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Processing Speed Mediates Executive Function Difficulties in Very Preterm Children in Middle Childhood

Published online by Cambridge University Press:  28 March 2011

Hanna Mulder ,
Nicola J. Pitchford  and
Neil Marlow
Hanna Mulder*
Affiliation:
School of Clinical Sciences, University of Nottingham, Nottingham, United Kingdom
Nicola J. Pitchford
Affiliation:
School of Psychology, University of Nottingham, Nottingham, United Kingdom
Neil Marlow
Affiliation:
School of Clinical Sciences, University of Nottingham, Nottingham, United Kingdom
*
Correspondence and reprint requests to: Hanna Mulder, Faculty of Social Sciences, Department of Pedagogical Sciences, Utrecht University, PO Box 80.140, 3508 TC Utrecht, The Netherlands. E-mail: h.mulder2@uu.nl
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Abstract

Executive function and attention difficulties are reported in very preterm (VPT) children at school entry, but it is unclear if these remain at later ages and/or if these difficulties are mediated by more basic functions, such as processing speed. Processing speed has been shown to underlie academic and behavioral problems in VPT children in middle childhood (Mulder, Pitchford, & Marlow, 2010, 2011), so may also underpin executive function and attention difficulties. We investigated this by comparing VPT (gestational age <31 weeks; N = 56) to term children (N = 22) aged 9–10 years on a comprehensive battery of executive function and attention tasks from the Test of Everyday Attention for Children (Manly, Robertson, Anderson, & Nimmo-Smith, 1999) and NEPSY (Korkman, Kirk, & Kemp, 1998). Selective and sustained attention, inhibition, working memory, shifting, verbal fluency, planning, and processing speed were examined. Group differences favoring term children were shown on most executive function tasks (i.e., inhibition, working memory, verbal fluency, and shifting), all of which were mediated by slow processing speed in the VPT group, except response inhibition. Seemingly, processing speed is an important determinant underpinning many neuropsychological deficits seen in VPT children in middle childhood. (JINS, 2011, 17, 445–454)

Keywords

Premature birthInhibitionChildCognitionBehaviorNeuropsychology
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 17 , Issue 3 , May 2011 , pp. 445 - 454
Copyright
Copyright © The International Neuropsychological Society 2011

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References

Aarnoudse-Moens, C.S.H., Smidts, D.P., Oosterlaan, J., Duivenvoorden, H.J., Weisglas-Kuperus, N. (2009). Executive function in very preterm children at early school age. Journal of Abnormal Child Psychology, 37(7), 981–993.CrossRefGoogle ScholarPubMed
Anderson, P.J., Doyle, L.W. (2004). Executive functioning in school-aged children who were born very preterm or with extremely low birth weight in the 1990s. Pediatrics, 114(1), 50–57.Google Scholar
Aron, A.R., Durston, S., Eagle, D.M., Logan, G.D., Stinear, C.M., Stuphorn, V. (2007). Converging evidence for a fronto-basal-ganglia network for inhibitory control of action and cognition. Journal of Neuroscience, 27(44), 11860–11864.Google Scholar
Bayless, S., Stevenson, J. (2007). Executive functions in school-age children born very prematurely. Early Human Development, 83(4), 247–254.CrossRefGoogle ScholarPubMed
Bhutta, A.T., Cleves, M.A., Casey, P.H., Cradock, M.M., Anand, K.J.S. (2002). Cognitive and behavioral outcomes of school-aged children who were born preterm - A meta-analysis. Journal of the American Medical Association, 288(6), 728–737.CrossRefGoogle ScholarPubMed
Blair, C., Razza, R.P. (2007). Relating effortful control, executive function, and false belief understanding to emerging math and literacy ability in kindergarten. Child Development, 78(2), 647–663.Google Scholar
Bohm, B., Smedler, A.C., Forssberg, H. (2004). Impulse control, working memory and other executive functions in preterm children when starting school. Acta Paediatrica, 93(10), 1363–1371.CrossRefGoogle ScholarPubMed
Botting, N., Powls, A., Cooke, R.W., Marlow, N. (1998). Cognitive and educational outcome of very-low-birthweight children in early adolescence. Developmental Medicine & Child Neurology, 40(10), 652–660.Google Scholar
Bracewell, M., Marlow, N. (2002). Patterns of motor disability in very preterm children. Mental Retardation and Developmental Disabilities Research Reviews, 8(4), 241–248.Google Scholar
Brocki, K.C., Bohlin, G. (2004). Executive functions in children aged 6 to 13: A dimensional and developmental study. Developmental Neuropsychology, 26(2), 571–593.CrossRefGoogle ScholarPubMed
Bull, R., Espy, K.A., Wiebe, S.A. (2008). Short-term memory, working memory, and executive functioning in preschoolers: Longitudinal predictors of mathematical achievement at age 7 years. Developmental Neuropsychology, 33(3), 205–228.CrossRefGoogle ScholarPubMed
Cohen, J. (1992). A power primer. Psychological Bulletin, 112(1), 155–159.Google Scholar
Communities & Local Government, English Indices of Deprivation. 2007. Retrieved from http://www.communities.gov.uk.Google Scholar
Constable, R.T., Ment, L.R., Vohr, B.R., Kesler, S.R., Fulbright, R.K., Lacadie, C., Reiss, A.R. (2008). Prematurely born children demonstrate white matter microstructural differences at 12 years of age, relative to term control subjects: An investigation of group and gender effects. Pediatrics, 121(2), 306–316.CrossRefGoogle ScholarPubMed
Counsell, S.J., Edwards, A.D., Chew, A.T.M., Anjari, M., Dyet, L.E., Srinivasan, L., Cowan, F.M.C. (2008). Specific relations between neurodevelopmental abilities and white matter microstructure in children born preterm. Brain, 131(12), 3201–3208.CrossRefGoogle ScholarPubMed
Curtis, W.J., Zhuang, J., Townsend, E.L., Hu, X., Nelson, C.A. (2006). Memory in early adolescents born prematurely: A functional magnetic resonance imaging investigation. Developmental Neuropsychology, 29(2), 341–377.Google Scholar
Delobel-Ayoub, M., Arnaud, C., White-Koning, M., Casper, C., Pierrat, V., Garel, M., Larroque, B. (2009). Behavioral problems and cognitive performance at 5 years of age after very preterm birth: The EPIPAGE study. Pediatrics, 123(6), 1485–1492.Google Scholar
Edgin, J.O., Inder, T.E., Anderson, P.J., Hood, K.M., Clark, C.A.C., Woodward, L.J. (2008). Executive functioning in preschool children born very preterm: Relationship with early white matter pathology. Journal of the International Neuropsychological Society, 14(1), 90–101.CrossRefGoogle ScholarPubMed
Espy, K.A., Stalets, M.M., McDiarmid, M.M., Senn, T.E., Cwik, M.F., Hamby, A. (2002). Executive functions in preschool children born preterm: Application of cognitive neuroscience paradigms. Child Neuropsychology, 8(2), 83–92.CrossRefGoogle ScholarPubMed
Friedman, N.P., Haberstick, B.C., Willcutt, E.G., Miyake, A., Young, S.E., Corley, R.P., Hewitt, J.K. (2007). Greater attention problems during childhood predict poorer executive functioning in late adolescence. Psychological Science, 18(10), 893–900.CrossRefGoogle ScholarPubMed
Garon, N., Bryson, S.E., Smith, I.M. (2008). Executive function in preschoolers: A review using an integrative framework. Psychological Bulletin, 134(1), 31–60.Google Scholar
Gathercole, S.E., Alloway, T.P., Kirkwood, H.J., Elliott, J.G., Holmes, J., Hilton, K.A. (2008). Attentional and executive function behaviours in children with poor working memory. Learning and Individual Differences, 18(2), 214–223.Google Scholar
Gathercole, S.E., Pickering, S.J., Knight, C., Stegmann, Z. (2004). Working memory skills and educational attainment: Evidence from national curriculum assessments at 7 and 14 years of age. Applied Cognitive Psychology, 18(1), 1–16.Google Scholar
Goyen, T.A., Lui, K., Woods, R. (1998). Visual-motor, visual-perceptual, and fine motor outcomes in very-low-birthweight children at 5 years. Developmental Medicine & Child Neurology, 40(2), 76–81.CrossRefGoogle ScholarPubMed
Hart, A.R., Whitby, E.W., Griffiths, P.D., Smith, M.F. (2008). Magnetic resonance imaging and developmental outcome following preterm birth: Review of current evidence. Developmental Medicine & Child Neurology, 50(9), 655–663.Google Scholar
Huddy, C.L., Johnson, A., Hope, P.L. (2001). Educational and behavioural problems in babies of 32–35 weeks gestation. Archives of Disease in Childhood Fetal & Neonatal Edition, 85(1), F23–F28.CrossRefGoogle ScholarPubMed
Huizinga, M., Dolan, C.V., van der Molen, M.W. (2006). Age-related change in executive function: Developmental trends and a latent variable analysis. Neuropsychologia, 44(11), 2017–2036.CrossRefGoogle Scholar
Huppi, P.S., Maier, S.E., Peled, S., Zientara, G.P., Barnes, P.D., Jolesz, F.A., Volpe, J.J. (1998). Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatric Research, 44(4), 584–590.Google Scholar
Johnson, S. (2007). Cognitive and behavioural outcomes following very preterm birth. Seminars in Fetal & Neonatal Medicine, 12(5), 363–373.Google Scholar
Johnson, S., Hennessy, E., Smith, R., Trikic, R., Wolke, D., Marlow, N. (2009). Academic attainment and special educational needs in extremely preterm children at 11 years of age: The EPICure Study. Archives of Disease in Childhood Fetal & Neonatal Edition, 94(4), F283–F289.CrossRefGoogle ScholarPubMed
Korkman, M., Kirk, U., Kemp, S. (1998). NEPSY: A developmental neuropsychological assessment. San Antonio, TX: Psychological Corporation.Google Scholar
Kulseng, S., Jennekens-Schinkel, A., Naess, P., Romundstad, P., Indredavik, M., Vik, T., Brubakk, A.M. (2006). Very-lowbirthweight and term small-for-gestational-age adolescents: Attention revisited. Acta Paediatrica, 95(2), 224–230.CrossRefGoogle ScholarPubMed
Lawrence, E.J., Rubia, K., Murray, R.M., McGuire, P.K., Walshe, M., Allin, M., Nosarti, C. (2009). The neural basis of response inhibition and attention allocation as mediated by gestational age. Human Brain Mapping, 30(3), 1038–1050.CrossRefGoogle ScholarPubMed
Lehto, J.E., Juujarvi, P., Kooistra, L., Pulkkinen, L. (2003). Dimensions of executive functioning: Evidence from children. British Journal of Developmental Psychology, 21(1), 59–80.CrossRefGoogle Scholar
Lezak, M.D. (1982). The problem of assessing executive functions. International Journal of Psychology, 17(1), 281–297.CrossRefGoogle Scholar
Luria, A.R. (1966). Higher cortical functions in man. NY: Basic Books.Google Scholar
Manly, T., Robertson, I.H., Anderson, V., Nimmo-Smith, I. (1999). Test of Everyday Attention for Children (TEA-Ch). London: Harcourt Assessment.Google Scholar
Marlow, N., Hennessy, E.M., Bracewell, M.A., Wolke, D. (2007). Motor and executive function at 6 years of age after extremely preterm birth. Pediatrics, 120(4), 793–804.Google Scholar
Miyake, A., Friedman, N.P., Emerson, M.J., Witzki, A.H., Howerter, A., Wager, T.D. (2000). The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: A latent variable analysis. Cognitive Psychology, 41(1), 49–100.CrossRefGoogle ScholarPubMed
Mulder, H., Pitchford, N.J., Hagger, M.S., Marlow, N. (2009). Development of executive function and attention in preterm children: A systematic review. Developmental Neuropsychology, 34(4), 393–421.Google Scholar
Mulder, H., Pitchford, N.J., Marlow, N. (2010). Processing speed and working memory underlie academic attainment in very preterm children. Archives of Disease in Childhood Fetal & Neonatal Edition, 95(4), F267–F272.Google Scholar
Mulder, H., Pitchford, N.J., Marlow, N. (2011). Inattentive behaviour is associated with poor working memory and slow processing speed in very pre-term children in middle childhood. British Journal of Educational Psychology, 81(1), 147–160.CrossRefGoogle ScholarPubMed
Nosarti, C., Giouroukou, E., Healy, E., Rifkin, L., Walshe, M., Reichenberg, A., Murray, R.M. (2008). Grey and white matter distribution in very preterm adolescents mediates neurodevelopmental outcome. Brain, 131(1), 205–217.Google Scholar
Nosarti, C., Giouroukou, E., Micali, N., Rifkin, L., Morris, R.G., Murray, R.M. (2007). Impaired executive functioning in young adults born very preterm. Journal of the International Neuropsychological Society, 13(4), 571–581.CrossRefGoogle ScholarPubMed
Nosarti, C., Rubia, K., Smith, A.B., Frearson, S., Williams, S.C., Rifkin, L., Murray, R.M. (2006). Altered functional neuroanatomy of response inhibition in adolescent males who were born very preterm. Developmental Medicine & Child Neurology, 48(4), 265–271.CrossRefGoogle ScholarPubMed
Peterson, B.S. (2003). Brain imaging studies of the anatomical and functional consequences of preterm birth for human brain development. Annals of the New York Academy of Sciences, 1008, 219–237.Google Scholar
Peterson, B.S., Vohr, B., Kane, M.J., Whalen, D.H., Schneider, K.C., Katz, K.H., Ment, R.M. (2002). A functional magnetic resonance imaging study of language processing and its cognitive correlates in prematurely born children. Pediatrics, 110(6), 1153–1162.CrossRefGoogle ScholarPubMed
Peterson, B.S., Vohr, B., Staib, L.H., Cannistraci, C.J., Dolberg, A., Schneider, K.C., Ment, R.M. (2000). Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. Journal of the American Medical Association, 284(15), 1939–1947.Google Scholar
Pizzo, R., Urben, S., van der Linden, M., Borradori-Tolsa, C., Freschi, M., Forcada-Guex, M., Barisnikov, K. (2010). Attentional networks efficiency in preterm children. Journal of the International Neuropsychological Society, 16(1), 130–137.CrossRefGoogle ScholarPubMed
Posner, M.I., Petersen, S.E. (1990). The attention system of the human brain. Annual Review of Neuroscience, 13, 25–42.CrossRefGoogle ScholarPubMed
Preacher, K.J., Hayes, A.F. (2004). SPSS and SAS procedures for estimating indirect effects in simple mediation models. Behavior Research Methods, Instruments & Computers, 36(4), 717–731.Google Scholar
Raz, A., Buhle, J. (2006). Typologies of attentional networks. Nature Reviews Neuroscience, 7(5), 367–379.Google Scholar
Romine, C.B., Reynolds, C.R. (2005). Model of the development of frontal lobe functioning: Findings from a meta-analysis. Applied Neuropsychology, 12(4), 190–201.Google Scholar
Rose, S.A., Feldman, J.F. (1995). Prediction of IQ and specific cognitive abilities at 11 years from infancy measures. Developmental Psychology, 31(4), 685–696.Google Scholar
Rose, S.A., Feldman, J.F. (1996). Memory and processing speed in preterm children at eleven years: A comparison with full-terms. Child Development, 67(5), 2005–2021.Google Scholar
Rose, S.A., Feldman, J.F., Jankowski, J.J. (2009). Information processing in toddlers: Continuity from infancy and persistence of preterm deficits. Intelligence, 37(3), 311–320.CrossRefGoogle ScholarPubMed
Rose, S.A., Feldman, J.F., Jankowski, J.J., van Rossem, R. (2005). Pathways from prematurity and infant abilities to later cognition. Child Development, 76(6), 1172–1184.Google Scholar
Rose, S.A., Feldman, J.F., Jankowski, J.J., van Rossem, R. (2008). A cognitive cascade in infancy: Pathways from prematurity to later mental development. Intelligence, 36(4), 367–378.CrossRefGoogle ScholarPubMed
Skranes, J., Vangberg, T.R., Kulseng, S., Indredavik, M.S., Evensen, K.A.I., Martinussen, M., Brubakk, A.M. (2007). Clincal findings and white matter abnormalities seen on diffusion tensor imaging in adolescents with very low birth weight. Brain, 130(3), 654–666.Google Scholar
Snyder, E.H., Davis, D.W., Burns, B.M., Robinson, J.B. (2007). Examining attention networks in preschool children born with very low birth weights. Journal of Early Childhood and Infant Psychology, 3, 185–203.Google Scholar
Soria-Pastor, S., Gimenez, M., Narberhaus, A., Falcon, C., Botet, F., Bargallo, N., Junque, C. (2008). Patterns of cerebral white matter damage and cognitive impairment in adolescents born very preterm. International Journal of Developmental Neuroscience, 26, 647–654.Google Scholar
St Clair-Thompson, H.L., Gathercole, S.E. (2006). Executive functions and achievements in school: Shifting, updating, inhibition, and working memory. The Quarterly Journal of Experimental Psychology, 59(4), 745–759.Google Scholar
Taylor, H.G., Minich, N.M., Klein, N., Hack, M. (2004). Longitudinal outcomes of very low birth weight: Neuropsychological findings. Journal of the International Neuropsychological Society, 10(2), 149–163.Google Scholar
Van de Weijer-Bergsma, E., Wijnroks, L., Jongmans, M.J. (2008). Attention development in infants and preschool children born preterm: A review. Infant Behavior and Development, 31(3), 333–351.Google Scholar
Vangberg, T.R., Skranes, J., Dale, A.M., Martinussen, M., Brubakk, A.-M., Haraldseth, O. (2006). Changes in white matter diffusion anisotropy in adolescents born prematurely. Neuroimage, 32(4), 1538–1548.CrossRefGoogle ScholarPubMed
Wechsler, D. (2004). Wechsler intelligence scale for children - Fourth UK edition. London: Harcourt Assessment.Google Scholar
Welsh, M.C., Pennington, B.F., Groisser, D.B. (1991). A normative-developmental study of executive function - A window on prefrontal function in children. Developmental Neuropsychology, 7(2), 131–149.CrossRefGoogle Scholar
Wolke, D., Samara, M., Bracewell, M., Marlow, N., & EPICure Study Group (2008). Specific language difficulties and school achievement in children born at 25 weeks of gestation or less. Journal of Pediatrics, 152(2), 256–262.CrossRefGoogle ScholarPubMed
Wolke, D., Waylen, A., Samara, M., Steer, C., Goodman, R., Ford, T., Lamberts, K. (2009). Selective drop-out in longitudinal studies and non-biased prediction of behaviour disorders. British Journal of Psychiatry, 195(3), 249–256.Google Scholar
Yung, A., Poon, G., Qiu, D.-Q., Chu, J., Lam, B., Leung, C., Khong, P.L. (2007). White matter volume and anisotropy in preterm children: A pilot study of neurocognitive correlates. Pediatric Research, 61(6), 732–736.Google Scholar