White Matter and Cognition in Adults Who Were Born Preterm

Background and Purpose Individuals born very preterm (before 33 weeks of gestation, VPT) are at risk of damage to developing white matter, which may affect later cognition and behaviour. Methods We used diffusion tensor MRI (DT-MRI) to assess white matter microstructure (fractional anisotropy; FA) in 80 VPT and 41 term-born individuals (mean age 19.1 years, range 17–22, and 18.5 years, range17–22 years, respectively). VPT individuals were part of a 1982–1984 birth cohort which had been followed up since birth; term individuals were recruited by local press advertisement. General intellectual function, executive function and memory were assessed. Results The VPT group had reduced FA in four clusters, and increased FA in four clusters relative to the Term group, involving several association tracts of both hemispheres. Clusters of increased FA were associated with more severe neonatal brain injury in the VPT group. Clusters of reduced FA were associated with lower birth weight and perinatal hypoxia, and with reduced adult cognitive performance in the VPT group only. Conclusions Alterations of white matter microstructure persist into adulthood in VPT individuals and are associated with cognitive function.

[1]  M A Rutherford,et al.  Magnetic resonance imaging of the brain in a cohort of extremely preterm infants. , 1999, The Journal of pediatrics.

[2]  Tomoki Arichi,et al.  Diffusion Tensor Imaging in Preterm Infants With Punctate White Matter Lesions , 2011, Pediatric Research.

[3]  Derek K. Jones,et al.  Isotropic resolution diffusion tensor imaging with whole brain acquisition in a clinically acceptable time , 2002, Human brain mapping.

[4]  M. Hack.  Young adult outcomes of very-low-birth-weight children. , 2006, Seminars in fetal & neonatal medicine.

[5]  Michelle Hampson,et al.  Functional connectivity to a right hemisphere language center in prematurely born adolescents , 2010, NeuroImage.

[6]  Michelle Hampson,et al.  Microstructural and functional connectivity in the developing preterm brain. , 2011, Seminars in perinatology.

[7]  Chiara Nosarti,et al.  Neural substrates of letter fluency processing in young adults who were born very preterm: Alterations in frontal and striatal regions , 2009, NeuroImage.

[8]  P. Basser,et al.  Estimation of the effective self-diffusion tensor from the NMR spin echo. , 1994, Journal of magnetic resonance. Series B.

[9]  Michelle Hampson,et al.  Preterm birth results in alterations in neural connectivity at age 16 years , 2011, NeuroImage.

[10]  Derek K. Jones,et al.  Age effects on diffusion tensor magnetic resonance imaging tractography measures of frontal cortex connections in schizophrenia , 2006, Human brain mapping.

[11]  J. Wyatt,et al.  PROBABILITÉ OF NEURODEVELOPMENTAL DISORDERS ESTIMATED FROM ULTRASOUND APPEARANCE OF BRAINS OF VERY PRETERM INFANTS , 1987, Developmental medicine and child neurology.

[12]  R. Edelman,et al.  Clinical magnetic resonance imaging , 1990 .

[13]  Derek K. Jones,et al.  Spatial Normalization and Averaging of Diffusion Tensor MRI Data Sets , 2002, NeuroImage.

[14]  H. Forssberg,et al.  Preterm Children Have Disturbances of White Matter at 11 Years of Age as Shown by Diffusion Tensor Imaging , 2003, Pediatric Research.

[15]  R. Kikinis,et al.  Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. , 2001, Pediatrics.

[16]  M. Moseley,et al.  Diffusion tensor brain imaging findings at term-equivalent age may predict neurologic abnormalities in low birth weight preterm infants. , 2003, AJNR. American journal of neuroradiology.

[17]  M. Kraut,et al.  Diffusion tensor MR imaging of the brain and white matter tractography. , 2002, AJR. American journal of roentgenology.

[18]  H. Harrison.  Outcomes in young adulthood for very-low-birth-weight infants. , 2002, The New England journal of medicine.

[19]  V. Schmithorst,et al.  Cognitive functions correlate with white matter architecture in a normal pediatric population: A diffusion tensor MRI study , 2005, Human brain mapping.

[20]  G. Molenaers,et al.  Quantitative diffusion tensor imaging in cerebral palsy due to periventricular white matter injury. , 2005, Brain : a journal of neurology.

[21]  P. Basser,et al.  Diffusion tensor MR imaging of the human brain. , 1996, Radiology.

[22]  Michael I. Miller,et al.  Multi-contrast human neonatal brain atlas: Application to normal neonate development analysis , 2011, NeuroImage.

[23]  Anders M. Dale,et al.  Changes in white matter diffusion anisotropy in adolescents born prematurely , 2006, NeuroImage.

[24]  Karl J. Friston,et al.  A Voxel-Based Morphometric Study of Ageing in 465 Normal Adult Human Brains , 2001, NeuroImage.

[25]  Gro C. Christensen Løhaugen,et al.  Young adults born preterm with very low birth weight demonstrate widespread white matter alterations on brain DTI , 2011, NeuroImage.

[26]  Deanne K. Thompson,et al.  Abnormal White Matter Signal on MR Imaging Is Related to Abnormal Tissue Microstructure , 2009, American Journal of Neuroradiology.

[27]  J. Volpe.  Cerebral white matter injury of the premature infant-more common than you think. , 2003, Pediatrics.

[28]  John Suckling,et al.  Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain , 1999, IEEE Transactions on Medical Imaging.

[29]  Chiara Nosarti,et al.  Adolescents who were born very preterm have decreased brain volumes. , 2002, Brain : a journal of neurology.

[30]  Maxwell P. Henderson,et al.  Effects of very low birthweight on brain structure in adulthood. , 2004, Developmental medicine and child neurology.

[31]  Christopher J. Cannistraci,et al.  Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. , 2000, JAMA.

[32]  Chiara Nosarti,et al.  Cerebellar growth and behavioural & neuropsychological outcome in preterm adolescents. , 2008, Brain : a journal of neurology.

[33]  Robin M. Murray,et al.  The Maudsley Family Study 4. Normal planum temporale asymmetry in familial schizophrenia , 1997, British Journal of Psychiatry.

[34]  Alan C. Evans,et al.  Brain development during childhood and adolescence: a longitudinal MRI study , 1999, Nature Neuroscience.

[35]  David Wechsler,et al.  Wechsler Memory scale. , 2005 .

[36]  D. Larkman,et al.  Axial and Radial Diffusivity in Preterm Infants Who Have Diffuse White Matter Changes on Magnetic Resonance Imaging at Term-Equivalent Age , 2006, Pediatrics.

[37]  A. Dale,et al.  Clinical findings and white matter abnormalities seen on diffusion tensor imaging in adolescents with very low birth weight. , 2007, Brain : a journal of neurology.

[38]  J. Perlman,et al.  White matter injury in the preterm infant: an important determination of abnormal neurodevelopment outcome. , 1998, Early human development.

[39]  Steven P. Miller,et al.  Serial quantitative diffusion tensor MRI of the premature brain: Development in newborns with and without injury , 2002, Journal of magnetic resonance imaging : JMRI.

[40]  Stefan Skare,et al.  Structural Correlates of Preterm Birth in the Adolescent Brain , 2009, Pediatrics.

[41]  Mark H. Johnson,et al.  Mapping Infant Brain Myelination with Magnetic Resonance Imaging , 2011, The Journal of Neuroscience.

[42]  P. Basser,et al.  Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. 1996. , 1996, Journal of magnetic resonance.

[43]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[44]  Chiara Nosarti,et al.  Corpus callosum size and very preterm birth: relationship to neuropsychological outcome. , 2004, Brain : a journal of neurology.

[45]  Derek K. Jones,et al.  Virtual in Vivo Interactive Dissection of White Matter Fasciculi in the Human Brain , 2002, NeuroImage.

[46]  P. Khong,et al.  White Matter Volume and Anisotropy in Preterm Children: A Pilot Study of Neurocognitive Correlates , 2007, Pediatric Research.

[47]  V. Menon,et al.  White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study. , 2005, Cerebral cortex.

[48]  Christian Beaulieu,et al.  Diffusion tensor imaging of neurodevelopment in children and young adults , 2005, NeuroImage.

[49]  H. Kinney,et al.  Oxidative and Nitrative Injury in Periventricular Leukomalacia: A Review , 2005, Brain pathology.

[50]  Chiara Nosarti,et al.  Growth of the corpus callosum in adolescents born preterm. , 2007, Archives of pediatrics & adolescent medicine.

[51]  B. Vohr,et al.  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 , 2008, Pediatrics.

[52]  Núria Bargalló,et al.  White matter volume and concentration reductions in adolescents with history of very preterm birth: A voxel-based morphometry study , 2006, NeuroImage.

[53]  Karl J. Friston,et al.  A Voxel-Based Method for the Statistical Analysis of Gray and White Matter Density Applied to Schizophrenia , 1995, NeuroImage.

[54]  Chiara Nosarti,et al.  Neural substrates of visual paired associates in young adults with a history of very preterm birth: Alterations in fronto-parieto-occipital networks and caudate nucleus , 2009, NeuroImage.

[55]  Paul W. Burgess,et al.  Theory and methodology in executive function research , 1997 .

[56]  D. Holtzman,et al.  Selective Vulnerability of Late Oligodendrocyte Progenitors to Hypoxia–Ischemia , 2002, The Journal of Neuroscience.

[57]  M. Catani,et al.  The rises and falls of disconnection syndromes. , 2005, Brain : a journal of neurology.

[58]  Chiara Nosarti,et al.  Impaired executive functioning in young adults born very preterm , 2007, Journal of the International Neuropsychological Society.

[59]  Derek K. Jones,et al.  Diffusion tensor MRI of the corpus callosum and cognitive function in adults born preterm , 2009, Neuroreport.

[60]  E. Kaplan,et al.  Integrating clinical assessment with cognitive neuroscience: construct validation of the California Verbal Learning Test. , 1988, Journal of consulting and clinical psychology.

[61]  Dyz,et al.  DIFFUSION-TENSOR MR IMAGING FUNDAMENTALS , 2005 .

[62]  M. Mapstone.  Neuropsychological Assessment, 4th Edition , 2005, Neurology.

[63]  Ke Zhou,et al.  Diffusion tensor imaging of normal white matter maturation from late childhood to young adulthood: Voxel-wise evaluation of mean diffusivity, fractional anisotropy, radial and axial diffusivities, and correlation with reading development , 2008, NeuroImage.

[64]  B. Luna,et al.  Reading performance correlates with white‐matter properties in preterm and term children , 2010, Developmental medicine and child neurology.

[65]  P. Szeszko,et al.  MRI atlas of human white matter , 2006 .

[66]  R. Sternberg,et al.  Intelligence: Knowns and unknowns. , 1996 .

[67]  P. Rabbitt,et al.  Methodology of Frontal and Executive Function , 1999 .

[68]  Roland G. Henry,et al.  Diffusion tensor imaging: serial quantitation of white matter tract maturity in premature newborns , 2004, NeuroImage.

[69]  Chiara Nosarti,et al.  Grey and white matter distribution in very preterm adolescents mediates neurodevelopmental outcome. , 2008, Brain : a journal of neurology.

[70]  R. Murray,et al.  The very preterm brain in young adulthood: the neural correlates of verbal paired associate learning. , 2010, The Journal of pediatrics.

[71]  Paul D Griffiths,et al.  Magnetic resonance imaging and developmental outcome following preterm birth: review of current evidence , 2008, Developmental medicine and child neurology.

[72]  Paul M. Thompson,et al.  The link between callosal thickness and intelligence in healthy children and adolescents , 2011, NeuroImage.

[73]  D. Miller,et al.  Brain structure and neurocognitive and behavioural function in adolescents who were born very preterm , 1999, The Lancet.

[74]  S. Wakana,et al.  MRI Atlas of Human White Matter , 2005 .