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Research ArticlePediatric Neuroimaging
Open Access

Aberrant Structural Brain Connectivity in Adolescents with Attentional Problems Who Were Born Prematurely

O. Tymofiyeva, D. Gano, R.J. Trevino, H.C. Glass, T. Flynn, S.M. Lundy, P.S. McQuillen, D.M. Ferriero, A.J. Barkovich and D. Xu
American Journal of Neuroradiology October 2018, DOI: https://doi.org/10.3174/ajnr.A5834
O. Tymofiyeva
aFrom the Departments of Radiology & Biomedical Imaging (O.T., R.J.T., T.F., A.J.B., D.X.)
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D. Gano
bNeurology (D.G., H.C.G., D.M.F.)
cPediatrics (D.G., H.C.G., S.M.L., P.S.M., D.M.F.), University of California, San Francisco, San Francisco. California.
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R.J. Trevino Jr
aFrom the Departments of Radiology & Biomedical Imaging (O.T., R.J.T., T.F., A.J.B., D.X.)
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H.C. Glass
bNeurology (D.G., H.C.G., D.M.F.)
cPediatrics (D.G., H.C.G., S.M.L., P.S.M., D.M.F.), University of California, San Francisco, San Francisco. California.
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T. Flynn
aFrom the Departments of Radiology & Biomedical Imaging (O.T., R.J.T., T.F., A.J.B., D.X.)
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S.M. Lundy
cPediatrics (D.G., H.C.G., S.M.L., P.S.M., D.M.F.), University of California, San Francisco, San Francisco. California.
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P.S. McQuillen
cPediatrics (D.G., H.C.G., S.M.L., P.S.M., D.M.F.), University of California, San Francisco, San Francisco. California.
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D.M. Ferriero
bNeurology (D.G., H.C.G., D.M.F.)
cPediatrics (D.G., H.C.G., S.M.L., P.S.M., D.M.F.), University of California, San Francisco, San Francisco. California.
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A.J. Barkovich
aFrom the Departments of Radiology & Biomedical Imaging (O.T., R.J.T., T.F., A.J.B., D.X.)
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D. Xu
aFrom the Departments of Radiology & Biomedical Imaging (O.T., R.J.T., T.F., A.J.B., D.X.)
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Abstract

BACKGROUND AND PURPOSE: Differences in structural brain connectivity that underlie inattention have been previously investigated in adolescents with attention deficit/hyperactivity disorder, but not in the context of premature birth, which is often associated with attentional problems. The purpose of this study was to identify the neural correlates of attentional problems in adolescents born prematurely and determine neonatal predictors of those neural correlates and attention problems.

MATERIALS AND METHODS: The study included 24 adolescents (12.5 ± 1.8 years of age; 12 girls, 12 boys) who were born prematurely and underwent MR imaging of the brain and cognitive assessment, both shortly after birth and as adolescents. Structural connectivity was assessed at adolescence using diffusion tensor imaging and tractography.

RESULTS: Of the 24 subjects, 12 had attention deficits. A set of axonal pathways connecting the frontal, parietal, temporal, and occipital lobes had significantly lower fractional anisotropy in subjects with attentional problems. The temporoparietal connection between the left precuneus and left middle temporal gyrus was the most significantly underconnected interlobar axonal pathway. Low birth weight and ventriculomegaly, but not white matter injury or intraventricular hemorrhage on neonatal MR imaging, predicted temporoparietal hypoconnectivity in adolescence. However, neither birth weight nor other neonatal characteristics were associated with attention deficits directly.

CONCLUSIONS: We identified an aberrant structural brain connectivity pattern, involving temporoparietal hypoconnectivity, in prematurely born adolescents with attentional problems. We also identified birth weight as a potential neonatal predictor of the temporoparietal hypoconnectivity. These findings add to our understanding of the neural basis and etiology of inattention in adolescents after premature birth.

ABBREVIATIONS:

ADHD
attention deficit/hyperactivity disorder
AAL
Automated Anatomical Labeling
FA
fractional anisotropy
FDR
false discovery rate
TOVA
Test of Variables of Attention
WMI
white matter injury

Footnotes

  • Disclosures: Olga Tymofiyeva—RELATED: Grant: National Institutes of Health, Comments: National Institutes of Health grants P01NS082330, R01HD072074, and R21AT009173*; Support for Travel to Meetings for the Study or Other Purposes: National Institutes of Health, Comments: National Institutes of Health grants P01NS082330, R01HD072074, and R21AT009173*. Dawn Gano—RELATED: Grant: National Institutes of Health*; UNRELATED: Grants/Grants Pending: PERF*. Robert J. Trevino—UNRELATED: Other: Summer Research Training Program at the University of California, San Francisco; Maximizing Access to Research Careers—Undergraduate Student Training for Academic Research (MARC U-STAR), Comments: During my time at the University of California, San Francisco, I was in a living arrangement provided by the Summer Research Training Program at the University of California, San Francisco. I am also partly funded by the MARC U-STAR Program through National Institutes of Health/National Institute of General Medical Sciences MARC U-STAR GM07717. Hannah C. Glass—UNRELATED: medicolegal consulting: various Grants/Grants Pending: National Institutes of Health, Cerebral Palsy Alliance, Pediatric Epilepsy Research Foundation. Donna M. Ferriero—RELATED: Grant: National Institutes of Health*; UNRELATED: Grants/Grants Pending: National Institutes of Health, Cerebral Palsy Alliance*; Royalties: Elsevier for an edited book*. A. James Barkovich—RELATED: Grant: National Institutes of Health, Comments: grant to look at differences in brain injuries and brain structure in children born before 32 weeks' gestational age*. Duan Xu—RELATED: Grant: National Institutes of Health*; UNRELATED: Grants/Grants Pending: National Institutes of Health*. *Money paid to the institution.

  • This study was supported by P01NS082330 to D.M.F., P.S.M., D.X., and A.J.B.; NICHD R01HD072074 to D.X. and O.T.; NCCIH R21AT009173 to O.T.; and the University of California, San Francisco, Research Evaluation and Allocation Committee and the J. Jacobson Fund to O.T. and D.X.

  • The content of this article is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health or other funding agencies. The funding agencies did not play any role in study design or in the collection, analysis, and interpretation of data; in the writing of the report; and in the decision to submit the article for publication.

  • © 2018 by American Journal of Neuroradiology

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Cite this article
O. Tymofiyeva, D. Gano, R.J. Trevino, H.C. Glass, T. Flynn, S.M. Lundy, P.S. McQuillen, D.M. Ferriero, A.J. Barkovich, D. Xu
Aberrant Structural Brain Connectivity in Adolescents with Attentional Problems Who Were Born Prematurely
American Journal of Neuroradiology Oct 2018, DOI: 10.3174/ajnr.A5834

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Aberrant Structural Brain Connectivity in Adolescents with Attentional Problems Who Were Born Prematurely
O. Tymofiyeva, D. Gano, R.J. Trevino, H.C. Glass, T. Flynn, S.M. Lundy, P.S. McQuillen, D.M. Ferriero, A.J. Barkovich, D. Xu
American Journal of Neuroradiology Oct 2018, DOI: 10.3174/ajnr.A5834
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