Common and specific impairments in attention functioning in girls with chromosome 22q11.2 deletion, fragile X or Turner syndromes

Journal of Neurodevelopmental Disorders

Tony J Simon²  Judith L Ross¹  Danielle J Harvey⁴  Elliott A Beaton³  Andrea I Quintero² 

[1] Department of Pediatrics, Thomas Jefferson University, 1025 Walnut Street, Philadelphia, PA 19107, USA;MIND Institute and Department of Psychiatry and Behavioral Sciences, University of California, Davis, 2825 50th Street, Sacramento, CA 95817, USA;Department of Psychology, University of New Orleans, 2000 Lakeshore Drive, New Orleans, LA 70148, USA;Department of Public Health, Division of Biostatistics, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA

关键词: Turner syndrome;    Fragile X syndrome;    DiGeorge syndrome;    Velocardiofacial syndrome;    Chromosome 22q11.2 deletion syndrome;    Developmental disorder;    Cognitive development;    Visuospatial cognition;    Attention networks test;   

Others  :  804510
DOI  :  10.1186/1866-1955-6-5

 received in 2013-06-28, accepted in 2014-02-26,  发布年份 2014

【 摘 要 】

Background

Chromosome 22q11.2 deletion syndrome (22q11.2DS), fragile X syndrome (FXS), and Turner syndrome (TS) are complex and variable developmental syndromes caused by different genetic abnormalities; yet, they share similar cognitive impairments in the domains of numbers, space, and time. The atypical development of foundational neural networks that underpin the attentional system is thought to result in further impairments in higher-order cognitive functions. The current study investigates whether children with similar higher-order cognitive impairments but different genetic disorders also show similar impairments in alerting, orienting, and executive control of attention.

Methods

Girls with 22q11.2DS, FXS, or TS and typically developing (TD) girls, aged 7 to 15 years, completed an attention network test, a flanker task with alerting and orienting cues. Exploration of reaction times and accuracy allowed us to test for potential commonalities in attentional functioning in alerting, orienting, and executive control. Linear regression models were used to test whether the predictors of group and chronological age were able to predict differences in attention indices.

Results

Girls with 22q11.2DS, FXS, or TS demonstrated unimpaired function of the alerting system and impaired function of the executive control system. Diagnosis-specific impairments were found such that girls with FXS made more errors and had a reduced orienting index, while girls with 22q11.2DS showed specific age-related deficits in the executive control system.

Conclusions

These results suggest that the control but not the implementation of attention is selectively impaired in girls with 22q11.2DS, TS or FXS. Additionally, the age effect on executive control in girls with 22q11.2DS implies a possible altered developmental trajectory.

【 授权许可】

   
2014 Quintero et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Kravitz DJ, Saleem KS, Baker CI, Mishkin M: A new neural framework for visuospatial processing. Nat Rev Neurosci 2011, 12(4):217-230.
• [2]Nieder A, Dehaene S: Representation of number in the brain. Annu Rev Neurosci 2009, 32:185-208.
• [3]Corbetta M, Patel G, Shulman GL: The reorienting system of the human brain: from environment to theory of mind. Neuron 2008, 58(3):306-324.
• [4]Simon TJ: A new account of the neurocognitive foundations of impairments in space, time and number processing in children with chromosome 22q11.2 deletion syndrome. Dev Disabil Res Rev 2008, 14:52-58.
• [5]Scerif G: Attention trajectories, mechanisms and outcomes: at the interface between developing cognition and environment. Dev Sci 2010, 13(6):805-812.
• [6]Walter E, Mazaika PK, Reiss AL: Insights into brain development from neurogenetic syndromes: evidence from fragile X syndrome, Williams syndrome, Turner syndrome and velocardiofacial syndrome. Neuroscience 2009, 164:257-271.
• [7]Scerif G, Steele A: Neurocognitive Development of Attention Across Genetic Syndromes: Inspecting a Disorder. Prog Brain Res 2011, 189:285-301.
• [8]Simon TJ: Clues to the foundations of numerical cognitive impairments: evidence from genetic disorders. Dev Neuropsychol 2011, 36(6):788-805.
• [9]Cornish K, Scerif G, Karmiloff-Smith A: Tracing syndrome-specific trajectories of attention across the lifespan. Cortex 2007, 43(6):672-685.
• [10]Munir F, Cornish KM, Wilding J: A neuropsychological profile of attention deficits in young males with fragile X syndrome. Neuropsychologia 2000, 38(9):1261-1270.
• [11]Cornish KM, Munir F, Cross G: Differential impact of the FMR-1 full mutation on memory and attention functioning: a neuropsychological perspective. J Cogn Neurosci 2001, 13:144-150.
• [12]Scerif G, Cornish K, Wilding J, Driver J, Karmiloff-Smith A: Visual search in typically developing toddlers and toddlers with Fragile X or Williams syndrome. Dev Sci 2004, 7:116-130.
• [13]Mazzocco MMM, Singh Bhatia N, Lesniak-Karpiak K: Visuospatial skills and their association with math performance in girls with fragile X or Turner syndrome. Child Neuropsychol 2006, 12(2):87-110.
• [14]Lasker AG, Mazzocco MMM, Zee DS: Ocular motor indicators of executive dysfunction in fragile X and Turner syndromes. Brain Cogn 2007, 63(3):203-220.
• [15]Simon TJ, Takarae Y, DeBoer T, McDonald-McGinn DM, Zackai EH, Ross JL: Overlapping numerical cognition impairments in children with chromosome 22q11.2 deletion or Turner syndromes. Neuropsychologia 2008, 46:82-94.
• [16]Campbell LE, Stevens A, Daly E, Toal F, Azuma R, Karmiloff-Smith A, Murphy DGM, Murphy KC: A comparative study of cognition and brain anatomy between two neurodevelopmental disorders: 22q11.2 deletion syndrome and Williams syndrome. Neuropsychologia 2009, 47(4):1034-1044.
• [17]Botto LD, May K, Fernhoff PM, Correa A, Coleman K, Rasmussen SA, Merritt RK, O’Leary LA, Wong LY, Elixson EM, Mahle WT, Campbell RM: A population-based study of the 22q11.2 deletion: phenotype, incidence, and contribution to major birth defects in the population. Pediatrics 2003, 112(1 Pt 1):101-107.
• [18]Robin NH, Shprintzen RJ: Defining the clinical spectrum of deletion 22q11.2. J Peds 2005, 147(1):90-96.
• [19]Kobrynski LJ, Sullivan KE: Velocardiofacial syndrome, DiGeorge syndrome: the chromosome 22q11.2 deletion syndromes. Lancet 2007, 370(9596):1443-1452.
• [20]Moss EM, Batshaw ML, Solot CB, Gerdes M, McDonald-McGinn DM, Driscoll DA, Emanuel BS, Zackai EH, Wang PP: Psychoeducational profile of the 22q11.2 microdeletion: a complex pattern. J Pediatr 1999, 134(2):193-198.
• [21]Woodin MF, Wang PP, Aleman D, McDonald-McGinn DM, Zackai EH, Moss E: Neuropsychological profile of children and adolescents with the 22q11.2 microdeletion. Genet Med 2001, 3:34-39.
• [22]Jacobson C, Shearer J, Habel A, Kane F, Tsakanikos E, Kravariti E: Core neuropsychological characteristics of children and adolescents with 22q11.2 deletion. J Intellect Disabil Res 2010, 54(8):701-713.
• [23]Simon TJ, Bearden CE, Mc-Ginn DM, Zackai EH: Visuospatial and numerical cognitive deficits in children with chromosome 22q11.2 deletion syndrome. Cortex 2005, 41(2):145-155.
• [24]Bish JP, Chiodo R, Mattei V, Simon TJ: Domain specific attentional impairments in children with chromosome 22q11.2 deletion syndrome. Brain Cogn 2007, 64(3):265-273.
• [25]Sobin C, Kiley-Brabeck K, Daniels S, Blundell M, Anyane-Yeboa K, Karayiorgou M: Networks of attention in children with the 22q11 deletion syndrome. Dev Neuropsychol 2004, 26(2):611-626.
• [26]Bish JP, Ferrante SM, McDonald-McGinn DM, Zackai EH, Simon TJ: Maladaptive conflict monitoring as evidence for executive dysfunction in children with chromosome 22q11.2 deletion syndrome. Dev Sci 2005, 8:36-43.
• [27]Swillen A, Devriendt K, Legius E, Prinzie P, Vogels A, Ghesquière P, Fryns JP: The behavioural phenotype in velo-cardio-facial syndrome (VCFS): from infancy to adolescence. Genet Couns 1999, 10:79-88.
• [28]Swillen A, Devriendt K, Legius E, Eyskens B, Dumoulin M, Gewillig M, Fryns JP: Intelligence and psychosocial adjustment in velocardiofacial syndrome: a study of 37 children and adolescents with VCFS. J Med Genet 1997, 34(6):453-458.
• [29]De Smedt B, Swillen A, Verschaffel L, Ghesquière P: Mathematical learning disabilities in children with 22q11.2 deletion syndrome: a review. Dev Disabil Res Rev 2009, 15:4-10.
• [30]Beckett L, Yu Q, Long AN: The impact of Fragile, X: prevalence, numbers affected, and economic impact. A White Paper Prepared for the National Fragile X Foundation, Davis CA, USA. 2005
• [31]Cornish K, Turk J, Wilding J, Sudhalter V, Munir F, Kooy F, Hagerman RJ: Annotation: deconstructing the attention deficit in fragile X syndrome: a developmental neuropsychological approach. J Child Psychol Psychiatry 2004, 45(6):1042-1053.
• [32]Scerif G, Karmiloff-Smith A, Campos R, Elsabbagh M, Driver J, Cornish K: To look or not to look? Typical and atypical development of oculomotor control. J Cogn Neurosci 2005, 17(4):591-604.
• [33]Bray S, Dunkin B, Hong DS, Reiss AL: Reduced functional connectivity during working memory in Turner syndrome. Cereb Cortex 2011, 21(11):2471-2481.
• [34]Bennetto L, Pennington BF, Porter D, Taylor AK, Hagerman RJ: Profile of cognitive functioning in women with the fragile X mutation. Neuropsychology 2001, 15(2):290-299.
• [35]Mazzocco MMM: Math learning disability and math LD subtypes: evidence from studies of Turner syndrome, fragile X syndrome, and neurofibromatosis type 1. J Learn Disabil 2001, 34(6):520-533.
• [36]Hall SS, Burns DD, Lightbody AA, Reiss AL: Longitudinal changes in intellectual development in children with Fragile X syndrome. J Abnorm Child Psychol 2008, 36(6):927-939.
• [37]Hong D, Scaletta Kent J, Kesler SR: Cognitive profile of Turner syndrome. Dev Disabil Res Rev 2009, 15(4):270-278.
• [38]Shaffer JW: A specific cognitive deficit observed in gonadal aplasia (Turner’s syndrome). J Clin Psychol 1962, 18:403-406.
• [39]Lepage JFF, Dunkin B, Hong DS, Reiss AL: Contribution of executive functions to visuospatial difficulties in prepubertal girls with Turner syndrome. Dev Neuropsychol 2011, 36(8):988-1002.
• [40]Ross JL, Zinn A, McCauley E: Neurodevelopmental and psychosocial aspects of Turner syndrome. Ment Retard Dev Disabil Res Rev 2000, 6(2):135-141.
• [41]Posner MI, Petersen SE: The attention system of the human brain. Annu Rev Neurosci 1990, 13:25-42.
• [42]Fan J, McCandliss BD, Sommer T, Raz A, Posner MI: Testing the efficiency and independence of attentional networks. J Cogn Neurosci 2002, 14(3):340-347.
• [43]Fan J, McCandliss BD, Fossella J, Flombaum JI, Posner MI: The activation of attentional networks. NeuroImage 2005, 26(2):471-479.
• [44]Konrad K, Neufang S, Thiel CM, Specht K, Hanisch C, Fan J, Herpertz-Dahlmann B, Fink GR: Development of attentional networks: an fMRI study with children and adults. NeuroImage 2005, 28(2):429-439.
• [45]Fossella J, Sommer T, Fan J, Wu Y, Swanson JM, Pfaff DW, Posner MI: Assessing the molecular genetics of attention networks. BMC Neurosci 2002, 3:14. BioMed Central Full Text
• [46]Cornish K, Wilding J: Attention, Genes, and Developmental Disorders. London: Oxford University Press; 2010.
• [47]Rueda MR, Fan J, McCandliss BD, Halparin JD, Gruber DB, Lercari LP, Posner MI: Development of attentional networks in childhood. Neuropsychologia 2004, 42(8):1029-1040.
• [48]Johnson MH, Grossmann T, Kadosh KC: Mapping functional brain development: building a social brain through interactive specialization. Dev Psychol 2009, 45:151-159.
• [49]Karmiloff-Smith A: Development itself is the key to understanding developmental disorders. Trends Cogn Sci 1998, 2(10):389-398.
• [50]Johnson MH: Functional brain development in humans. Nat Rev Neurosc 2001, 2(7):475-483.
• [51]Atkinson J, Braddick O: Visual attention in the first years: typical development and developmental disorders. Dev Med Child Neurol 2012, 54(7):589-595.
• [52]Hodapp RM, Dykens EM, Hagerman RJ, Schreiner R, Lachiewicz AM, Leckman JF: Developmental implications of changing trajectories of IQ in males with fragile X syndrome. J Am Acad Child Adolesc Psychiatry 1990, 29(2):214-219.
• [53]Riddle JE, Cheema A, Sobesky WE, Gardner SC, Taylor AK, Pennington BF, Hagerman RJ: Phenotypic involvement in females with the FMR1 gene mutation. Am J Ment Retard 1998, 102(6):590-601.
• [54]Antshel KM, Conchelos J, Lanzetta G, Fremont W, Kates WR: Behavior and corpus callosum morphology relationships in velocardiofacial syndrome (22q11.2 deletion syndrome). Psychiatry Res Neuroimaging 2005, 138(3):235-245.
• [55]Sobin C, Kiley-Brabeck K, Monk SH, Khuri J, Karayiorgou M: Sex differences in the behavior of children with the 22q11 deletion syndrome. Psychiatry Res Neuroimaging 2009, 166:24-34.
• [56]Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, Nugent TF, Herman DH, Clasen LS, Toga AW, Rapoport JL, Thompson PM: Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci 2004, 101(21):8174-8179.
• [57]Stoddard J, Beckett L, Simon TJ: Atypical development of the executive attention network in children with chromosome 22q11.2 deletion syndrome. J Neurodevelopmental Disord 2011, 3:76-85.
• [58]Wechsler D: Wechsler Abbreviated Scale of Intelligence. San Antonio: The Psychological Corporation; 1999.
• [59]Wechsler D: The Wechsler Intelligence Scale for Children. San Antonio: The Psychological Corporation; 1991.
• [60]Wechsler D: The Wechsler Intelligence Scale for Children. London: Pearson Assessment; 2004.
• [61]Townsend JT, Ashby FG: The Stochastic Modeling of Elementary Psychological Processes. New York: Cambridge University Press; 1983.
• [62]Machizawa MG, Driver J: Principal component analysis of behavioural individual differences suggests that particular aspects of visual working memory may relate to specific aspects of attention. Neuropsychologia 2011, 49(6):1518-1526.
• [63]Mackie MA, Van Dam NT, Fan J: Cognitive control and attentional functions. Brain Cogn 2013, 82(3):301-312.
• [64]Westlye LT, Grydeland H, Walhovd KB, Fjell AM: Associations between regional cortical thickness and attentional networks as measured by the attention network test. Cereb Cortex 2011, 21(2):345-356.
• [65]Van der Molen MJW, Van der Molen MW, Ridderinkhof KR, Hamel BCJ, Curfs LMG, Ramakers GJA: Attentional set-shifting in fragile X syndrome. Brain Cogn 2012, 78(3):206-217.
• [66]Lewandowski KE, Shashi V, Berry PM, Kwapil TR: Schizophrenic-like neurocognitive deficits in children and adolescents with 22q11 deletion syndrome. Am J Med Genet B Neuropsychiatr Genet 2007, 144B:27-36.
• [67]Parasuraman R, Warm JS, See JE: Brain systems of vigilance. In The Attentive Brain. Edited by Parasuraman R. Cambridge: MIT Press; 1998:221-256.
• [68]Howley SA, Prasad SE, Pender NP, Murphy KC: Relationship between reaction time, fine motor control, and visual-spatial perception on vigilance and visual-motor tasks in 22q11.2 deletion syndrome. Res Dev Disabil 2012, 33(5):1495-1502.
• [69]Sobin C, Kiley-Brabeck K, Karayiorgou M: Lower prepulse inhibition in children with the 22q11 deletion syndrome. Am J Psychiatry 2005, 162(6):1090.
• [70]Romans SM, Roeltgen DP, Kushner H, Ross JL: Executive function in girls with Turner’s syndrome. Dev Neuropsychol 1997, 13:23-40.
• [71]Romans SM, Stefanatos GA, Roeltgen DP, Kushner H, Ross JL: Transition to young adulthood in Ullrich-Turner syndrome: neurodevelopmental changes. Am J Med Genet Part A 1998, 79(2):140-147.
• [72]Ross JL, Stefanatos GA, Kushner H, Zinn A, Bondy C, Roeltgen DP: Persistent cognitive deficits in adult women with Turner syndrome. Neurology 2002, 58(2):218-225.
• [73]Luck SJ, Gold JM: The construct of attention in schizophrenia. Biol Psychiatry 2008, 64(1):34-39.
• [74]Woodcock KA, Oliver C, Humphreys GW: Task-switching deficits and repetitive behaviour in genetic neurodevelopmental disorders: data from children with Prader–Willi syndrome chromosome 15 q11-q13 deletion and boys with Fragile X syndrome. Cogn Neuropsychol 2009, 26(2):172-194.
• [75]Scerif G, Cornish K, Wilding J, Driver J, Karmiloff-Smith A: Delineation of early attentional control difficulties in fragile X syndrome: focus on neurocomputational changes. Neuropsychologia 2007, 45(8):1889-1898.
• [76]Jonides J, Irwin DE: Capturing attention. Cognition 1981, 10:145-150.
• [77]Brodeur DA, Enns JT: Covert visual orienting across the lifespan. Can J Exp Psychol 1997, 51:20-35.
• [78]Shapiro HM, Takarae Y, Harvey DJ, Cabaral MH, Simon TJ: A cross-sectional study of the development of volitional control of spatial attention in children with chromosome 22q11.2 deletion syndrome. J Neurodevelopmental Disord 2012, 4:5. BioMed Central Full Text
• [79]Flanagan T, Enns JT, Murphy MM, Russo N, Abbeduto L, Randolph B, Burack JA: Differences in visual orienting between persons with Down or fragile X syndrome. Brain Cogn 2007, 65:128-134.
• [80]Cavanagh P: Attention routines and the architecture of selection. In Cognitive Neuroscience of Attention. Edited by Posner MI. New York: Guilford Press; 2004:13-28.
• [81]Simon TJ, Luck SJ: Attentional impairments in children with chromosome 22q11.2 deletion syndrome. In Cognitive Neuroscience of Attention. Edited by Posner MI. New York: Guilford Press; 2011:441-453.
• [82]Corbetta M, Kincade JM, Ollinger JM, McAvoy MP, Shulman GL: Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nat Neurosci 2000, 3(3):292-297.
• [83]Corbetta M, Shulman GL: Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 2002, 3(3):215-229.
• [84]Marrocco RT, Davidson MC: Neurochemistry of attention. In The Attentitive Brain. Edited by Parasuraman R. Cambridge: MIT Press; 1998:35-50.
• [85]Bearden CE, van Erp T G M, Dutton RA, Lee AD, Simon TJ, Cannon TD, Emanuel BS, McDonald-McGinn DM, Zackai EH, Thompson PM: Alterations in midline cortical thickness and gyrification patterns mapped in children with 22q11.2 deletions. Cereb Cortex 2009, 19:115-126.
• [86]Lee AD, Leow AD, Lu A, Reiss AL, Hall S, Chiang MC, Toga AW, Thompson PM: 3D pattern of brain abnormalities in Fragile X syndrome visualized using tensor-based morphometry. NeuroImage 2007, 34(3):924-938.
• [87]Rebok GW, Smith CB, Pascualvaca DM, Mirsky AF, Anthony BJ, Kellam SG: Developmental changes in attentional performance in urban children from eight to thirteen years. Child Neuropsychol 1997, 3:28-46.
• [88]Ristic J, Kingstone A: Rethinking attentional development: reflexive and volitional orienting in children and adults. Dev Sci 2009, 12(2):289-296.
• [89]Wahlstrom D, White T, Luciana M: Neurobehavioral evidence for changes in dopamine system activity during adolescence. Neurosci Biobehav Rev 2010, 34(5):631-648.
• [90]Villalon-Reina J, Jahanshad N, Beaton E, Toga AW, Thompson PM, Simon TJ: White matter microstructural abnormalities in girls with chromosome 22q11.2 deletion syndrome, Fragile X or Turner syndrome as evidenced by diffusion tensor imaging. NeuroImage 2013, 81:1-14.