Differences in cortico-striatal-cerebellar activation during working memory in syndromal and nonsyndromal children with prenatal alcohol exposure

Human Brain Mapping

Volumn 34, Issue 8, 2013, Pages 1931-1945

  Diwadkar, Vaibhav A ^a   Meintjes, Ernesta M ^b   Goradia, Dhruman ^a   Dodge, Neil C ^a   Warton, Christopher ^b   Molteno, Christopher D ^b   Jacobson, Sandra W ^a,b   Jacobson, Joseph L ^a,b  

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

^b UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

Fetal alcohol spectrum disorder; Fetal alcohol syndrome; FMRI; Prenatal alcohol exposure; Working memory

Indexed keywords

ALCOHOL;

ARTICLE; BRAIN CORTEX; CAUDATE NUCLEUS; CEREBELLUM; CHILD; CHILDHOOD DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DIAGONAL BAND OF BROCA; FEMALE; FETAL ALCOHOL SYNDROME; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INFERIOR FRONTAL GYRUS; MALE; MENTAL TASK; NEUROIMAGING; NEUROPSYCHOLOGICAL TEST; PARIETAL CORTEX; POTENTIAL DIFFERENCE; PREFRONTAL CORTEX; PREGNANCY; PRENATAL EXPOSURE; PRIORITY JOURNAL; PUTAMEN; SCHOOL CHILD; SENSITIVITY ANALYSIS; VERBAL MEMORY; WORKING MEMORY;

FETAL ALCOHOL SPECTRUM DISORDER; FETAL ALCOHOL SYNDROME; FMRI; PRENATAL ALCOHOL EXPOSURE; WORKING MEMORY;

ALCOHOL DRINKING; BRAIN; BRAIN MAPPING; CHILD; FEMALE; FETAL ALCOHOL SPECTRUM DISORDERS; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, SHORT-TERM; NEUROPSYCHOLOGICAL TESTS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84880134391     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22042     Document Type: Article

References (75)

1. Annett M ( 1970): A classification of hand preference by association analysis. Br J Psychology 61: 303-321.
2. Archibald SL, Fennema-Notestine C, Gamst A, Riley EP, Mattson SN, Jernigan TL ( 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. Astley SJ, Aylward EH, Olson HC, Kerns K, Brooks A, Coggins TE, Davies J, Dorn S, Gendler B, Jirikowic T, Kraegel P, Maravilla K, Richards T ( 2009a): Functional magnetic resonance imaging outcomes from a comprehensive magnetic resonance study of children with fetal alcohol spectrum disorders. J Neurodev Disord 1: 61-80.
5. Astley SJ, Aylward EH, Olson HC, Kerns K, Brooks A, Coggins TE, Davies J, Dorn S, Gendler B, Jirikowic T, Kraegel P, Maravilla K, Richards T ( 2009b): Magnetic resonance imaging outcomes from a comprehensive magnetic resonance study of children with fetal alcohol spectrum disorders. Alcohol Clin Exp Res 33: 1671-1689.
6. Baddeley A ( 1992): Working memory. Science 255: 556-559.
7. Baddeley A ( 1996): The fractionation of working memory. Proc Natl Acad Sci USA 93: 13468-13472.
8. Bakshi N, Pruitt P, Radwan J, Keshavan MS, Rajan U, Zajac-Benitez C, Diwadkar VA ( 2011): Inefficiently increased anterior cingulate modulation of cortical systems during working memory in young offspring of schizophrenia patients. J Psychiatr Res 45: 1067-1076.
9. Bledowski C, Kaiser J, Rahm B ( 2010): Basic operations in working memory: Contributions from functional imaging studies. Behav Brain Res 214: 172-179.
10. Burden MJ, Jacobson SW, Sokol RJ, Jacobson JL ( 2005): Effects of prenatal alcohol exposure on attention and working memory at 7.5 years of age. Alcohol Clin Exp Res 29: 443-452.
11. Callicott JH, Mattay VS, Verchinski BA, Marenco S, Egan MF, Weinberger DR ( 2003): Complexity of prefrontal cortical dysfunction in schizophrenia: More than up or down. Am J Psychiatry 160: 2209-2215.
12. Carter RC, Jacobson SW, Molteno CD, Chiodo LM, Viljoen D, Jacobson JL ( 2005): Effects of prenatal alcohol exposure on infant visual acuity. J Pediatr 147: 473-479.
13. Casey BJ, Cohen JD, Jezzard P, Turner R, Noll DC, Trainor RJ, Giedd J, Kaysen D, Hertz-Pannier L, Rapoport JL ( 1995): Activation of prefrontal cortex in children during a nonspatial working memory task with functional MRI. Neuroimage 2: 221-229.
14. Chang C, Crottaz-Herbette S, Menon V ( 2007): Temporal dynamics of basal ganglia response and connectivity during verbal working memory. Neuroimage 34: 1253-1269.
15. Chein JM, Fissell K, Jacobs S, Fiez JA ( 2002): Functional heterogeneity within Broca's area during verbal working memory. Physiol Behav 77: 635-639.
16. Chen SH, Desmond JE ( 2005): Cerebrocerebellar networks during articulatory rehearsal and verbal working memory tasks. Neuroimage 24: 332-338.
17. Cohen JD, Perlstein WM, Braver TS, Nystrom LE, Noll DC, Jonides J, Smith EE ( 1997): Temporal dynamics of brain activation during a working memory task. Nature 386: 604-608.
18. Coles CD, Platzman KA, Raskind-Hood CL, Brown RT, Falek A, Smith IE ( 1997): A comparison of children affected by prenatal alcohol exposure and attention deficit, hyperactivity disorder. Alcohol Clin Exp Res 21: 150-161.
19. Connor PD, Sampson PD, Bookstein FL, Barr HM, Streissguth AP ( 2000): Direct and indirect effects of prenatal alcohol damage on executive function. Dev Neuropsychol 18: 331-354.
20. Croxford J, Viljoen D ( 1999): Alcohol consumption by pregnant women in the Western Cape. S Afr Med J 89: 962-965.
21. Desmond JE, Chen SH, DeRosa E, Pryor MR, Pfefferbaum A, Sullivan EV ( 2003): Increased frontocerebellar activation in alcoholics during verbal working memory: An fMRI study. Neuroimage 19: 1510-1520.
22. Desmond JE, Gabrieli JD, Wagner AD, Ginier BL, Glover GH ( 1997): Lobular patterns of cerebellar activation in verbal working-memory and finger-tapping tasks as revealed by functional MRI. J Neurosci 17: 9675-9685.
23. Dickstein SG, Bannon K, Castellanos FX, Milham MP ( 2006): The neural correlates of attention deficit hyperactivity disorder: An ALE meta-analysis. J Child Psychol Psychiatry 47: 1051-1062.
24. Diwadkar VA, Pruitt P, Zhang A, Radwan J, Keshavan MS, Murphy E, Rajan U, Zajac-Benitez C ( 2012): The neural correlates of performance in adolescents at risk for schizophrenia: Inefficiently increased cortico-striatal responses measured with fMRI. J Psychiatr Res 46: 12-21.
25. 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.
26. Durisko C, Fiez JA ( 2010): Functional activation in the cerebellum during working memory and simple speech tasks. Cortex 46: 896-906.
27. Eckert MA, Leonard CM, Richards TL, Aylward EH, Thomson J, Berninger VW ( 2003): Anatomical correlates of dyslexia: Frontal and cerebellar findings. Brain 126: 482-494.
28. Edin F, Macoveanu J, Olesen P, Tegner J, Klingberg T ( 2007): Stronger synaptic connectivity as a mechanism behind development of working memory-related brain activity during childhood. J Cogn Neurosci 19: 750-760.
29. 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.
30. 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.
31. Hoyme HE, May PA, Kalberg WO, Kodituwakku P, Gossage JP, Trujillo PM, Buckley DG, Miller JH, Aragon AS, Khaole N, Viljoen DL, Jones KL, Robinson LK ( 2005): A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: Clarification of the 1996 institute of medicine criteria. Pediatrics 115: 39-47.
32. 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.
33. Jacobson SW, Chiodo LM, Sokol RJ, Jacobson JL ( 2002): Validity of maternal report of prenatal alcohol, cocaine, and smoking in relation to neurobehavioral outcome. Pediatrics 109: 815-825.
34. Jacobson SW, Stanton ME, Molteno CD, Burden MJ, Fuller DS, Hoyme HE, Robinson LK, Khaole N, Jacobson JL ( 2008): Impaired eyeblink conditioning in children with fetal alcohol syndrome. Alcohol Clin Exp Res 32: 365-372.
35. Jansma JM, Ramsey NF, van der Wee NJ, Kahn RS ( 2004): Working memory capacity in schizophrenia: A parametric fMRI study. Schizophr Res 68: 159-171.
36. Kerns KA, Don A, Mateer CA, Streissguth AP ( 1997): Cognitive deficits in nonretarded adults with fetal alcohol syndrome. J Learn Disabil 30: 685-693.
37. Kirschen MP, Chen SH, Schraedley-Desmond P, Desmond JE ( 2005): Load- and practice-dependent increases in cerebro-cerebellar activation in verbal working memory: An fMRI study. NeuroImage 24: 462-472.
38. Kodituwakku PW, Handmaker NS, Cutler SK, Weathersby EK, Handmaker SD ( 1995): Specific impairments in self-regulation in children exposed to alcohol prenatally. Alcohol Clin Exp Res 19: 1558-1564.
39. Landau SM, Lal R, O'Neil JP, Baker S, Jagust WJ ( 2009): Striatal dopamine and working memory. Cereb Cortex 19: 445-454.
40. Lewis SJ, Dove A, Robbins TW, Barker RA, Owen AM ( 2004): Striatal contributions to working memory: A functional magnetic resonance imaging study in humans. Eur J Neurosci 19: 755-760.
41. Luna B ( 2009): Developmental changes in cognitive control through adolescence. Adv Child Dev Behav 37: 233-278.
42. Madge EM, vandenberg AR, Robinson M, Landman J ( 1981): Junior South African Individual Scales. Pretoria: Human Sciences Research Council.
43. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH ( 2003): An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19: 1233-1239.
44. Marvel CL, Desmond JE ( 2010): Functional topography of the cerebellum in verbal working memory. Neuropsychol Rev 20: 271-279.
45. Mattson SN, Riley EP, Gramling L, Delis DC, Jones KL ( 1998): Neuropsychological comparison of alcohol-exposed children with or without physical features of fetal alcohol syndrome. Neuropsychology 12: 146-153.
46. May PA, Brooke L, Gossage JP, Croxford J, Adnams C, Jones KL, Robinson L, Viljoen D ( 2000): Epidemiology of fetal alcohol syndrome in a South African community in the Western Cape Province. Am J Public Health 90: 1905-1912.
47. May PA, Gossage JP, Marais AS, Adnams CM, Hoyme HE, Jones KL, Robinson LK, Khaole NC, Snell C, Kalberg WO, Hendricks L, Brooke L, Stellavato C, Viljoen DL ( 2007): The epidemiology of fetal alcohol syndrome and partial FAS in a South African community. Drug Alcohol Depend 88: 259-271.
48. McNab F, Klingberg T ( 2008): Prefrontal cortex and basal ganglia control access to working memory. Nat Neurosci 11: 103-107.
49. Meintjes EM, Jacobson JL, Molteno CD, Gatenby JC, Warton C, Cannistraci CJ, Hoyme HE, Robinson LK, Khaole N, Gore JC, Jacobson SW ( 2010): An FMRI study of number processing in children with fetal alcohol syndrome. Alcohol Clin Exp Res 34: 1450-1464.
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. Nardelli A, Lebel C, Rasmussen C, Andrew G, Beaulieu C ( 2011): Extensive deep gray matter volume reductions in children and adolescents with fetal alcohol spectrum disorders. Alcohol Clin Exp Res 35: 1404-1417.
52. Nichols T, Brett M, Andersson J, Wager T, Poline JB ( 2005): Valid conjunction inference with the minimum statistic. Neuroimage 25: 653-660.
53. O'Hare ED, Lu LH, Houston SM, Bookheimer SY, Mattson SN, O'Connor MJ, Sowell ER ( 2009): Altered frontal-parietal functioning during verbal working memory in children and adolescents with heavy prenatal alcohol exposure. Hum Brain Mapp 30: 3200-3208.
54. Olson HC, 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.
55. Pfefferbaum A, Desmond JE, Galloway C, Menon V, Glover GH, Sullivan EV ( 2001): Reorganization of frontal systems used by alcoholics for spatial working memory: An fMRI study. NeuroImage 14: 7-20.
56. Ravizza SM, Delgado MR, Chein JM, Becker JT, Fiez JA ( 2004): Functional dissociations within the inferior parietal cortex in verbal working memory. Neuroimage 22: 562-573.
57. Roussotte FF, Bramen JE, Nunez SC, Quandt LC, Smith L, O'Connor MJ, Bookheimer SY, Sowell ER ( 2011): Abnormal brain activation during working memory in children with prenatal exposure to drugs of abuse: The effects of methamphetamine, alcohol, and polydrug exposure. NeuroImage 54: 3067-3075.
58. Salmi J, Pallesen KJ, Neuvonen T, Brattico E, Korvenoja A, Salonen O, Carlson S ( 2009): Cognitive and motor loops of the human cerebro-cerebellar system. J Cogn Neurosci 22: 2663-2676.
59. Santhanam P, Li Z, Hu X, Lynch ME, Coles CD ( 2009): Effects of prenatal alcohol exposure on brain activation during an arithmetic task: An fMRI study. Alcohol Clin Exp Res 33: 1901-1908.
60. Schneider ML, Moore CF, Barnhart TE, Larson JA, DeJesus OT, Mukherjee J, Nickles RJ, Converse AK, Roberts AD, Kraemer GW ( 2005): Moderate-level prenatal alcohol exposure alters striatal dopamine system function in rhesus monkeys. Alcohol Clin Exp Res 29: 1685-1697.
61. Smith EE, Jonides J ( 1998): Neuroimaging analyses of human working memory. Proc Natl Acad Sci USA 95: 12061-12068.
62. Sowell ER, Thompson PM, Mattson SN, Tessner KD, Jernigan TL, Riley EP, Toga AW ( 2002): Regional brain shape abnormalities persist into adolescence after heavy prenatal alcohol exposure. Cereb Cortex 12: 856-865.
63. 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.
64. Sowell ER, Mattson SN, Kan E, Thompson PM, Riley EP, Toga AW ( 2008): Abnormal cortical thickness and brain-behavior correlation patterns in individuals with heavy prenatal alcohol exposure. Cereb Cortex 18: 136-144.
65. Spadoni AD, Bazinet AD, Fryer SL, Tapert SF, Mattson SN, Riley EP ( 2009): BOLD response during spatial working memory in youth with heavy prenatal alcohol exposure. Alcohol Clin Exp Res 33: 2067-2076.
66. Stoodley CJ, Schmahmann JD ( 2009): Functional topography in the human cerebellum: A meta-analysis of neuroimaging studies. Neuroimage 44: 489-501.
67. Stoodley CJ, Valera EM, Schmahmann JD ( 2010): An fMRI study of intra-individual functional topography in the human cerebellum. Behav Neurol 23: 65-79.
68. Strand F, Forssberg H, Klingberg T, Norrelgen F ( 2008): Phonological working memory with auditory presentation of pseudo-words-An event related fMRI Study. Brain Res 1212: 48-54.
69. Stratton KM, Howe C, Battaglia F ( 1996): Fetal Alcohol Syndrome: Diagnosis, Epidemiology, Prevention, and Treatment. Washington, DC: National Academy Press.
70. Streissguth AP, Bookstein FL, Sampson PD, Barr HM ( 1993): The Enduring Effects of Prenatal Alcohol Exposure on Child Development, Birth Through 7 Years: A Partial Least Squares Solution. Ann Arbor: University of Michigan Press.
71. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M ( 2002): Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15: 273-289.
72. Vasic N, Lohr C, Steinbrink C, Martin C, Wolf RC ( 2008): Neural correlates of working memory performance in adolescents and young adults with dyslexia. Neuropsychologia 46: 640-648.
73. Voytek B, Knight RT ( 2010): Prefrontal cortex and basal ganglia contributions to visual working memory. Proc Natl Acad Sci USA 107: 18167-18172.
74. Wager TD, Smith EE ( 2003): Neuroimaging studies of working memory: A meta-analysis. Cogn Affect Behav Neurosci 3: 255-274.
75. Wolf RC, Plichta MM, Sambataro F, Fallgatter AJ, Jacob C, Lesch KP, Herrmann MJ, Schonfeldt-Lecuona C, Connemann BJ, Gron G, Vasic N ( 2009): Regional brain activation changes and abnormal functional connectivity of the ventrolateral prefrontal cortex during working memory processing in adults with attention-deficit/hyperactivity disorder. Hum Brain Mapp 30: 2252-2266.