Anterior cingulate cortex surface area relates to behavioral inhibition in adolescents with and without heavy prenatal alcohol exposure

Behavioural Brain Research

Volumn 292, Issue , 2015, Pages 26-35

  Migliorini, Robyn ^a,b   Moore, Eileen M ^a   Glass, Leila ^a,b   Infante, M Alejandra ^a,b   Tapert, Susan F ^c,d   Jones, Kenneth Lyons ^e   Mattson, Sarah N ^a   Riley, Edward P ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b SAN DIEGO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Anterior cingulate cortex; Fetal alcohol spectrum disorders (FASD); Fetal alcohol syndrome (FAS); Prenatal alcohol exposure; Response inhibition; Structural neuroimaging

Indexed keywords

ALCOHOL;

ACCURACY; ADOLESCENT; ANTERIOR CINGULATE; ARTICLE; BRAIN FUNCTION; BRAIN SIZE; CHILD; CHILD BEHAVIOR; COGNITION; CONTROLLED STUDY; CORRELATIONAL STUDY; GRAY MATTER; HUMAN; INHIBITION (PSYCHOLOGY); MALE; NERVE CELL DIFFERENTIATION; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PRENATAL EXPOSURE; PRIORITY JOURNAL; RESPONSE TIME; SURFACE AREA; VELOCITY; ANATOMY AND HISTOLOGY; BEHAVIOR; CASE CONTROL STUDY; CINGULATE GYRUS; FEMALE; FETAL ALCOHOL SYNDROME; NEUROPSYCHOLOGICAL TEST; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY;

ADOLESCENT; BEHAVIOR; CASE-CONTROL STUDIES; CHILD; FEMALE; FETAL ALCOHOL SPECTRUM DISORDERS; GYRUS CINGULI; HUMANS; INHIBITION (PSYCHOLOGY); MAGNETIC RESONANCE IMAGING; MALE; NEUROPSYCHOLOGICAL TESTS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84935031005     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2015.05.037     Document Type: Article

References (71)

1. Hoyme H.E., May P.A., Kalberg W.O., Kodituwakku P., Gossage J.P., Trujillo P.M., et al. A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: clarification of the 1996 institute of medicine criteria. Pediatrics 2005, 115:39-47.
2. Jones K.L., Smith D.W. Recognition of the fetal alcohol syndrome in early infancy. Lancet 1973, 302:999-1001.
3. Mattson S.N., Riley E.P., Gramling L., Delis D.C., Jones K.L. Heavy prenatal alcohol exposure with or without physical features of fetal alcohol syndrome leads to IQ deficits. J. Pediatr. 1997, 131:718-721.
4. Mattson S.N., Riley E.P., Gramling L., Delis D.C., Jones K.L. Neuropsychological comparison of alcohol-exposed children with or without physical features of fetal alcohol syndrome. Neuropsychology 1998, 12:146-153.
5. Bertrand J., Floyd R., Weber M., O'Connor M., Riley E., Johnson K., et al. Fetal Alcohol Syndrome: Guidelines for Referral and Diagnosis 2004, Centers for Disease Control and Prevention, Atlanta, GA.
6. Alvarez J.A., Emory E. Executive function and the frontal lobes: a meta-analytic review. Neuropsychol. Rev. 2006, 16:17-42.
7. Mattson S.N., Roesch S.C., Glass L., Deweese B.N., Coles C.D., Kable J.A., et al. Further development of a neurobehavioral profile of fetal alcohol spectrum disorders. Alcohol. Clin. Exp. Res. 2013, 37:517-528.
8. Mattson S.N., Goodman A.M., Caine C., Delis D.C., Riley E.P. Executive functioning in children with heavy prenatal alcohol exposure. Alcohol. Clin. Exp. Res. 1999, 23:1808-1815.
9. Rasmussen C., Bisanz J. Executive functioning in children with fetal alcohol spectrum disorders: profiles and age-related differences. Child Neuropsychol. 2009, 15:201-215.
10. Connor P.D., Sampson P.D., Bookstein F.L., Barr H.M., Streissguth A.P. Direct and indirect effects of prenatal alcohol damage on executive function. Dev. Neuropsychol. 2000, 18:331-354.
11. Driscoll C.D., Chen J.S., Riley E.P. Passive avoidance performance in rats prenatally exposed to alcohol during various periods of gestation. Neurobehav. Toxicol. Teratol. 1982, 4:99-103.
12. Gallo P.V., Weinberg J. Neuromotor development and response inhibition following prenatal ethanol exposure. Neurobehav. Toxicol. Teratol. 1982, 4:505-513.
13. Olmstead M.C., Martin A., Brien J.F., Reynolds J.N. Chronic prenatal ethanol exposure increases disinhibition and perseverative responding in the adult guinea pig. Behav. Pharmacol. 2009, 20:554-557.
14. Riley E.P., Lochry E.A., Shapiro N.R. Lack of response inhibition in rats prenatally exposed to alcohol. Psychopharmacology (Berl) 1979, 62:47-52.
15. Bari A., Robbins T.W. Inhibition and impulsivity: behavioral and neural basis of response control. Prog. Neurobiol. 2013, 108:44-79.
16. Schonfeld A.M., Paley B., Frankel F., O'Connor M.J. Executive functioning predicts social skills following prenatal alcohol exposure. Child Neuropsychol. 2006, 12:439-452.
17. Kim S., Nordling J.K., Yoon J.E., Boldt L.J., Kochanska G. Effortful control in "hot" and "cool" tasks differentially predicts children's behavior problems and academic performance. J. Abnorm. Child Psychol. 2013, 41:43-56.
18. Fernie G., Peeters M., Gullo M.J., Christiansen P., Cole J.C., Sumnall H., et al. Multiple behavioural impulsivity tasks predict prospective alcohol involvement in adolescents. Addiction 2013, 108:1916-1923.
19. Disney E.R., Iacono W., McGue M., Tully E., Legrand L. Strengthening the case: prenatal alcohol exposure is associated with increased risk for conduct disorder. Pediatrics 2008, 122:e1225-e1230.
20. Bhatara V., Loudenberg R., Ellis R. Association of attention deficit hyperactivity disorder and gestational alcohol exposure: an exploratory study. J. Atten. Disord. 2006, 9:515-522.
21. Fryer S.L., McGee C.L., Matt G.E., Riley E.P., Mattson S.N. Evaluation of psychopathological conditions in children with heavy prenatal alcohol exposure. Pediatrics 2007, 119:e733-e741.
22. Paley B., O'Connor M.J. Intervention for individuals with fetal alcohol spectrum disorders: treatment approaches and case management. Dev. Disabil. Res. Rev. 2009, 15:258-267.
23. Steele V.R., Aharoni E., Munro G.E., Calhoun V.D., Nyalakanti P., Stevens M.C., et al. A large scale (N=102) functional neuroimaging study of response inhibition in a Go/NoGo task. Behav. Brain Res. 2013, 256:529-536.
24. Braver T.S., Barch D.M., Gray J.R., Molfese D.L., Snyder A. Anterior cingulate cortex and response conflict: effects of frequency, inhibition and errors. Cereb. Cortex 2001, 11:825-836.
25. Kerns J.G., Cohen J.D., MacDonald A.W., Cho R.Y., Stenger V.A., Carter C.S. Anterior cingulate conflict monitoring and adjustments in control. Science 2004, 303:1023-1026.
26. Gruber S.A., Rogowska J., Holcomb P., Soraci S., Yurgelun-Todd D. Stroop performance in normal control subjects: an fMRI study. Neuroimage 2002, 16:349-360.
27. Garavan H., Hester R., Murphy K., Fassbender C., Kelly C. Individual differences in the functional neuroanatomy of inhibitory control. Brain Res. 2006, 1105:130-142.
28. Fitzgerald K.D., Zbrozek C.D., Welsh R.C., Britton J.C., Liberzon I., Taylor S.F. Pilot study of response inhibition and error processing in the posterior medial prefrontal cortex in healthy youth. J. Child Psychol. Psychiatry. 2008, 49:986-994.
29. Whelan R., Conrod P.J., Poline J.B., Lourdusamy A., Banaschewski T., Barker G.J., et al. Adolescent impulsivity phenotypes characterized by distinct brain networks. Nat. Neurosci. 2012, 15:920-925.
30. Hart H., Radua J., Nakao T., Mataix-Cols D., Rubia K. Meta-analysis of functional magnetic resonance imaging studies of inhibition and attention in attention-deficit/hyperactivity disorder: exploring task-specific, stimulant medication, and age effects. JAMA Psychiatry 2013, 70:185-198.
31. Chan A.S., Han Y.M., Leung W.W.-M., Leung C., Wong V.C., Cheung M.-C. Abnormalities in the anterior cingulate cortex associated with attentional and inhibitory control deficits: a neurophysiological study on children with autism spectrum disorders. Res. Autism Spectr. Disord. 2011, 5:254-266.
32. Gavita O.A., Capris D., Bolno J., David D. Anterior cingulate cortex findings in child disruptive behavior disorders: a meta-analysis. Aggress. Violent Behav. 2012, 17:507-513.
33. Takeuchi H., Taki Y., Sassa Y., Hashizume H., Sekiguchi A., Nagase T., et al. Regional gray and white matter volume associated with Stroop interference: evidence from voxel-based morphometry. Neuroimage 2012, 59:2899-2907.
34. Borst G., Cachia A., Vidal J., Simon G., Fischer C., Pineau A., et al. Folding of the anterior cingulate cortex partially explains inhibitory control during childhood: a longitudinal study. Dev. Cogn. Neurosci. 2014, 9:126-135.
35. Casey B.J., Trainor R., Giedd J., Vauss Y., Vaituzis C.K., Hamburger S., et al. The role of the anterior cingulate in automatic and controlled processes: a developmental neuroanatomical study. Dev. Psychobiol. 1997, 30:61-69.
36. Fjell A.M., Walhovd K.B., Brown T.T., Kuperman J.M., Chung Y., Hagler D.J., et al. Multimodal imaging of the self-regulating developing brain. Proc. Natl. Acad. Sci. U S A 2012, 109:19620-19625.
37. Fryer S.L., Tapert S.F., Mattson S.N., Paulus M.P., Spadoni A.D., Riley E.P. Prenatal alcohol exposure affects frontal-striatal BOLD response during inhibitory control. Alcohol. Clin. Exp. Res. 2007, 31:1415-1424.
38. O'Brien J.W., Norman A.L., Fryer S.L., Tapert S.F., Paulus M.P., Jones K.L., et al. Effect of predictive cuing on response inhibition in children with heavy prenatal alcohol exposure. Alcohol. Clin. Exp. Res. 2013, 37:644-654.
39. Ware A.L., Infante M.A., O'Brien J.W., Tapert S.F., Jones K.L., Riley E.P., et al. An fMRI study of behavioral response inhibition in adolescents with and without histories of heavy prenatal alcohol exposure. Behav. Brain Res. 2014.
40. Lebel C., Roussotte F., Sowell E.R. Imaging the impact of prenatal alcohol exposure on the structure of the developing human brain. Neuropsychol. Rev. 2011, 21:102-118.
41. Wozniak J.R., Muetzel R.L. What does diffusion tensor imaging reveal about the brain and cognition in fetal alcohol spectrum disorders?. Neuropsychol. Rev. 2011, 21:133-147.
42. Lebel C., Mattson S.N., Riley E.P., Jones K.L., Adnams C.M., May P.A., et al. A longitudinal study of the long-term consequences of drinking during pregnancy: heavy in utero alcohol exposure disrupts the normal processes of brain development. J. Neurosci. 2012, 32:15243-15251.
43. Bjorkquist O.A., Fryer S.L., Reiss A.L., Mattson S.N., Riley E.P. Cingulate gyrus morphology in children and adolescents with fetal alcohol spectrum disorders. Psychiatry Res. 2010, 181:101-107.
44. Panizzon M.S., Fennema-Notestine C., Eyler L.T., Jernigan T.L., Prom-Wormley E., Neale M., et al. Distinct genetic influences on cortical surface area and cortical thickness. Cereb. Cortex 2009, 19:2728-2735.
45. Rakic P. Specification of cerebral cortical areas. Science 1988, 241:170-176.
46. Rakic P. Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 2009, 10:724-735.
47. Wierenga L.M., Langen M., Oranje B., Durston S. Unique developmental trajectories of cortical thickness and surface area. Neuroimage 2014, 87:120-126.
48. Rajaprakash M., Chakravarty M.M., Lerch J.P., Rovet J. Cortical morphology in children with alcohol-related neurodevelopmental disorder. Brain Behav. 2014, 4:41-50.
49. Sowell E.R., Mattson S.N., Kan E., Thompson P.M., Riley E.P., Toga A.W. Abnormal cortical thickness and brain-behavior correlation patterns in individuals with heavy prenatal alcohol exposure. Cereb. Cortex 2008, 18:136-144.
50. Zhou D., Lebel C., Lepage C., Rasmussen C., Evans A., Wyper K., et al. Developmental cortical thinning in fetal alcohol spectrum disorders. Neuroimage 2011, 58:16-25.
51. Shaffer D., Fisher P., Lucas C.P., Dulcan M.K., Schwab-Stone M.E. NIMH Diagnostic Interview Schedule for Children Version IV (NIMH DISC-IV): description, differences from previous versions, and reliability of some common diagnoses. J. Am. Acad. Child Adolesc. Psychiatry 2000, 39:28-38.
52. Desikan R.S., Segonne F., Fischl B., Quinn B.T., Dickerson B.C., Blacker D., et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 2006, 31:968-980.
53. Fischl B., van der Kouwe A., Destrieux C., Halgren E., Segonne F., Salat D.H., et al. Automatically parcellating the human cerebral cortex. Cereb. Cortex 2004, 14:11-22.
54. Reuter M., Rosas H.D., Fischl B. Highly accurate inverse consistent registration: a robust approach. Neuroimage 2010, 53:1181-1196.
55. Segonne F., Dale A.M., Busa E., Glessner M., Salat D., Hahn H.K., et al. A hybrid approach to the skull stripping problem in MRI. Neuroimage 2004, 22:1060-1075.
56. Segonne F., Pacheco J., Fischl B. Geometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Trans. Med. Imaging 2007, 26:518-529.
57. Sled J.G., Zijdenbos A.P., Evans A.C. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans. Med. Imaging 1998, 17:87-97.
58. Wechsler D. Manual for the Wechsler Intelligence Scale for Children-Fourth Edition Integrated 2004, Pearson, San Antonio. 4th ed.
59. Rasmussen C., Tamana S., Baugh L., Andrew G., Tough S., Zwaigenbaum L. Neuropsychological impairments on the NEPSY-II among children with FASD. Child Neuropsychol. 2013, 19:337-349.
60. Hollingshead A.B. Four factor index of social status. Yale J. Sociol. 2011, 8:21-51.
61. Im K., Lee J.M., Lyttelton O., Kim S.H., Evans A.C., Kim S.I. Brain size and cortical structure in the adult human brain. Cereb. Cortex 2008, 18:2181-2191.
62. Dennis M., Francis D.J., Cirino P.T., Schachar R., Barnes M.A., Fletcher J.M. Why IQ is not a covariate in cognitive studies of neurodevelopmental disorders. J. Int. Neuropsychol. Soc. 2009, 15:331-343.
63. Delis D.C., Kaplan E., Kramer J.H. Delis-Kaplan Executive Function System (D-KEFS) 2001, The Psychological Corporation, San Antonio, TX.
64. Bosco C., Diaz E. Placental hypoxia and foetal development versus alcohol exposure in pregnancy. Alcohol Alcohol. 2012, 47:109-117.
65. Bush G., Luu P., Posner M.I. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 2000, 4:215-222.
66. Shaw P., Malek M., Watson B., Sharp W., Evans A., Greenstein D. Development of cortical surface area and gyrification in attention-deficit/hyperactivity disorder. Biol. Psychiatry 2012, 72:191-197.
67. Neta M., Schlaggar B.L., Petersen S.E. Separable responses to error, ambiguity, and reaction time in cingulo-opercular task control regions. Neuroimage 2014, 99:59-68.
68. Burden M.J., Jacobson S.W., Jacobson J.L. Relation of prenatal alcohol exposure to cognitive processing speed and efficiency in childhood. Alcohol. Clin. Exp. Res. 2005, 29:1473-1483.
69. Jacobson S.W. Specificity of neurobehavioral outcomes associated with prenatal alcohol exposure. Alcohol. Clin. Exp. Res. 1998, 22:313-320.
70. Simmons R.W., Wass T., Thomas J.D., Riley E.P. Fractionated simple and choice reaction time in children with prenatal exposure to alcohol. Alcohol. Clin. Exp. Res. 2002, 26:1412-1419.
71. Treit S., Chen Z., Rasmussen C., Beaulieu C. White matter correlates of cognitive inhibition during development: a diffusion tensor imaging study. Neuroscience 2014, 276:87-97.