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Research Article

Long-term influence of normal variation in neonatal characteristics on human brain development

Kristine B. Walhovd, Anders M. Fjell, Timothy T. Brown, Joshua M. Kuperman, Yoonho Chung, Donald J. Hagler Jr, J. Cooper Roddey, Matthew Erhart, Connor McCabe, Natacha Akshoomoff, David G. Amaral, Cinnamon S. Bloss, Ondrej Libiger, Nicholas J. Schork, Burcu F. Darst, B. J. Casey, Linda Chang, Thomas M. Ernst, Jean Frazier, Jeffrey R. Gruen, Walter E. Kaufmann, Sarah S. Murray, Peter van Zijl, Stewart Mostofsky, Anders M. Dale, and for the Pediatric Imaging, Neurocognition,, and Genetics Study
  1. aDepartment of Psychology, University of Oslo, 0373 Oslo, Norway;
  2. bMultimodal Imaging Laboratory,
  3. Departments of cNeurosciences,
  4. dRadiology,
  5. fPsychiatry, and
  6. pCognitive Science, and
  7. eCenter for Human Development, University of California at San Diego, La Jolla, CA 92037;
  8. gDepartment of Psychiatry and Behavioral Sciences, University of California, Davis, CA 95817;
  9. hScripps Genomic Medicine, Scripps Translational Science Institute and Scripps Health, La Jolla, CA 92037;
  10. iSackler Institute for Developmental Psychobiology, Weil Cornell Medical College, New York, NY 10065;
  11. jDepartment of Medicine, University of Hawaii and Queen's Medical Center, Honolulu, HI 96813;
  12. kDepartment of Psychiatry, University of Massachusetts Medical School, Boston, MA 01655;
  13. lDepartments of Pediatrics and Genetics, Yale University School of Medicine, New Haven, CT 06520;
  14. mKennedy Krieger Institute and
  15. oF. M. Kirby Research Center, Kennedy Krieger Institute and Department of Radiology, Johns Hopkins University School of Medicine, Baltimore, MD 21205; and
  16. nChildren's Hospital Boston, Harvard Medical School, Boston, MA 02115

              See allHide authors and affiliations

              PNAS first published November 19, 2012; https://doi.org/10.1073/pnas.1208180109
              Kristine B. Walhovd
              aDepartment of Psychology, University of Oslo, 0373 Oslo, Norway;
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              • For correspondence: k.b.walhovd@psykologi.uio.no
              Anders M. Fjell
              aDepartment of Psychology, University of Oslo, 0373 Oslo, Norway;
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              Timothy T. Brown
              bMultimodal Imaging Laboratory,
              Departments of cNeurosciences,
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              Joshua M. Kuperman
              bMultimodal Imaging Laboratory,
              dRadiology,
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              Yoonho Chung
              bMultimodal Imaging Laboratory,
              eCenter for Human Development, University of California at San Diego, La Jolla, CA 92037;
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              Donald J. Hagler Jr
              bMultimodal Imaging Laboratory,
              dRadiology,
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              J. Cooper Roddey
              bMultimodal Imaging Laboratory,
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              Matthew Erhart
              bMultimodal Imaging Laboratory,
              dRadiology,
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              Connor McCabe
              eCenter for Human Development, University of California at San Diego, La Jolla, CA 92037;
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              Natacha Akshoomoff
              eCenter for Human Development, University of California at San Diego, La Jolla, CA 92037;
              fPsychiatry, and
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              David G. Amaral
              gDepartment of Psychiatry and Behavioral Sciences, University of California, Davis, CA 95817;
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              Cinnamon S. Bloss
              hScripps Genomic Medicine, Scripps Translational Science Institute and Scripps Health, La Jolla, CA 92037;
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              Ondrej Libiger
              hScripps Genomic Medicine, Scripps Translational Science Institute and Scripps Health, La Jolla, CA 92037;
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              Nicholas J. Schork
              hScripps Genomic Medicine, Scripps Translational Science Institute and Scripps Health, La Jolla, CA 92037;
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              Burcu F. Darst
              hScripps Genomic Medicine, Scripps Translational Science Institute and Scripps Health, La Jolla, CA 92037;
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              B. J. Casey
              iSackler Institute for Developmental Psychobiology, Weil Cornell Medical College, New York, NY 10065;
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              Linda Chang
              jDepartment of Medicine, University of Hawaii and Queen's Medical Center, Honolulu, HI 96813;
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              Thomas M. Ernst
              jDepartment of Medicine, University of Hawaii and Queen's Medical Center, Honolulu, HI 96813;
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              Jean Frazier
              kDepartment of Psychiatry, University of Massachusetts Medical School, Boston, MA 01655;
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              Jeffrey R. Gruen
              lDepartments of Pediatrics and Genetics, Yale University School of Medicine, New Haven, CT 06520;
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              Walter E. Kaufmann
              mKennedy Krieger Institute and
              nChildren's Hospital Boston, Harvard Medical School, Boston, MA 02115
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              Sarah S. Murray
              hScripps Genomic Medicine, Scripps Translational Science Institute and Scripps Health, La Jolla, CA 92037;
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              Peter van Zijl
              oF. M. Kirby Research Center, Kennedy Krieger Institute and Department of Radiology, Johns Hopkins University School of Medicine, Baltimore, MD 21205; and
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              Stewart Mostofsky
              mKennedy Krieger Institute and
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              Anders M. Dale
              bMultimodal Imaging Laboratory,
              Departments of cNeurosciences,
              dRadiology,
              fPsychiatry, and
              pCognitive Science, and
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              1. Edited by Marcus E. Raichle, Washington University, St. Louis, MO, and approved October 2, 2012 (received for review May 16, 2012)

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              Abstract

              It is now recognized that a number of cognitive, behavioral, and mental health outcomes across the lifespan can be traced to fetal development. Although the direct mediation is unknown, the substantial variance in fetal growth, most commonly indexed by birth weight, may affect lifespan brain development. We investigated effects of normal variance in birth weight on MRI-derived measures of brain development in 628 healthy children, adolescents, and young adults in the large-scale multicenter Pediatric Imaging, Neurocognition, and Genetics study. This heterogeneous sample was recruited through geographically dispersed sites in the United States. The influence of birth weight on cortical thickness, surface area, and striatal and total brain volumes was investigated, controlling for variance in age, sex, household income, and genetic ancestry factors. Birth weight was found to exert robust positive effects on regional cortical surface area in multiple regions as well as total brain and caudate volumes. These effects were continuous across birth weight ranges and ages and were not confined to subsets of the sample. The findings show that (i) aspects of later child and adolescent brain development are influenced at birth and (ii) relatively small differences in birth weight across groups and conditions typically compared in neuropsychiatric research (e.g., Attention Deficit Hyperactivity Disorder, schizophrenia, and personality disorders) may influence group differences observed in brain parameters of interest at a later stage in life. These findings should serve to increase our attention to early influences.

              • neurodevelopmental
              • anterior cingulate
              • cortical area
              • magnetic resonance imaging

              Footnotes

              • ↵1To whom correspondence should be addressed. E-mail: k.b.walhovd{at}psykologi.uio.no.
              • ↵2Data used in preparation of this study were obtained from the Pediatric Imaging, Neurocognition, and Genetics Study (PING) database. As such, the investigators within PING contributed to the design and implementation of PING and/or provided data but did not participate in the analysis or writing of this report. A complete listing of PING investigators can be found in the Supporting Information.

              • Author contributions: K.B.W., A.M.F., T.T.B., N.A., D.G.A., C.S.B., N.J.S., B.J.C., L.C., T.M.E., J.F., J.R.G., W.E.K., S.S.M., P.Z., S.M., and A.M.D. designed research; K.B.W., A.M.F, T.T.B., C.M., N.A., D.G.A., C.S.B., N.J.S., B.F.D., B.J.C., L.C., T.M.E., J.F., J.R.G., W.E.K., S.S.M., P.Z., S.M., and A.M.D. performed research; P.I.N.G. contributed new reagents/analytic tools; K.B.W., A.M.F., J.M.K., Y.C., D.J.H., J.C.R., M.E., O.L., and A.M.D. analyzed data; K.B.W. and A.M.F. wrote the paper; and P.I.N.G. provided phenotype and genotype data.

              • Conflict of interest statement: A.M.D. is a founder of and holds equity interest in CorTechs Labs, La Jolla, CA and serves on its scientific advisory board. The terms of this arrangement have been reviewed and approved by the University of California at San Diego, in accordance with its conflict of interest policies.

              • This article is a PNAS Direct Submission.

              • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1208180109/-/DCSupplemental.

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              Birth weight and brain development
              Kristine B. Walhovd, Anders M. Fjell, Timothy T. Brown, Joshua M. Kuperman, Yoonho Chung, Donald J. Hagler, J. Cooper Roddey, Matthew Erhart, Connor McCabe, Natacha Akshoomoff, David G. Amaral, Cinnamon S. Bloss, Ondrej Libiger, Nicholas J. Schork, Burcu F. Darst, B. J. Casey, Linda Chang, Thomas M. Ernst, Jean Frazier, Jeffrey R. Gruen, Walter E. Kaufmann, Sarah S. Murray, Peter van Zijl, Stewart Mostofsky, Anders M. Dale, for the Pediatric Imaging, Neurocognition, and Genetics Study
              Proceedings of the National Academy of Sciences Nov 2012, 201208180; DOI: 10.1073/pnas.1208180109

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              Birth weight and brain development
              Kristine B. Walhovd, Anders M. Fjell, Timothy T. Brown, Joshua M. Kuperman, Yoonho Chung, Donald J. Hagler, J. Cooper Roddey, Matthew Erhart, Connor McCabe, Natacha Akshoomoff, David G. Amaral, Cinnamon S. Bloss, Ondrej Libiger, Nicholas J. Schork, Burcu F. Darst, B. J. Casey, Linda Chang, Thomas M. Ernst, Jean Frazier, Jeffrey R. Gruen, Walter E. Kaufmann, Sarah S. Murray, Peter van Zijl, Stewart Mostofsky, Anders M. Dale, for the Pediatric Imaging, Neurocognition, and Genetics Study
              Proceedings of the National Academy of Sciences Nov 2012, 201208180; DOI: 10.1073/pnas.1208180109
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