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An allometric scaling relationship in the brain of preterm infants Rachel A. Paul1, Christopher D. Smyser2,3, Cynthia E. Rogers1,3, Ian English4, Michael Wallendorf5, Dimitrios Alexopoulos2, Erin J. Meyer6, David C. Van Essen7, Jeffrey J. Neil8 & Terrie E. Inder9 1

Department of Psychiatry, Washington University School of Medicine, St. Louis, Missouri Department of Neurology, Washington University School of Medicine, St. Louis, Missouri 3 Department of Pediatrics, Washington University School of Medicine, St. Louis, Missouri 4 Medical College of Wisconsin, Milwaukee, Wisconsin 5 Division of Biostatistics, Washington University School of Medicine, St. Louis, Missouri 6 Case Western Reserve Medical School, Cleveland, Ohio 7 Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 8 Department of Neurology, Boston Children’s Hospital, Boston, Massachusetts 9 Department of Pediatric Newborn Medicine, Brigham and Women’s Hospital, Boston, Massachusetts 2

Correspondence Terrie Inder, Department of Pediatric Newborn Medicine, Brigham and Women’s Hospital, 75 Francis St, Boston, MA 02215. Tel: (617) 552-6650; Fax: (617) 278-6983; E-mail: [email protected] Funding Information This study was supported by the National Institutes of Health (grant numbers R01 HD057098, UL1 TR000448, KL2 TR000250, R01MH60974, and K12 NS001690), the McDonnell Center for Systems Neuroscience, the Intellectual and Developmental Disabilities Research Center at Washington University (National Institutes of Health/NICHD P30 HD062171) and the Doris Duke Foundation.

Abstract Allometry has been used to demonstrate a power–law scaling relationship in the brain of premature born infants. Forty-nine preterm infants underwent neonatal MRI scans and neurodevelopmental testing at age 2 . Measures of cortical surface area and total cerebral volume demonstrated a power–law scaling relationship (a = 1.27). No associations were identified between these measures and investigated clinical variables. Term equivalent cortical surface area and total cerebral volume measures and scaling exponents were not related to outcome. These findings confirm a previously reported allometric scaling relationship in the preterm brain, and suggest that scaling is not a sensitive indicator of aberrant cortical maturation.

Received: 3 September 2014; Accepted: 5 September 2014 Annals of Clinical and Translational Neurology 2014; 1(11): 933–937 doi: 10.1002/acn3.130

Introduction Premature birth is associated with altered cerebral volumes, cortical surface area, and cortical folding at term equivalent postmenstrual age (PMA).1–4 One useful way to quantify these effects involves allometric analysis. In general, allometry assesses the degree to which the sizes and shapes of various body parts conform to isometric scaling relationships.5 By relating overall brain volume to surface area (and, indirectly, cortical volume), allometry has been used to investigate the evolutionary advantages

of having a gyrencephalic (highly folded) cerebral cortex over a lissencephalic one.6 It can also provide a quantitative method for examining the changing geometry of the developing brain. Allometric relationships can be expressed mathematically as CSA = b(TCV)a where CSA is cortical surface area, TCV is total cerebral volume, b is a scaling factor and a is a scaling exponent related to the relative growth rates of CSA and TCV. An a with values less than 2/3 signifies a differential increase of TCV relative to CSA (negative allometry), and a greater than 2/3 signifies a differential increase of CSA to TCV (positive

ª 2014 The Authors. Annals of Clinical and Translational Neurology published by Wiley Periodicals, Inc on behalf of American Neurological Association. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.

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Allometric Scaling in Preterm Infants’ Brains

allometry). In a study of 113 premature infants, Kapellou and colleagues demonstrated that the expansion of CSA occurs at a much faster rate than the expansion of the tissue volume in infants, with a scaling exponent of a = 1.29,7,8 consistent with the rapid gyrification during this period. The measured scaling exponent was lower in males and infants who were more premature at birth, and was shown to have a positive relationship with neurodevelopmental outcome at 2 years of age. Here, we reexamined these issues in 49 preterm infants scanned at higher spatial resolution and analyzed using improved cortical surface-based methods.

Methods Fifty-eight very preterm infants (born at

An allometric scaling relationship in the brain of preterm infants.

Allometry has been used to demonstrate a power-law scaling relationship in the brain of premature born infants. Forty-nine preterm infants underwent n...
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