Advertisement

Neuropsychology Review

, 21:148 | Cite as

Biobehavioral Markers of Adverse Effect in Fetal Alcohol Spectrum Disorders

  • Sandra W. Jacobson
  • Joseph L. Jacobson
  • Mark E. Stanton
  • Ernesta M. Meintjes
  • Christopher D. Molteno
Review

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.

Keywords

Fetal alcohol syndrome Eyeblink conditioning Arithmetic Fetal alcohol spectrum disorders Biomarkers Behavioral phenotype Prenatal alcohol exposure 

Notes

Acknowledgments

The Detroit longitudinal study was funded by grants R01 AA06966, R01 AA09524, and P50 AA0706 from the NIH/National Institute on Alcohol Abuse and Alcoholism (NIAAA). Recruitment of the Cape Town longitudinal cohort was funded by two administrative supplements to R01-AA09524, the NIH Office of Research on Minority Health, and the Foundation for Alcohol Related Research, Cape Town, South Africa. The 5-year follow-up assessment of the Cape Town longitudinal cohort was funded by U01 AA014790 in conjunction with the NIAAA Collaborative Initiative on Fetal Alcohol Spectrum Disorders (CIFASD); the 9-year follow-up by R01 AA016781. Recruitment and assessment of the Cape Town cross-sectional cohort were funded by an NIH Fogarty International Research Collaboration Award from the NIH (R03 TW007030), a Children’s Bridge grant from the Office of the President of Wayne State University, a Focus Area grant (FA2005040800024) from the National Research Foundation of South Africa, the South African Research Chairs Initiative of the Department of Science and Technology and National Research Foundation of South Africa, and a seed money grant from the University of Cape Town. The Cape Town dysmorphology assessments were funded, in part, by U24 AA014815 from CIFASD. All these projects received supplemental funding from the Joseph Young, Sr., Fund from the State of Michigan. We thank Robert J. Sokol for his collaboration in the Detroit longitudinal study; Denis Viljoen for his collaboration in the recruitment of the Cape Town longitudinal cohort; John C. Gore and J. Christopher Gatenby for their collaboration in the implementation of the Cape Town neuroimaging studies; Rafael Klorman and Joel Nigg for their collaboration in the ADHD diagnosis; H. Eugene Hoyme, Luther K. Robinson, and Nathaniel Khaole, for performing the FAS dysmorphology assessments; and Neil C. Dodge for assistance with the preparation of this manuscript.

References

  1. 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.PubMedCrossRefGoogle Scholar
  2. 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.PubMedCrossRefGoogle Scholar
  3. 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.PubMedGoogle Scholar
  4. 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.PubMedCrossRefGoogle Scholar
  5. 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.PubMedCrossRefGoogle Scholar
  6. 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.PubMedGoogle Scholar
  7. 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.PubMedCrossRefGoogle Scholar
  8. 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.PubMedGoogle Scholar
  9. 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.PubMedCrossRefGoogle Scholar
  10. Bonthius, D. J., & West, J. R. (1991). Permanent neuronal deficits in rats exposed to alcohol during the brain growth spurt. Teratology, 44, 147–163.PubMedCrossRefGoogle Scholar
  11. 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.PubMedCrossRefGoogle Scholar
  12. 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.CrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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.PubMedCrossRefGoogle Scholar
  15. Butterworth, B. (1999). The mathematical brain. London: Macmillan.Google Scholar
  16. Butterworth, B. (2005). The development of arithmetical abilities. Journal of Child Psychology and Psychiatry, 46, 3–18.PubMedCrossRefGoogle Scholar
  17. 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.PubMedCrossRefGoogle Scholar
  18. 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.Google Scholar
  19. Castellanos, F. X., & Tannock, R. (2002). Neuroscience of attention-deficit/hyperactivity disorder: the search for endophenotypes. Nature Reviews. Neuroscience, 3, 617–628.PubMedGoogle Scholar
  20. 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.PubMedCrossRefGoogle Scholar
  21. 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.Google Scholar
  22. 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.PubMedCrossRefGoogle Scholar
  23. 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.PubMedCrossRefGoogle Scholar
  24. 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.PubMedCrossRefGoogle Scholar
  25. Christian, K. M., & Thompson, R. F. (2003). Neural substrates of eyeblink conditioning: acquisition and retention. Learning & Memory, 10, 427–455.CrossRefGoogle Scholar
  26. 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.PubMedCrossRefGoogle Scholar
  27. Clark, R. E., & Squire, L. R. (1998). Classical conditioning and brain systems: the role of awareness. Science, 280, 77–81.PubMedCrossRefGoogle Scholar
  28. 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.PubMedCrossRefGoogle Scholar
  29. Clarren, S. K. (1977). Central nervous system malformations in two offspring of alcoholic women. Birth Defects Original Article Series, 13, 151–153.PubMedGoogle Scholar
  30. Clarren, S. K. (1986). Neuropathology and fetal alcohol syndrome. In J. R. West (Ed.), Alcohol and brain development. New York: Oxford University Press.Google Scholar
  31. Clarren, S. K., & Smith, D. W. (1978). The fetal alcohol syndrome. The New England Journal of Medicine, 298, 1063–1067.PubMedCrossRefGoogle Scholar
  32. Coffin, J. M., & Boegle, A. (2000). Failure of dyslexics to achieve eyeblink conditioning following five days of training. Society for Neuroscience Abstracts, 26.Google Scholar
  33. 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.PubMedCrossRefGoogle Scholar
  34. 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.PubMedCrossRefGoogle Scholar
  35. 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.CrossRefGoogle Scholar
  36. 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.PubMedCrossRefGoogle Scholar
  37. 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.PubMedCrossRefGoogle Scholar
  38. Croxford, J., & Viljoen, D. (1999). Alcohol consumption by pregnant women in the Western Cape. South African Medical Journal, 89, 962–965.PubMedGoogle Scholar
  39. Dehaene, S., & Cohen, L. (1995). Towards an anatomical and functional model of number processing. Mathematical Cognition, 1, 83–120.Google Scholar
  40. Dehaene, S., Piazza, M., Pinel, P., & Cohen, L. (2003). Three parietal circuits for number processing. Cognitive Neuropsychology, 20, 487–506.PubMedCrossRefGoogle Scholar
  41. Dehaene, S., Molko, N., Cohen, L., & Wilson, A. J. (2004). Arithmetic and the brain. Current Opinion in Neurobiology, 14, 218–224.PubMedCrossRefGoogle Scholar
  42. 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.PubMedCrossRefGoogle Scholar
  43. 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.Google Scholar
  44. 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.PubMedCrossRefGoogle Scholar
  45. 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.PubMedCrossRefGoogle Scholar
  46. 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.PubMedCrossRefGoogle Scholar
  47. 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.CrossRefGoogle Scholar
  48. 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.PubMedCrossRefGoogle Scholar
  49. 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.PubMedCrossRefGoogle Scholar
  50. 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.PubMedGoogle Scholar
  51. 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.PubMedCrossRefGoogle Scholar
  52. 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.PubMedCrossRefGoogle Scholar
  53. Gottesman, I. I., & Gould, T. D. (2003). The endophenotype concept in psychiatry: etymology and strategic intentions. The American Journal of Psychiatry, 160, 636–645.PubMedCrossRefGoogle Scholar
  54. 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.PubMedCrossRefGoogle Scholar
  55. 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.PubMedCrossRefGoogle Scholar
  56. 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.CrossRefGoogle Scholar
  57. 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.CrossRefGoogle Scholar
  58. Gruber, O., Indefrey, P., Steinmetz, H., & Kleinschmidt, A. (2001). Dissociating neural correlates of cognitive components in mental calculation. Cerebral Cortex, 11, 350–359.PubMedCrossRefGoogle Scholar
  59. Guerri, C., Pascual, M., & Renau-Piqueras, J. (2001). Glia and fetal alcohol syndrome. Neurotoxicology, 22, 593–599.PubMedCrossRefGoogle Scholar
  60. 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.PubMedCrossRefGoogle Scholar
  61. 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.PubMedCrossRefGoogle Scholar
  62. 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.PubMedGoogle Scholar
  63. 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.Google Scholar
  64. 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.PubMedCrossRefGoogle Scholar
  65. 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.PubMedCrossRefGoogle Scholar
  66. Ivkovich, D., Paczkowski, C. M., & Stanton, M. E. (2000). Ontogeny of delay versus trace eyeblink conditioning in the rat. Developmental Psychobiology, 36, 148–160.PubMedCrossRefGoogle Scholar
  67. 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.Google Scholar
  68. 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.PubMedCrossRefGoogle Scholar
  69. 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.PubMedCrossRefGoogle Scholar
  70. 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.CrossRefGoogle Scholar
  71. 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.Google Scholar
  72. 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.PubMedCrossRefGoogle Scholar
  73. 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.CrossRefGoogle Scholar
  74. 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.CrossRefGoogle Scholar
  75. 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.PubMedCrossRefGoogle Scholar
  76. 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.CrossRefGoogle Scholar
  77. 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.CrossRefGoogle Scholar
  78. 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.Google Scholar
  79. Jones, K. L., & Smith, D. W. (1973). Recognition of the fetal alcohol syndrome in early infancy. Lancet, 2, 999–1001.CrossRefGoogle Scholar
  80. 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.PubMedCrossRefGoogle Scholar
  81. 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.PubMedGoogle Scholar
  82. 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.CrossRefGoogle Scholar
  83. 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.CrossRefGoogle Scholar
  84. 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.PubMedCrossRefGoogle Scholar
  85. Kim, J. J., & Thompson, R. F. (1997). Cerebellar circuits and synaptic mechanisms involved in classical eyeblink conditioning. Trends in Neuroscience, 20, 177–181.CrossRefGoogle Scholar
  86. 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.PubMedCrossRefGoogle Scholar
  87. 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.PubMedCrossRefGoogle Scholar
  88. 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.PubMedCrossRefGoogle Scholar
  89. 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.PubMedCrossRefGoogle Scholar
  90. 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.Google Scholar
  91. 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.PubMedCrossRefGoogle Scholar
  92. 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.PubMedCrossRefGoogle Scholar
  93. 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.PubMedCrossRefGoogle Scholar
  94. Kopera-Frye, K., Dehaene, S., & Streissguth, A. P. (1996). Impairments of number processing induced by prenatal alcohol exposure. Neuropsychologia, 34, 1187–1196.PubMedCrossRefGoogle Scholar
  95. Krupa, D. J., Thompson, J. K., & Thompson, R. F. (1993). Localization of a memory trace in the mammalian brain. Science, 260, 989–991.PubMedCrossRefGoogle Scholar
  96. 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.CrossRefGoogle Scholar
  97. Lavond, D. G., & Steinmetz, J. E. (1989). Acquisition of classical conditioning without cerebellar cortex. Behavioral Brain Research, 33, 113–164.CrossRefGoogle Scholar
  98. Lavond, D. G., Kim, J. J., & Thompson, R. F. (1993). Mammalian brain substrates of aversive classical conditioning. Annual Reviews in Psychology, 44, 317–342.CrossRefGoogle Scholar
  99. 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.Google Scholar
  100. 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.PubMedCrossRefGoogle Scholar
  101. 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.Google Scholar
  102. 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.Google Scholar
  103. 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.PubMedCrossRefGoogle Scholar
  104. 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.PubMedCrossRefGoogle Scholar
  105. 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.PubMedCrossRefGoogle Scholar
  106. 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.PubMedCrossRefGoogle Scholar
  107. 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.PubMedGoogle Scholar
  108. 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.PubMedCrossRefGoogle Scholar
  109. 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.CrossRefGoogle Scholar
  110. 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.PubMedCrossRefGoogle Scholar
  111. 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.PubMedCrossRefGoogle Scholar
  112. 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.PubMedCrossRefGoogle Scholar
  113. 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.
  114. 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.PubMedCrossRefGoogle Scholar
  115. 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.PubMedGoogle Scholar
  116. 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.PubMedGoogle Scholar
  117. 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.PubMedCrossRefGoogle Scholar
  118. 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.PubMedCrossRefGoogle Scholar
  119. 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.PubMedCrossRefGoogle Scholar
  120. 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.PubMedGoogle Scholar
  121. 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.PubMedCrossRefGoogle Scholar
  122. 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.PubMedCrossRefGoogle Scholar
  123. 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.PubMedCrossRefGoogle Scholar
  124. 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.PubMedCrossRefGoogle Scholar
  125. 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.PubMedGoogle Scholar
  126. 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.PubMedCrossRefGoogle Scholar
  127. Mix, K., Huttenlocher, J., & Levine, S. (2002). Math without words: Quantitative development in infancy and early childhood. New York: Oxford University Press.CrossRefGoogle Scholar
  128. 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.PubMedCrossRefGoogle Scholar
  129. 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.Google Scholar
  130. 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.CrossRefGoogle Scholar
  131. Moyer, J. R., Deyo, R. A., & Disterhoft, J. F. (1990). Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behavioral Neuroscience, 104, 243–252.PubMedCrossRefGoogle Scholar
  132. 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.PubMedGoogle Scholar
  133. 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.PubMedCrossRefGoogle Scholar
  134. 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.PubMedCrossRefGoogle Scholar
  135. 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.Google Scholar
  136. Ohyama, T., Nores, W. L., Murphy, M., & Mauk, M. D. (2003). What the cerebellum computes. Trends in Neuroscience, 26, 222–227.CrossRefGoogle Scholar
  137. 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.PubMedGoogle Scholar
  138. 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.PubMedCrossRefGoogle Scholar
  139. 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.Google Scholar
  140. 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.PubMedCrossRefGoogle Scholar
  141. 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.PubMedGoogle Scholar
  142. Rasmussen, C., & Bisanz, J. (2009). Exploring mathematics difficulties in children with fetal alcohol spectrum disorders. Child Development Perspectives, 3, 125–130.CrossRefGoogle Scholar
  143. 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.PubMedCrossRefGoogle Scholar
  144. 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.PubMedCrossRefGoogle Scholar
  145. 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.PubMedCrossRefGoogle Scholar
  146. 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.PubMedGoogle Scholar
  147. 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.PubMedCrossRefGoogle Scholar
  148. 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.PubMedCrossRefGoogle Scholar
  149. 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.Google Scholar
  150. 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.PubMedCrossRefGoogle Scholar
  151. 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.Google Scholar
  152. 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.CrossRefGoogle Scholar
  153. 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.PubMedCrossRefGoogle Scholar
  154. 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.Google Scholar
  155. 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.CrossRefGoogle Scholar
  156. 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. Google Scholar
  157. Stanton, M. E. (2000). Multiple memory systems, development, and conditioning. Behavioral Brain Research, 110, 25–37.CrossRefGoogle Scholar
  158. 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.PubMedCrossRefGoogle Scholar
  159. 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.Google Scholar
  160. Stanton, M. E., & Goodlett, C. R. (1998). Neonatal ethanol exposure impairs eyeblink conditioning in weanling rats. Alcoholism, Clinical and Experimental Research, 22, 270–275.PubMedCrossRefGoogle Scholar
  161. 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.Google Scholar
  162. Steinmetz, J. E. (2000). Brain substrates of classical eyeblink conditioning: a highly localized but also distributed system. Behavioural Brain Research, 110, 13–24.PubMedCrossRefGoogle Scholar
  163. Sternberg, S. (1966). High speed scanning in human memory. Science, 153, 652–654.PubMedCrossRefGoogle Scholar
  164. Stratton, K., Howe, C., & Battaglia, F. (1996). Fetal alcohol syndrome: Diagnosis, epidemiology, prevention, and treatment. Washington, DC: National Academy Press.Google Scholar
  165. 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.PubMedCrossRefGoogle Scholar
  166. 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.PubMedCrossRefGoogle Scholar
  167. 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.PubMedCrossRefGoogle Scholar
  168. 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.PubMedCrossRefGoogle Scholar
  169. 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.PubMedCrossRefGoogle Scholar
  170. Thompson, R. F. (1986). The neurobiology of learning and memory. Science, 233, 941–947.PubMedCrossRefGoogle Scholar
  171. Thompson, R. F. (2005). In search of memory traces. Annual Reviews in Psychology, 56, 1–23.CrossRefGoogle Scholar
  172. 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.PubMedCrossRefGoogle Scholar
  173. 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.PubMedCrossRefGoogle Scholar
  174. Venkatraman, V., Ansari, D., & Chee, M. W. L. (2005). Neural correlates of symbolic and non-symbolic arithmetic. Neuropsychologia, 43, 744–753.PubMedCrossRefGoogle Scholar
  175. Wager, T. D., & Smith, E. E. (2003). Neuroimaging studies of working memory: a meta-analysis. Cognitive, Affective & Behavioral Neuroscience, 3, 255–274.CrossRefGoogle Scholar
  176. 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.PubMedCrossRefGoogle Scholar
  177. Weiss, C., Kronforst-Collins, M. A., & Disterhoft, J. F. (1996). Activity of hippocampal pyramidal neurons during trace eyeblink conditioning. Hippocampus, 6, 192–209.PubMedCrossRefGoogle Scholar
  178. 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.CrossRefGoogle Scholar
  179. 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.PubMedCrossRefGoogle Scholar
  180. 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.PubMedCrossRefGoogle Scholar
  181. Woodruff-Pak, D. S., & Disterhoft, J. F. (2008). Where is the trace in trace conditioning? Trends in Neuroscience, 31, 105–112.CrossRefGoogle Scholar
  182. Woodruff-Pak, D. S., & Steinmetz, J. E. (2000a). Eyeblink classical conditioning: Volume I—Applications in humans. Boston: Kluwer Academic Publishers.Google Scholar
  183. Woodruff-Pak, D. S., & Steinmetz, J. E. (2000b). Eyeblink classical conditioning: Volume II—Applications in animals. Boston: Kluwer Academic Publishers.Google Scholar
  184. 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.Google Scholar
  185. 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.PubMedCrossRefGoogle Scholar
  186. 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.CrossRefGoogle Scholar
  187. Wynn, K. (1992). Addition and subtraction by human infants. Nature, 358, 749–750.PubMedCrossRefGoogle Scholar
  188. Wynn, K. (1995). Origins of numerical knowledge. Mathematical Cognition, 1, 35–60.Google Scholar
  189. Wynn, K. (1996). Infants’ individuation and enumeration of sequential actions. Psychological Science, 7, 164–169.CrossRefGoogle Scholar
  190. Wynn, K., & Chiang, W. C. (1998). Limits to infants’ knowledge of objects: the case of magical appearance. Psychological Science, 9, 448–455.CrossRefGoogle Scholar
  191. Wynn, K., Bloom, P., & Chiang, W. C. (2002). Enumeration of collective entities by 5-month-old infant. Cognition, 83, B55–B62.PubMedCrossRefGoogle Scholar
  192. 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.PubMedCrossRefGoogle Scholar
  193. 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.PubMedCrossRefGoogle Scholar
  194. 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.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Sandra W. Jacobson
    • 1
    • 2
    • 3
  • Joseph L. Jacobson
    • 1
    • 2
    • 3
  • Mark E. Stanton
    • 4
  • Ernesta M. Meintjes
    • 2
    • 5
  • Christopher D. Molteno
    • 3
  1. 1.Department of Psychiatry and Behavioral NeurosciencesWayne State University School of MedicineDetroitUSA
  2. 2.Department of Human Biology, Faculty of Health SciencesUniversity of Cape TownCape TownSouth Africa
  3. 3.Department of Psychiatry and Mental Health, Faculty of Health SciencesUniversity of Cape TownCape TownSouth Africa
  4. 4.Department of PsychologyUniversity of DelawareNewarkUSA
  5. 5.MRC/UCT Medical Imaging Research UnitUniversity of Cape TownCape TownSouth Africa

Personalised recommendations