An fMRI study of number processing in children with fetal alcohol syndrome

Alcoholism: Clinical and Experimental Research

Volumn 34, Issue 8, 2010, Pages 1450-1464

  Meintjes, Ernesta M ^a   Jacobson, Joseph L ^b,c   Molteno, Christopher D ^b   Gatenby, J Christopher ^d   Warton, Christopher ^b   Cannistraci, Christopher J ^d   Hoyme, H Eugene ^e   Robinson, Luther K ^f   Khaole, Nathaniel ^b   Gore, John C ^d   Jacobson, Sandra W ^b,c  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d VANDERBILT UNIVERSITY   (United States)

^e UNIVERSITY OF SOUTH DAKOTA   (United States)

^f UNIVERSITY AT BUFFALO   (United States)

Author keywords

Arithmetic; Fetal Alcohol Spectrum Disorder; Fetal Alcohol Syndrome; FMRI; Number Processing

Indexed keywords

ARTICLE; BRAIN REGION; CEREBELLUM VERMIS; CHILD; CLINICAL ARTICLE; CONTROL GROUP; CONTROLLED STUDY; FEMALE; FETAL ALCOHOL SYNDROME; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; NEUROIMAGING; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE SCANNER; PARIETAL LOBE; PRENATAL EXPOSURE; PRIORITY JOURNAL; RIGHT HANDEDNESS; SCHOOL CHILD; SKULL; SOUTH AFRICA; SUBICULUM; TASK PERFORMANCE;

BRAIN; BRAIN MAPPING; CHILD; COHORT STUDIES; FEMALE; FETAL ALCOHOL SYNDROME; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MATHEMATICAL CONCEPTS; MENTAL PROCESSES; PREGNANCY; PSYCHOMOTOR PERFORMANCE; SOUTH AFRICA;

EID: 77954922220     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/j.1530-0277.2010.01230.x     Document Type: Article

References (78)

1. Annett M (1970) A classification of hand preference by association analysis. Br J Psychol 61 : 303 321.
2. Archibald SL, Fennema-Notestine C, Gamst A, Riley EP, Mattson SN, Jernigan TJ (2001) Brain dysmorphology in individuals with severe prenatal alcohol exposure. Dev Med Child Neurol 43 : 148 154.
3. Astley SJ, Clarren SK (2001) Measuring the facial phenotype of individuals with prenatal alcohol exposure: correlations with brain dysfunction. Alcohol Alcohol 36 : 147 159.
4. Burden MJ, Jacobson SW, Jacobson JL (2005) The relation of prenatal alcohol exposure to cognitive processing speed and efficiency in childhood. Alcohol Clin Exp Res 29 : 1473 1483.
5. Butterworth B (1999) The Mathematical Brain. Macmillan
6. Cantlon JF, Brannon EM, Carter EJ, Pelphrey KA (2006) Functional imaging of numerical processing in adults and 4-y-old children. PLoS Biol 4 : e125.
7. Carmichael Olson H, Feldman JJ, Streissguth AP, Sampson PD, Bookstein FL (1998) Neuropsychological deficits in adolescents with fetal alcohol syndrome: clinical findings. Alcohol Clin Exp Res 22 : 1998 2012.
8. Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioral correlates. Brain 129 : 564 583.
9. Chiodo LM, Jacobson SW, Jacobson JL (2004) Neurodevelopmental effects of postnatal lead exposure at very low levels. Neurotoxicol Teratol 26 : 359 371.
10. Chochon F, Cohen L, van de Moortele PF, Dehaene S (1999) Differential contributions of the left and right inferior parietal lobules to number processing. J Cogn Neurosci 11 : 617 630.
11. Clarren SK (1977) Central nervous system malformations in two offspring of alcoholic women. Birth Defects Orig Artic Ser 13 : 151 153.
12. Clarren SK, Smith DW (1978) The fetal alcohol syndrome. N Engl J Med 298 : 1063 1067.
13. Corbetta M, Kincade JM, Ollinger JM, McAoy MP, Shulman GL (2000) Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nat Neurosci 3 : 202 207.
14. Croxford J, Viljoen D (1999) Alcohol consumption by pregnant women in the Western Cape. S Afr Med J 89 : 962 965.
15. Davis N, Cannistraci CJ, Rogers BP, Gatenby JC, Fuchs LS, Anderson AW, Gore JC (2009) Aberrant functional activation in school age children at-risk for mathematical disability: a functional imaging study of simple arithmetic skill. Neuropsychologia 47 : 2470 2479.
16. Dehaene S, Cohen L (1995) Towards an anatomical and functional model of number processing. Math Cogn 1 : 83 120.
17. Dehaene S, Molko N, Cohen L, Wilson AJ (2004) Arithmetic and the brain. Curr Opin Neurobiol 14 : 218 224.
18. Dehaene S, Piazza M, Pinel P, Cohen L (2003) Three parietal circuits for number processing. Cogn Neuropsychol 20 : 487 506.
19. Delazer M, Ischebeck A, Domahs F, Zamarian L, Koppelstaetter F, Siedentopf CM, Kaufmann L, Benke T, Felber S 2005) Learning strategies and learning by drill - evidence from an fMRI study. NeuroImage 25 : 839 849.
20. Dodge NC, Jacobson JL, Molteno CD, Meintjes EM, Bangalore S, Diwadkar V, Hoyme EH, Robinson LK, Khaole N, Avison MJ, Jacobson SW (2009) Prenatal alcohol exposure and interhemispheric transfer of tactile information: Detroit and Cape Town findings. Alcohol Clin Exp Res 33 : 1628 1637.
21. Dodge NC, Jacobson SW, Molteno CD, Pienaar M, Aitken L, Burden MJ et al. (2007) Precursors of arithmetic deficits in fetal alcohol exposed children in Cape Town, South Africa. Alcohol Clin Exp Res 31 : P700.
22. Eger E, Sterzer P, Russ MO, Giraud AL, Kleinschmidt A (2003) A supramodal number representation in human intraparietal cortex. Neuron 37 : 719 725.
23. Fletcher PC, Shallice T, Frith CD, Frackowiak RSJ, Dolan RJ (1996) Brain activity during memory retrieval - the influence of imagery and semantic cueing. Brain 119 : 1587 1596.
24. Fryer SL, Tapert SF, Mattson SN, Paulus MP, Spadoni AD, Riley EP (2007) Prenatal alcohol exposure affects frontal-striatal BOLD response during inhibitory control. Alcohol Clin Exp Res 31 : 1415 1424.
25. Goldschmidt L, Richardson GA, Stoffer DS, Geva D, Day NL (1996) Prenatal alcohol exposure and academic achievement at age six: a nonlinear fit. Alcohol Clin Exp Res 20 : 763 770.
26. Greenland S, Rothman KJ (1998). Introduction to stratified analysis in Modern Epidemiology (Rothman KJ, Greenland S eds pp. 253 279. Lippincott, Williams, & Wilkins
27. Gruber O, Indefrey P, Steinmetz H, Kleinshmidt A (2001) Dissociating neural correlates of cognitive components in mental calculation. Cereb Cortex 11 : 350 359.
28. Halperin JM, Schulz KP (2006) Revisiting the role of the prefrontal cortex in the pathophysiology of attention-deficit/hyperactivity disorder. Psychol Bull 132 : 560 581.
29. Howell KK, Lynch ME, Platzman KA, Smith GH, Coles CD (2006) Prenatal alcohol exposure and ability, academic achievement, and school functioning in adolescence: a longitudinal follow-up. J Pediatr Psychol 31 : 116 126.
30. Hoyme HE, May PA, Kalberg WO, Kodituwakku P, Gossage JP, Trujillo PM 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.
31. Hubbard EM, Piazza M, Pinel P, Dehaene S (2005) Interactions between number and space in parietal cortex. Nat Rev Neurosci 6 : 435 448.
32. Jacobson SW, Chiodo LM, Jacobson JL, Sokol RJ (2002a) Validity of maternal report of alcohol, cocaine, and smoking during pregnancy in relation to infant neurobehavioral outcome. Pediatrics 109 : 815 825.
33. Jacobson SW, Dodge N, Dehaene S, Chiodo LM, Sokol RJ, Jacobson JL (2003) Evidence for a specific effect of prenatal alcohol on "number sense." Alcohol Clin Exp Res 27 : 121A.
34. Jacobson SW, Hay A, Molteno C, Marais AS, Carter RC, September M et al. (2002b) FAS and neurobehavioral deficits in alcohol-exposed South African infants. Alcohol Clin Exp Res 26 : 175A.
35. Jacobson JL, Jacobson SW, Molteno CD, Odendaal H (2006) A prospective examination of the incidence of heavy drinking during pregnancy among Cape Coloured South African women. Alcohol Clin Exp Res 30 : 233A.
36. Jacobson SW, Jacobson JL, Sokol RJ, Chiodo LM, 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. Alcohol Clin Exp Res 28 : 1732 1745.
37. Jacobson SW, Stanton ME, Molteno CD, Burden MJ, Fuller DS, Hoyme HE et al. (2008) Impaired eyeblink conditioning in children with fetal alcohol syndrome. Alcohol Clin Exp Res 32 : 365 372.
38. Jones KL, Smith DW (1973) Recognition of the fetal alcohol syndrome in early infancy. Lancet 2 : 999 1001.
39. 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.
40. Kaufman L, Vogel SE, Wood G, Kremser C, Schocke M, Zimmerhackl L et al. (2008) A developmental fMRI study of nonsymbolic numerical and spatial processing. Cortex 44 : 376 385.
41. 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. Cogn Brain Res 18 : 225 231.
42. Kong J, Wang C, Kwong K, Vangel M, Chua E, Gollub R (2005) The neural substrate of arithmetic operations and procedure complexity. Brain Res Cogn Brain Res 22 : 397 405.
43. Kopera-Frye K, Dehaene S, Streissguth AP (1996) Impairments of number processing induced by prenatal alcohol exposure. Neuropsychologia 34 : 1187 1196.
44. 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. Behav Brain Funct 2 : 31.
45. Lanphear BP, Dietrich K, Auinger P, Cox C (2000) Cognitive deficits associated with blood lead concentrations <10 microg/dL in US children and adolescents. Public Health Rep 115 : 521 529.
46. Maldonado G, Greenland S (1993) Simulation study of confounder-selection strategies. Am J Epidemiol 138 : 923 936.
47. Mattson SN, Riley EP, Gramling L, Delis DC, Jones KL (1997) Heavy prenatal alcohol exposure with or without physical features of fetal alcohol syndrome leads to IQ deficits. J Pediatr 131 : 718 721.
48. May PA, Brooke L, Gossage JP, Croxford J, Adnams C, Jones KL et al. (2000) Epidemiology of fetal alcohol syndrome in a South African community in the Western Cape Province. Am J Public Health 90 : 1905 1912.
49. Meintjes EM, Jacobson SW, Molteno CD, Gatenby JC, Warton C, Cannistraci CJ, Gore JC, Jacobson JL (2010) An fMRI study of magnitude comparison and exact addition in children. Magn Reson Imaging 28 : 351 362.
50. Menon V, Rivera SM, White CD, Glover GH, Reiss AL (2000) Dissociating prefrontal and parietal cortex activation during arithmetic processing. NeuroImage 12 : 357 365.
51. Mesulam MM, Nobre AC, Kim YH, Parish TB, Gitelman DR (2001) Heterogeneity of cingulate contributions to spatial attention. NeuroImage 13 : 1065 1072.
52. Molko N, Cachia A, Rivière D, Mangin JF, Bruandet M, Le Bihan D, Cohen L, Dehaene S (2003) Functional and structural alterations of the intraparietal sulcus in a developmental dyscalculia of genetic origin. Neuron 40 : 847 858.
53. Naccache L, Dehaene S (2001) The priming method: imaging unconscious repetition priming reveals an abstract representation of number in the parietal lobes. Cereb Cortex 11 : 966 974.
54. Pesenti M, Thioux M, Seron X, De Volder A (2000) Neuroanatomical substrates of Arabic number processing, numerical comparison, and simple addition: a PET study. J Cogn Neurosci 12 : 461 479.
55. Piazza M, Giacomini E, Le Bihan D, Dehaene S (2003) Single-trial classification of parallel pre-attentive and serial attentive processes using functional magnetic resonance imaging. Proc R Soc Lond B Biol Sci 270 : 1237 1245.
56. Pinel P, Dehaene S, Riviere D, Le Bihan D (2001) Modulation of parietal activation by semantic distance in a number comparison task. Neuroimage 14 : 1013 1026.
57. Price GR, Holloway I, Rasanen P, Vesterinen M, Ansari D (2007) Impaired parietal magnitude processing in developmental dyscalculia. Curr Biol 17 : R1042 R1043.
58. Qin Y, Carter CS, Silk EM, Stenger VA, Fissell K, Goode A, Anderson JR (2004) The change of the brain activation patterns as children learn algebra equation solving. Proc Natl Acad Sci USA 101 : 5686 5691.
59. Ridderinkhof KR, Ullsperger M, Crone EA, Nieuwenhuis S (2004) The role of the medial frontal cortex in cognitive control. Science 306 : 443 447.
60. Santhanam P, Li P, Hu X, Lynch ME, Coles C (2009) Effects of prenatal alcohol exposure on brain activation during an arithmetic task: an fMRI study. Alcohol Clin Exp Res 33 : 1901 1908.
61. Sattler JM (1992) Assessment of Children, 3rd ed. Jerome M. Sattler, Inc
62. Simon O, Mangin JF, 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.
63. Small DM, Gitelman DR, Gregory MD, Nobre AC, Parrish TB, Musulam M (2003) The posterior cingulate and medial prefrontal cortex mediate the anticipatory allocation of spatial attention. NeuroImage 18 : 633 641.
64. Sokol RJ, Debanne S, Ager J, Martier S, Ernhart C, Chik L (1985) Maximizing the efficiency of a study on alcohol-related birth defects by means of data collection and analytic strategy dissociation. Am J Perinatol 2 : 245 249.
65. Sowell ER, Lu LH, O'Hare ED, McCourt ST, Mattson SN, O'Connor MJ, Bookheimer SY (2007) Functional magnetic resonance imaging of verbal learning in children with heavy prenatal alcohol exposure. Neuroreport 18 : 635 639.
66. Sowell ER, Mattson SN, Kan E, Thompson PM, Riley ER, Toga AW (2008) Abnormal cortical thickness and brain-behavior correlation patterns in individuals with heavy prenatal alcohol exposure. Cereb Cortex 18 : 126 144.
67. Sowell ER, Mattson SN, Thompson PM, Jernigan TL, Riley EP, Toga AW (2001b) Mapping callosal morphology and cognitive correlates: effects of heavy prenatal alcohol exposure. Neurology 57 : 235 244.
68. Sowell ER, Thompson PM, Mattson SN, Tessner KD, Jernigan TL, Riley EP et al. (2001a) Voxel-based morphometric analyses of the brain in children and adolescents prenatally exposed to alcohol. Neuroreport 12 : 515 523.
69. Sowell ER, Thompson PM, Mattson SN, Tessner KD, Jernigan TL, Riley EP et al. (2002) Regional brain shape abnormalities persist into adolescence after heavy prenatal alcohol exposure. Cereb Cortex 12 : 856 865.
70. Stanescu-Cosson R, Pinel P, van de Moortele PF, Le Bihan D, Cohen L, Dehaene S (2000) Understanding dissociations in dyscalculia: a brain imaging study of the impact of number size on the cerebral networks for exact and approximate calculation. Brain 123 : 2240 2255.
71. Stratton K, Howe C, Battaglia F (1996) Fetal alcohol syndrome: diagnosis, epidemiology, prevention, and treatment. National Academy Press
72. Streissguth AP, Aase JM, Clarren SK, Randels SP, LaDue RA, Smith DF (1991) Fetal Alcohol Syndrome in adolescents and adults. JAMA 265 : 1961 1967.
73. Streissguth AP, Barr HM, Carmichael Olson H, Sampson PD, Bookstein FL, Burgess DM (1994) Drinking during pregnancy decreases word attack and arithmetic scores on standardized tests: adolescent data from a population-based prospective study. Alcohol Clin Exp Res 18 : 248 254.
74. Streissguth AP, Bookstein FL, Sampson PD, Barr HM (1989) Neurobehavioral effects of prenatal alcohol: part III. PLS analyses of neuropsychologic tests. Neurotoxicol Teratol 11 : 493 507.
75. Temple E, Posner MI (1998) Brain mechanisms of quantity are similar in 5-year-old children and adults. Proc Natl Acad Sci USA 95 : 7836 7841.
76. Venkatraman V, Ansari D, Chee MWL (2005) Neural correlates of symbolic and non-symbolic arithmetic. Neuropsychologia 43 : 744 753.
77. Wynn K, Bloom P, Chiang WC (2002) Enumeration of collective entities by 5-month-old infants. Cognition. 83 : B55 B62.
78. 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.