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. 2017 Nov;222(8):3653-3663.
doi: 10.1007/s00429-017-1424-0. Epub 2017 Apr 17.

Healthy cortical development through adolescence and early adulthood

Natalie J Forde  1   2 , Lisa Ronan  3 , Marcel P Zwiers  4 , Lizanne J S Schweren  5   6 , Aaron F Alexander-Bloch  7 , Barbara Franke  8 , Stephen V Faraone  9   10 , Jaap Oosterlaan  11 , Dirk J Heslenfeld  11 , Catharina A Hartman  5 , Jan K Buitelaar  4   12 , Pieter J Hoekstra  5
Affiliations

Healthy cortical development through adolescence and early adulthood

Natalie J Forde et al. Brain Struct Funct. 2017 Nov.

Abstract

Adolescence is a period of significant brain changes; however, the effects of age and sex on cortical development are yet to be fully characterized. Here, we utilized innovative intrinsic curvature (IC) analysis, along with the traditional cortical measures [cortical thickness (CT), local gyrification index (LGI), and surface area (SA)], to investigate how these indices (1) relate to each other and (2) depend on age and sex in adolescent cortical development. T1-weighted magnetic resonance images from 218 healthy volunteers (age range 8.3-29.2 years, M[SD] = 16.5[3.4]) were collected at two sites and processed with FreeSurfer and Caret software packages. Surface indices were extracted per cortex area (frontal, parietal, occipital, temporal, insula, and cingulate). Correlation analyses between the surface indices were conducted and age curves were modelled using generalized additive mixed-effect models. IC showed region-specific associations with LGI, SA, and CT, as did CT with LGI. SA was positively associated with LGI in all regions and CT in none. CT and LGI, but not SA, were inversely associated with age in all regions. IC was inversely associated with age in all but the occipital region. For all regions, males had larger cortical SA than females. Males also had larger LGI in all regions and larger IC of the frontal area; however, these effects were accounted for by sex differences in SA. There were no age-by-sex interactions. The study of IC adds a semi-independent, sensitive measure of cortical morphology that relates to the underlying cytoarchitecture and may aid understanding of normal brain development and deviations from it.

Keywords: Cortex; Cortical thickness; Intrinsic curvature; Local gyrification index; Neuro-development; Surface area.

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Conflict of interest statement

Funding

The NeuroIMAGE project was supported by the National Institute of Health (NIH) Grant R01MH62873 (to S.V. Faraone), Nederlands Wetenschappelijk Organisatie (NWO) Large Investment Grant 1750102007010 and ZonMW Grant 60-60600-97-193, and NWO grants 433-09-242 and 056-13-015 (to JKB) and grants from Radboud University Medical Center Nijmegen, University Medical Center Groningen, Accare and VU University Medical Center Amsterdam. Further funding has been received from the European Union under grant agreements number 316978 (TS-EUROTRAIN) and number 643051 (MiND). BF is supported by a Vici grant from NWO (grant number 016-130-669), and she and JKB received funding from the NIH Consortium grant U54 EB020403, supported by a cross-NIH alliance that funds Big Data to Knowledge Centers of Excellence. None of the funding sources had any influence on study design, data collection, analysis, or interpretation. Nor did they have an influence on writing or decision to publish this manuscript.

Conflict of interest

JKB has been in the past 3 years a consultant to/member of advisory board of/and/or speaker for Janssen Cilag BV, Eli Lilly, Shire, Medice, Lundbeck, Roche, and Servier. He is not an employee of any of these companies, and not a stock shareholder of any of these companies. He has no other financial or material support, including expert testimony, patents, or royalties. BF received an educational speaking fee from Merz.

Figures

Fig. 1
Fig. 1
Surface indices. Cortical thickness (CT) is taken as the average shortest distance from the cortical surface to the grey/white matter border below. Surface area (SA) is the sum of the area of each triangle on the tessellated surface. Gyrification index (GI) is the ratio between the outer hull (solid line) and the surface buried within sulci (broken line). Intrinsic curvature varies with a higher spatial frequency and reflects a deformation of the surface due to differential expansion. The grey dots in the figure above may be thought of as cells within the cortex with the arrows between as connections. Differential expansion of the cortex results in either positive or negative intrinsic curvature values. Uniform expansion generates an overall increase in distances between points but no change in the proportion of long-to-short connections. Differential expansion (positive or negative intrinsic curvature) also increases the overall distance between points, but more importantly, it also increases the relative proportion of short-to-long connections
Fig. 2
Fig. 2
Regions for analysis. Inflated view of the left hemisphere divided into the regions used for analysis. Left shows the lateral view and right the medial view
Fig. 3
Fig. 3
Age curves for each metric per region. Each graph plots a metric (columns from left to right correspond to intrinsic curvature skew, cortical thickness, local gyrification index, and surface area, respectively) over age separately for males and females in each region (rows from top to bottom correspond to frontal, parietal, temporal, occipital, cingulate, and insula regions, respectively). An increase in IC skew indicates a reduction in the degree of IC as a function of age. Males are depicted in black with females in grey. Broken lines represent the standard error for each
See this image and copyright information in PMC

References

    1. Alexander-Bloch AF, Reiss PT, Rapoport J, et al. Abnormal cortical growth in schizophrenia targets normative modules of synchronized development. Biol Psychiatry. 2014;76:438–446. doi: 10.1016/j.biopsych.2014.02.010. - DOI - PMC - PubMed
    1. Amlien IK, Fjell AM, Tamnes CK, et al. Organizing principles of human cortical development—thickness and area from 4 to 30 years: insights from comparative primate neuroanatomy. Cereb Cortex. 2016;26:257–267. doi: 10.1093/cercor/bhu214. - DOI - PubMed
    1. Brown TT, Kuperman JM, Chung Y, et al. Neuroanatomical assessment of biological maturity. Curr Biol. 2012;22:1693–1698. doi: 10.1016/j.cub.2012.07.002. - DOI - PMC - PubMed
    1. Crews F, He J, Hodge C. Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol Biochem Behav. 2007;86:189–199. doi: 10.1016/j.pbb.2006.12.001. - DOI - PMC - PubMed
    1. Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage. 1999;9:179–194. doi: 10.1006/nimg.1998.0395. - DOI - PubMed