pregnancy. Journal of the American Academy of Child and Adolescent Psychiatry, 41, 378–385.PubMedCrossRef Mick, E., Biederman, J., Faraone, S. V., Sayer, J., & Kleinman, S. (2002). Case-control study of attention-deficit hyperactivity disorder and maternal smoking, alcohol use, and drug use during pregnancy. Journal of the American Academy of Child and Adolescent Psychiatry, 41, 378–385.PubMedCrossRef
go back to reference Miller, M. W., & Al-Rabiai, S. (1994). Effects of prenatal exposure to ethanol on the number of axons in the pyramidal tract of the rat. Alcoholism, Clinical and Experimental Research, 18, 346–354.PubMedCrossRef Miller, M. W., & Al-Rabiai, S. (1994). Effects of prenatal exposure to ethanol on the number of axons in the pyramidal tract of the rat. Alcoholism, Clinical and Experimental Research, 18, 346–354.PubMedCrossRef
go back to reference Miller, M. W., & Robertson, S. (1993). Prenatal exposure to ethanol alters the postnatal development and transformation of radial glia to astrocytes in the cortex. The Journal of Comparative Neurology, 337, 253–266.PubMedCrossRef Miller, M. W., & Robertson, S. (1993). Prenatal exposure to ethanol alters the postnatal development and transformation of radial glia to astrocytes in the cortex. The Journal of Comparative Neurology, 337, 253–266.PubMedCrossRef
go back to reference Miller, M. J., Chen, N., Li, L., Tom, B., Weiss, C., Disterhoft, J. F., et al. (2003). FMRI of the conscious rabbit during unilateral classical eyeblink conditioning reveals bilateral cerebellar activation. The Journal of Neuroscience, 23, 11753–11758.PubMed Miller, M. J., Chen, N., Li, L., Tom, B., Weiss, C., Disterhoft, J. F., et al. (2003). FMRI of the conscious rabbit during unilateral classical eyeblink conditioning reveals bilateral cerebellar activation. The Journal of Neuroscience, 23, 11753–11758.PubMed
go back to reference Miller, L. C., Chan, W., Litvinova, A., Rubin, A., Comfort, K., Tirella, L., et al. (2006). Fetal alcohol spectrum disorders in children residing in Russian orphanages: a phenotypic survey. Alcoholism, Clinical and Experimental Research, 30, 531–538.PubMedCrossRef Miller, L. C., Chan, W., Litvinova, A., Rubin, A., Comfort, K., Tirella, L., et al. (2006). Fetal alcohol spectrum disorders in children residing in Russian orphanages: a phenotypic survey. Alcoholism, Clinical and Experimental Research, 30, 531–538.PubMedCrossRef
go back to reference Mix, K., Huttenlocher, J., & Levine, S. (2002). Math without words: Quantitative development in infancy and early childhood. New York: Oxford University Press.CrossRef Mix, K., Huttenlocher, J., & Levine, S. (2002). Math without words: Quantitative development in infancy and early childhood. New York: Oxford University Press.CrossRef
go back to reference Molchan, S. E., Sunderland, T., McIntosh, A. R., Herscovitch, P., & Schreurs, B. G. (1994). A functional anatomical study of associative learning in humans. Proceedings of the National Academy of Sciences of the United States of America, 91, 8122–8126.PubMedCrossRef Molchan, S. E., Sunderland, T., McIntosh, A. R., Herscovitch, P., & Schreurs, B. G. (1994). A functional anatomical study of associative learning in humans. Proceedings of the National Academy of Sciences of the United States of America, 91, 8122–8126.PubMedCrossRef
go back to reference Molteno, C. D., Bromley, K., Thomas, K. G. F., Meintjes, E. M., Jacobson, J. L., & Jacobson, S. W. (in press). Role of processing speed in fetal alcohol impairment of reading comprehension. Alcoholism: Clinical and Experimental Research, 35. Molteno, C. D., Bromley, K., Thomas, K. G. F., Meintjes, E. M., Jacobson, J. L., & Jacobson, S. W. (in press). Role of processing speed in fetal alcohol impairment of reading comprehension. Alcoholism: Clinical and Experimental Research, 35.
go back to reference Moore, E., Ward, R., Wetherill, L. F., Rogers, J. L., Autti-Ramo, I., Fagerlund, A., et al. (2007). Unique facial features distinguish fetal alcohol syndrome patients and controls in diverse ethnic populations. Alcoholism: Clinical and Experimental Research, 31, 1707–1713.CrossRef Moore, E., Ward, R., Wetherill, L. F., Rogers, J. L., Autti-Ramo, I., Fagerlund, A., et al. (2007). Unique facial features distinguish fetal alcohol syndrome patients and controls in diverse ethnic populations. Alcoholism: Clinical and Experimental Research, 31, 1707–1713.CrossRef
go back to reference Moyer, J. R., Deyo, R. A., & Disterhoft, J. F. (1990). Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behavioral Neuroscience, 104, 243–252.PubMedCrossRef Moyer, J. R., Deyo, R. A., & Disterhoft, J. F. (1990). Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behavioral Neuroscience, 104, 243–252.PubMedCrossRef
go back to reference Moyer, J. R., Thompson, L. T., & Disterhoft, J. F. (1996). Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. The Journal of Neuroscience, 16, 5536–5546.PubMed Moyer, J. R., Thompson, L. T., & Disterhoft, J. F. (1996). Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. The Journal of Neuroscience, 16, 5536–5546.PubMed
go back to reference Naccache, L., & Dehaene, S. (2001). The priming method: imaging unconscious repetition priming reveals an abstract representation of number in the parietal lobes. Cerebral Cortex, 11, 966–974.PubMedCrossRef Naccache, L., & Dehaene, S. (2001). The priming method: imaging unconscious repetition priming reveals an abstract representation of number in the parietal lobes. Cerebral Cortex, 11, 966–974.PubMedCrossRef
go back to reference O’Hare, E. D., Lu, L. H., Houston, S. M., Bookheimer, S. Y., Mattson, S. N., O’Connor, M. J., et al. (2009). Altered frontal-parietal functioning during verbal working memory in children and adolescents with heavy prenatal alcohol exposure. Human Brain Mapping, 30, 3200–3208.PubMedCrossRef O’Hare, E. D., Lu, L. H., Houston, S. M., Bookheimer, S. Y., Mattson, S. N., O’Connor, M. J., et al. (2009). Altered frontal-parietal functioning during verbal working memory in children and adolescents with heavy prenatal alcohol exposure. Human Brain Mapping, 30, 3200–3208.PubMedCrossRef
go back to reference O’Leary, C. E., Thomas, K. G. F., Molteno, C. D., Jacobson, J. L., & Jacobson, S. W. (in press). Verbal learning and memory in fetal alcohol spectrum disorder: Findings from Cape Town and Detroit. Alcoholism: Clinical and Experimental Research, 35. O’Leary, C. E., Thomas, K. G. F., Molteno, C. D., Jacobson, J. L., & Jacobson, S. W. (in press). Verbal learning and memory in fetal alcohol spectrum disorder: Findings from Cape Town and Detroit. Alcoholism: Clinical and Experimental Research, 35.
go back to reference Ohyama, T., Nores, W. L., Murphy, M., & Mauk, M. D. (2003). What the cerebellum computes. Trends in Neuroscience, 26, 222–227.CrossRef Ohyama, T., Nores, W. L., Murphy, M., & Mauk, M. D. (2003). What the cerebellum computes. Trends in Neuroscience, 26, 222–227.CrossRef
go back to reference Perrett, S. P., Ruiz, B. P., & Mauk, M. D. (1993). Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. The Journal of Neuroscience, 13, 1708–1718.PubMed Perrett, S. P., Ruiz, B. P., & Mauk, M. D. (1993). Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. The Journal of Neuroscience, 13, 1708–1718.PubMed
go back to reference Pesenti, M., Thioux, M., Seron, X., & De Volder, A. (2000). Neuroanatomical substrates of Arabic number processing, numerical comparison, and simple addition: a PET study. Journal of Cognitive Neuroscience, 12, 461–479.PubMedCrossRef Pesenti, M., Thioux, M., Seron, X., & De Volder, A. (2000). Neuroanatomical substrates of Arabic number processing, numerical comparison, and simple addition: a PET study. Journal of Cognitive Neuroscience, 12, 461–479.PubMedCrossRef
go back to reference Pinel, P., Piazza, M., Le Bihan, D., & Dehaene, S. (2004). Distributed and overlapping cerebral representations of number, size, and luminance during comparative judgments. Neuroimage, 41, 983–993. Pinel, P., Piazza, M., Le Bihan, D., & Dehaene, S. (2004). Distributed and overlapping cerebral representations of number, size, and luminance during comparative judgments. Neuroimage, 41, 983–993.
go back to reference Port, R. L., Romano, A. G., Steinmetz, J. E., Mikhail, A. A., & Patterson, M. M. (1986). Retention and acquisition of classical trace conditioned responses by rabbits with hippocampal lesions. Behavioral Neuroscience, 100, 745–752.PubMedCrossRef Port, R. L., Romano, A. G., Steinmetz, J. E., Mikhail, A. A., & Patterson, M. M. (1986). Retention and acquisition of classical trace conditioned responses by rabbits with hippocampal lesions. Behavioral Neuroscience, 100, 745–752.PubMedCrossRef
go back to reference Power, J. M., Thompson, L. T., Moyer, J. M., & Disterhoft, J. F. (1997). Enhanced synaptic transmission in CA1 hippocampus after eyeblink conditioning. Journal of Neurophysiology, 78, 1184–1187.PubMed Power, J. M., Thompson, L. T., Moyer, J. M., & Disterhoft, J. F. (1997). Enhanced synaptic transmission in CA1 hippocampus after eyeblink conditioning. Journal of Neurophysiology, 78, 1184–1187.PubMed
go back to reference Rasmussen, C., & Bisanz, J. (2009). Exploring mathematics difficulties in children with fetal alcohol spectrum disorders. Child Development Perspectives, 3, 125–130.CrossRef Rasmussen, C., & Bisanz, J. (2009). Exploring mathematics difficulties in children with fetal alcohol spectrum disorders. Child Development Perspectives, 3, 125–130.CrossRef
go back to reference Ridderinkhof, K. R., Ullsperger, M., Crone, E. A., & Nieuwenhuis, S. (2004). The role of the medial frontal cortex in cognitive control. Science, 306, 443–447.PubMedCrossRef Ridderinkhof, K. R., Ullsperger, M., Crone, E. A., & Nieuwenhuis, S. (2004). The role of the medial frontal cortex in cognitive control. Science, 306, 443–447.PubMedCrossRef
go back to reference Ross, S. M., & Ross, L. E. (1971). Comparison of trace and delay classical eyelid conditioning as a function of interstimulus interval. Journal of Experimental Psychology, 91, 165–167.PubMedCrossRef Ross, S. M., & Ross, L. E. (1971). Comparison of trace and delay classical eyelid conditioning as a function of interstimulus interval. Journal of Experimental Psychology, 91, 165–167.PubMedCrossRef
go back to reference Santhanam, P., Li, Z., Hu, X., Lynch, M. E., & Coles, C. D. (2009). Effects of prenatal alcohol exposure on brain activation during an arithmetic task: an fMRI study. Alcoholism, Clinical and Experimental Research, 33, 1901–1908.PubMedCrossRef Santhanam, P., Li, Z., Hu, X., Lynch, M. E., & Coles, C. D. (2009). Effects of prenatal alcohol exposure on brain activation during an arithmetic task: an fMRI study. Alcoholism, Clinical and Experimental Research, 33, 1901–1908.PubMedCrossRef
go back to reference Schreurs, B. G., Mcintosh, A. R., Bahro, M., Herscovitch, P., Sunderland, T., & Molchan, S. E. (1997). Lateralization and behavioral correlation of changes in regional cerebral blood flow with classical conditioning of the human eyeblink response. Journal of Neurophysiology, 77, 2153–2163.PubMed Schreurs, B. G., Mcintosh, A. R., Bahro, M., Herscovitch, P., Sunderland, T., & Molchan, S. E. (1997). Lateralization and behavioral correlation of changes in regional cerebral blood flow with classical conditioning of the human eyeblink response. Journal of Neurophysiology, 77, 2153–2163.PubMed
go back to reference Shors, T. J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T., & Gould, E. (2001). Neurogenesis in the adult is involved in the formation of trace memories. Nature, 410, 372–376.PubMedCrossRef Shors, T. J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T., & Gould, E. (2001). Neurogenesis in the adult is involved in the formation of trace memories. Nature, 410, 372–376.PubMedCrossRef
go back to reference Simon, O., Mangin, J. F., Cohen, L., Le Bihan, D., & Dehaene, S. (2002). Topographical layout of hand, eye, calculation, and language-related areas in the human parietal lobe. Neuron, 33, 475–487.PubMedCrossRef Simon, O., Mangin, J. F., Cohen, L., Le Bihan, D., & Dehaene, S. (2002). Topographical layout of hand, eye, calculation, and language-related areas in the human parietal lobe. Neuron, 33, 475–487.PubMedCrossRef
go back to reference Sokol, R., Martier, S., & Ernhart, C. (1985). Identification of alcohol abuse in the prenatal clinic. In N. C. Chang, & H. M. Chao (Eds.), Early identification of alcohol abuse. Rockville, MD: Alcohol, Drug Abuse, and Mental Health Administration Research Monograph No. 17. Sokol, R., Martier, S., & Ernhart, C. (1985). Identification of alcohol abuse in the prenatal clinic. In N. C. Chang, & H. M. Chao (Eds.), Early identification of alcohol abuse. Rockville, MD: Alcohol, Drug Abuse, and Mental Health Administration Research Monograph No. 17.
go back to reference Solomon, P. R., Vander Schaaf, E. R., Thompson, R. F., & Weisz, D. J. (1986). Hippocampus and trace conditioning of the rabbit’s classically conditioned nictitating membrane response. Behavioral Neuroscience, 100, 729–744.PubMedCrossRef Solomon, P. R., Vander Schaaf, E. R., Thompson, R. F., & Weisz, D. J. (1986). Hippocampus and trace conditioning of the rabbit’s classically conditioned nictitating membrane response. Behavioral Neuroscience, 100, 729–744.PubMedCrossRef
go back to reference Sowell, E. R., Mattson, S. N., Thompson, P. M., Jernigan, T. L., Riley, E. P., & Toga, A. W. (2001a). Mapping callosal morphology and cognitive correlates: effects of heavy prenatal alcohol exposure. Neurology, 57, 235–244. Sowell, E. R., Mattson, S. N., Thompson, P. M., Jernigan, T. L., Riley, E. P., & Toga, A. W. (2001a). Mapping callosal morphology and cognitive correlates: effects of heavy prenatal alcohol exposure. Neurology, 57, 235–244.
go back to reference Sowell, E. R., Thompson, P. M., Mattson, S. N., Tessner, K. D., Jernigan, T. L., Riley, E. P., et al. (2001b). Voxel-based morphometric analyses of the brain in children and adolescents prenatally exposed to alcohol. Neuroreport, 12, 515–523.CrossRef Sowell, E. R., Thompson, P. M., Mattson, S. N., Tessner, K. D., Jernigan, T. L., Riley, E. P., et al. (2001b). Voxel-based morphometric analyses of the brain in children and adolescents prenatally exposed to alcohol. Neuroreport, 12, 515–523.CrossRef
go back to reference Sowell, E. R., Thompson, P. M., Mattson, S. N., Tessner, K. D., Jernigan, T. L., Riley, E. P., et al. (2002). Regional brain shape abnormalities persist into adolescence after heavy prenatal alcohol exposure. Cerebral Cortex, 12, 856–865.PubMedCrossRef Sowell, E. R., Thompson, P. M., Mattson, S. N., Tessner, K. D., Jernigan, T. L., Riley, E. P., et al. (2002). Regional brain shape abnormalities persist into adolescence after heavy prenatal alcohol exposure. Cerebral Cortex, 12, 856–865.PubMedCrossRef
go back to reference Sowell, E. R., Mattson, S. N., Kan, E., Thompson, P. M., Riley, E. R., & Toga, A. W. (2008a). Abnormal cortical thickness and brain-behavior correlation patterns in individuals with heavy prenatal alcohol exposure. Cerebral Cortex, 18, 126–144. Sowell, E. R., Mattson, S. N., Kan, E., Thompson, P. M., Riley, E. R., & Toga, A. W. (2008a). Abnormal cortical thickness and brain-behavior correlation patterns in individuals with heavy prenatal alcohol exposure. Cerebral Cortex, 18, 126–144.
go back to reference Sowell, E. R., Johnson, A., Kan, E., Lu, L. H., Van Horn, J. D., Toga, A. W., et al. (2008b). Mapping white matter integrity and neurobehavioral correlates in children with fetal alcohol spectrum disorders. The Journal of Neuroscience, 28, 1313–1319.CrossRef Sowell, E. R., Johnson, A., Kan, E., Lu, L. H., Van Horn, J. D., Toga, A. W., et al. (2008b). Mapping white matter integrity and neurobehavioral correlates in children with fetal alcohol spectrum disorders. The Journal of Neuroscience, 28, 1313–1319.CrossRef
go back to reference Spottiswoode, B. S., Meintjes, E. M., Anderson, A. W., Molteno, C. D., Stanton, M. E., Dodge, N. C., et al. (in press). Diffusion tensor imaging of the cerebellum and eyeblink conditioning in fetal alcohol spectrum disorder. Alcoholism: Clinical and Experimental Research. Spottiswoode, B. S., Meintjes, E. M., Anderson, A. W., Molteno, C. D., Stanton, M. E., Dodge, N. C., et al. (in press). Diffusion tensor imaging of the cerebellum and eyeblink conditioning in fetal alcohol spectrum disorder. Alcoholism: Clinical and Experimental Research.
go back to reference Stanton, M. E. (2000). Multiple memory systems, development, and conditioning. Behavioral Brain Research, 110, 25–37.CrossRef Stanton, M. E. (2000). Multiple memory systems, development, and conditioning. Behavioral Brain Research, 110, 25–37.CrossRef
go back to reference Stanton, M. E., & Freeman, J. H. (1994). Eyeblink conditioning in the developing rat: an animal model of learning in developmental neurotoxicology. Environmental Health Perspectives, 102, 131–139.PubMedCrossRef Stanton, M. E., & Freeman, J. H. (1994). Eyeblink conditioning in the developing rat: an animal model of learning in developmental neurotoxicology. Environmental Health Perspectives, 102, 131–139.PubMedCrossRef
go back to reference Stanton, M. E., & Freeman, J. H. (2000). Developmental studies of eyeblink conditioning in the rat. In D. S. Woodruff-Pak & J. H. Steinmetz (Eds.), Eyeblink classical conditioning, vol. 2, animal models (pp. 17–49). Boston: Kluwer Academic Publishers. Stanton, M. E., & Freeman, J. H. (2000). Developmental studies of eyeblink conditioning in the rat. In D. S. Woodruff-Pak & J. H. Steinmetz (Eds.), Eyeblink classical conditioning, vol. 2, animal models (pp. 17–49). Boston: Kluwer Academic Publishers.
go back to reference Stanton, M. E., & Goodlett, C. R. (1998). Neonatal ethanol exposure impairs eyeblink conditioning in weanling rats. Alcoholism, Clinical and Experimental Research, 22, 270–275.PubMedCrossRef Stanton, M. E., & Goodlett, C. R. (1998). Neonatal ethanol exposure impairs eyeblink conditioning in weanling rats. Alcoholism, Clinical and Experimental Research, 22, 270–275.PubMedCrossRef
go back to reference Stanton, M. E., Claflin, D. I., & Herbert, J. S. (2010). Ontogeny of multiple memory systems: Eyeblink conditioning in rodents and humans. In M. S. Blumberg, J. H. Freeman, & S. R. Robinson (Eds.), Oxford handbook of developmental behavioral neuroscience (pp. 501–526). New York: Oxford University Press. Stanton, M. E., Claflin, D. I., & Herbert, J. S. (2010). Ontogeny of multiple memory systems: Eyeblink conditioning in rodents and humans. In M. S. Blumberg, J. H. Freeman, & S. R. Robinson (Eds.), Oxford handbook of developmental behavioral neuroscience (pp. 501–526). New York: Oxford University Press.
go back to reference Steinmetz, J. E. (2000). Brain substrates of classical eyeblink conditioning: a highly localized but also distributed system. Behavioural Brain Research, 110, 13–24.PubMedCrossRef Steinmetz, J. E. (2000). Brain substrates of classical eyeblink conditioning: a highly localized but also distributed system. Behavioural Brain Research, 110, 13–24.PubMedCrossRef
go back to reference Stratton, K., Howe, C., & Battaglia, F. (1996). Fetal alcohol syndrome: Diagnosis, epidemiology, prevention, and treatment. Washington, DC: National Academy Press. Stratton, K., Howe, C., & Battaglia, F. (1996). Fetal alcohol syndrome: Diagnosis, epidemiology, prevention, and treatment. Washington, DC: National Academy Press.
go back to reference Streissguth, A. P., Barr, H. M., & Sampson, P. D. (1990). Moderate prenatal alcohol exposure: effects on child IQ and learning problems at age 7 1/2 years. Alcoholism, Clinical and Experimental Research, 14, 662–669.PubMedCrossRef Streissguth, A. P., Barr, H. M., & Sampson, P. D. (1990). Moderate prenatal alcohol exposure: effects on child IQ and learning problems at age 7 1/2 years. Alcoholism, Clinical and Experimental Research, 14, 662–669.PubMedCrossRef
go back to reference Streissguth, A. P., Aase, J. M., Clarren, S. K., Randels, S. P., LaDue, R. A., & Smith, D. F. (1991). Fetal Alcohol Syndrome in adolescents and adults. JAMA, 265, 1961–1967.PubMedCrossRef Streissguth, A. P., Aase, J. M., Clarren, S. K., Randels, S. P., LaDue, R. A., & Smith, D. F. (1991). Fetal Alcohol Syndrome in adolescents and adults. JAMA, 265, 1961–1967.PubMedCrossRef
go back to reference Streissguth, A. P., Barr, H. M., Carmichael-Olson, H., Sampson, P. D., Bookstein, F. L., & Burgess, D. M. (1994). Drinking during pregnancy decreases Word Attack and Arithmetic scores on standardized tests: adolescent data from a population-based prospective study. Alcoholism, Clinical and Experimental Research, 18, 248–254.PubMedCrossRef Streissguth, A. P., Barr, H. M., Carmichael-Olson, H., Sampson, P. D., Bookstein, F. L., & Burgess, D. M. (1994). Drinking during pregnancy decreases Word Attack and Arithmetic scores on standardized tests: adolescent data from a population-based prospective study. Alcoholism, Clinical and Experimental Research, 18, 248–254.PubMedCrossRef
go back to reference Temple, E., & Posner, M. I. (1998). Brain mechanisms of quantity are similar in 5-year-old children and adults. Proceedings of the National Academy of Sciences of the United States of America, 95, 7836–7841.PubMedCrossRef Temple, E., & Posner, M. I. (1998). Brain mechanisms of quantity are similar in 5-year-old children and adults. Proceedings of the National Academy of Sciences of the United States of America, 95, 7836–7841.PubMedCrossRef
go back to reference Thomas, J. D., Goodlett, C. R., & West, J. R. (1998). Alcohol-induced Purkinje cell loss depends on developmental timing of alcohol exposure and correlates with motor performance. Developmental Brain Research, 105, 159–166.PubMedCrossRef Thomas, J. D., Goodlett, C. R., & West, J. R. (1998). Alcohol-induced Purkinje cell loss depends on developmental timing of alcohol exposure and correlates with motor performance. Developmental Brain Research, 105, 159–166.PubMedCrossRef
go back to reference Thompson, R. F. (2005). In search of memory traces. Annual Reviews in Psychology, 56, 1–23.CrossRef Thompson, R. F. (2005). In search of memory traces. Annual Reviews in Psychology, 56, 1–23.CrossRef
go back to reference Van der Zee, E., Kronforst-Collins, M. A., Maizels, E. T., Hunziger-Dunn, M., & Disterhoft, J. F. (1997). Gammaisoform-selective changes in PKC immunoreactivity after trace eyeblink conditioning in the rabbit hippocampus. Hippocampus, 7, 271–285.PubMedCrossRef Van der Zee, E., Kronforst-Collins, M. A., Maizels, E. T., Hunziger-Dunn, M., & Disterhoft, J. F. (1997). Gammaisoform-selective changes in PKC immunoreactivity after trace eyeblink conditioning in the rabbit hippocampus. Hippocampus, 7, 271–285.PubMedCrossRef
go back to reference Vaurio, L., Riley, E. P., & Mattson, S. M. (2008). Differences in executive functioning in children with heavy prenatal alcohol exposure or attention-deficit ⁄ hyperactivity disorder. Journal of the International Neuropsychological Society, 14, 119–129.PubMedCrossRef Vaurio, L., Riley, E. P., & Mattson, S. M. (2008). Differences in executive functioning in children with heavy prenatal alcohol exposure or attention-deficit ⁄ hyperactivity disorder. Journal of the International Neuropsychological Society, 14, 119–129.PubMedCrossRef
go back to reference Venkatraman, V., Ansari, D., & Chee, M. W. L. (2005). Neural correlates of symbolic and non-symbolic arithmetic. Neuropsychologia, 43, 744–753.PubMedCrossRef Venkatraman, V., Ansari, D., & Chee, M. W. L. (2005). Neural correlates of symbolic and non-symbolic arithmetic. Neuropsychologia, 43, 744–753.PubMedCrossRef
go back to reference Wager, T. D., & Smith, E. E. (2003). Neuroimaging studies of working memory: a meta-analysis. Cognitive, Affective & Behavioral Neuroscience, 3, 255–274.CrossRef Wager, T. D., & Smith, E. E. (2003). Neuroimaging studies of working memory: a meta-analysis. Cognitive, Affective & Behavioral Neuroscience, 3, 255–274.CrossRef
go back to reference Watari, H., Born, D. E., & Gleason, C. A. (2006). Effects of first trimester binge alcohol exposure on developing white matter in fetal sheep. Pediatric Research, 59, 560–564.PubMedCrossRef Watari, H., Born, D. E., & Gleason, C. A. (2006). Effects of first trimester binge alcohol exposure on developing white matter in fetal sheep. Pediatric Research, 59, 560–564.PubMedCrossRef
go back to reference Weiss, C., Kronforst-Collins, M. A., & Disterhoft, J. F. (1996). Activity of hippocampal pyramidal neurons during trace eyeblink conditioning. Hippocampus, 6, 192–209.PubMedCrossRef Weiss, C., Kronforst-Collins, M. A., & Disterhoft, J. F. (1996). Activity of hippocampal pyramidal neurons during trace eyeblink conditioning. Hippocampus, 6, 192–209.PubMedCrossRef
go back to reference Weiss, C., Bouwmeester, H., Power, J. M., & Disterhoft, J. F. (1999). Hippocampal lesions prevent trace eyeblink conditioning in the freely moving rat. Behavioral Brain Research, 99, 123–132.CrossRef Weiss, C., Bouwmeester, H., Power, J. M., & Disterhoft, J. F. (1999). Hippocampal lesions prevent trace eyeblink conditioning in the freely moving rat. Behavioral Brain Research, 99, 123–132.CrossRef
go back to reference Werden, D., & Ross, L. E. (1972). A comparison of the trace and delay classical conditioning performance of normal children. Journal of Experimental Child Psychology, 14, 126–132.PubMedCrossRef Werden, D., & Ross, L. E. (1972). A comparison of the trace and delay classical conditioning performance of normal children. Journal of Experimental Child Psychology, 14, 126–132.PubMedCrossRef
go back to reference 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, 28, 497–507.PubMedCrossRef 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, 28, 497–507.PubMedCrossRef
go back to reference Woodruff-Pak, D. S., & Disterhoft, J. F. (2008). Where is the trace in trace conditioning? Trends in Neuroscience, 31, 105–112.CrossRef Woodruff-Pak, D. S., & Disterhoft, J. F. (2008). Where is the trace in trace conditioning? Trends in Neuroscience, 31, 105–112.CrossRef
go back to reference Woodruff-Pak, D. S., & Steinmetz, J. E. (2000a). Eyeblink classical conditioning: Volume I—Applications in humans. Boston: Kluwer Academic Publishers. Woodruff-Pak, D. S., & Steinmetz, J. E. (2000a). Eyeblink classical conditioning: Volume I—Applications in humans. Boston: Kluwer Academic Publishers.
go back to reference Woodruff-Pak, D. S., & Steinmetz, J. E. (2000b). Eyeblink classical conditioning: Volume II—Applications in animals. Boston: Kluwer Academic Publishers. Woodruff-Pak, D. S., & Steinmetz, J. E. (2000b). Eyeblink classical conditioning: Volume II—Applications in animals. Boston: Kluwer Academic Publishers.
go back to reference Wozniak, J. R., & Muetzel, R. L. (2011). What does diffusion tensor imaging reveal about the brain and cognition in fetal alcohol spectrum disorders? Neuropsychology Review, 21. Wozniak, J. R., & Muetzel, R. L. (2011). What does diffusion tensor imaging reveal about the brain and cognition in fetal alcohol spectrum disorders? Neuropsychology Review, 21.
go back to reference Wozniak, J. R., Mueller, B. A., Chang, P., Muetzel, R. L., Caros, L., & Lim, K. O. (2006). Diffusion tensor imaging in children with fetal alcohol spectrum disorders. Alcoholism, Clinical and Experimental Research, 30, 1799–1806.PubMedCrossRef Wozniak, J. R., Mueller, B. A., Chang, P., Muetzel, R. L., Caros, L., & Lim, K. O. (2006). Diffusion tensor imaging in children with fetal alcohol spectrum disorders. Alcoholism, Clinical and Experimental Research, 30, 1799–1806.PubMedCrossRef
go back to reference Wozniak, J. R., Muetzel, R. L., Mueller, B. A., McGee, C. L., Freerks, M. A., Ward, E. E., et al. (2009). Microstructural corpus callosum anomalies in children with prenatal alcohol exposure: an extension of previous diffusion tensor imaging findings. Alcoholism, Clinical and Experimental Research, 30, 1825–1835.CrossRef Wozniak, J. R., Muetzel, R. L., Mueller, B. A., McGee, C. L., Freerks, M. A., Ward, E. E., et al. (2009). Microstructural corpus callosum anomalies in children with prenatal alcohol exposure: an extension of previous diffusion tensor imaging findings. Alcoholism, Clinical and Experimental Research, 30, 1825–1835.CrossRef
go back to reference Wynn, K. (1995). Origins of numerical knowledge. Mathematical Cognition, 1, 35–60. Wynn, K. (1995). Origins of numerical knowledge. Mathematical Cognition, 1, 35–60.
go back to reference Wynn, K. (1996). Infants’ individuation and enumeration of sequential actions. Psychological Science, 7, 164–169.CrossRef Wynn, K. (1996). Infants’ individuation and enumeration of sequential actions. Psychological Science, 7, 164–169.CrossRef
go back to reference Wynn, K., & Chiang, W. C. (1998). Limits to infants’ knowledge of objects: the case of magical appearance. Psychological Science, 9, 448–455.CrossRef Wynn, K., & Chiang, W. C. (1998). Limits to infants’ knowledge of objects: the case of magical appearance. Psychological Science, 9, 448–455.CrossRef
go back to reference Wynn, K., Bloom, P., & Chiang, W. C. (2002). Enumeration of collective entities by 5-month-old infant. Cognition, 83, B55–B62.PubMedCrossRef Wynn, K., Bloom, P., & Chiang, W. C. (2002). Enumeration of collective entities by 5-month-old infant. Cognition, 83, B55–B62.PubMedCrossRef
go back to reference Zago, L., Pesenti, M., Mellet, E., Crivello, F., Mazoyer, B., & Tzourio-Mazoyer, N. (2001). Neural correlates of simple and complex mental calculation. Neuroimage, 13, 314–327.PubMedCrossRef Zago, L., Pesenti, M., Mellet, E., Crivello, F., Mazoyer, B., & Tzourio-Mazoyer, N. (2001). Neural correlates of simple and complex mental calculation. Neuroimage, 13, 314–327.PubMedCrossRef
go back to reference Zago, L., Petit, L., Turbelin, M., Andersson, F., Vigneau, M., & Tzourio-Mazoyer, N. (2008). How verbal and spatial manipulation networks contribute to calculation: an fMRI study. Neuropsychologia, 46, 2403–2414.PubMedCrossRef Zago, L., Petit, L., Turbelin, M., Andersson, F., Vigneau, M., & Tzourio-Mazoyer, N. (2008). How verbal and spatial manipulation networks contribute to calculation: an fMRI study. Neuropsychologia, 46, 2403–2414.PubMedCrossRef
go back to reference Zoeller, R. T., Butnariu, O. V., Fletcher, D. L., & Riley, E. P. (1994). Limited postnatal ethanol exposure permanently alters the expression of mRNAS encoding myelin basic protein and myelin-associated glycoprotein in cerebellum. Alcoholism, Clinical and Experimental Research, 18, 909–916.PubMedCrossRef Zoeller, R. T., Butnariu, O. V., Fletcher, D. L., & Riley, E. P. (1994). Limited postnatal ethanol exposure permanently alters the expression of mRNAS encoding myelin basic protein and myelin-associated glycoprotein in cerebellum. Alcoholism, Clinical and Experimental Research, 18, 909–916.PubMedCrossRef
Metadata
Title
Biobehavioral Markers of Adverse Effect in Fetal Alcohol Spectrum Disorders
Authors
Sandra W. Jacobson
Joseph L. Jacobson
Mark E. Stanton
Ernesta M. Meintjes
Christopher D. Molteno
Publication date
01-06-2011
Publisher
Springer US
Published in
Neuropsychology Review / Issue 2/2011
Print ISSN: 1040-7308
Electronic ISSN: 1573-6660
DOI
https://doi.org/10.1007/s11065-011-9169-7

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