Developmental change in regional brain structure over 7 months in early adolescence: comparison of approaches for longitudinal atlas-based parcellation.

paper Cited Public

Authors: Sullivan, Edith V; Pfefferbaum, Adolf; Rohlfing, Torsten; Baker, Fiona C; Padilla, Mayra L; Colrain, Ian M
Year: 2011
Journal: NeuroImage
PMID: 21511039
DOI: 10.1016/j.neuroimage.2011.04.003
PMCID: PMC3101309

Early adolescence is a time of rapid change in neuroanatomy and sexual development. Precision in tracking changes in brain morphology with structural MRI requires image segmentation with minimal error. Here, we compared two approaches to achieve segmentation by image registration with an atlas to quantify regional brain structural development over a 7-month interval in normal, early adolescent boys and girls. Adolescents were scanned twice (average interval=7.3 months), yielding adequate data for analysis in 16 boys (baseline age 10.9 to 13.9 years; Tanner Stage=1 to 4) and 12 girls (baseline age=11.2 to 13.7 years; Tanner Stage=3 to 4). Brain volumes were derived from T1-weighted (SPGR) images and dual-echo Fast Spin-Echo (FSE) images collected on a GE 3T scanner with an 8-channel phased-array head coil and analyzed by registration-based parcellation using the SRI24 atlas. The "independent" method required two inter-subject registrations: both baseline (MRI 1) to atlas and follow-up (MRI 2) to the atlas. The "sequential" method required one inter-subject registration, which was MRI 1 to the atlas, and one intra-subject registration, which was MRI 2 to MRI 1. Gray matter/white matter/CSF were segmented in both MRI-1 and MRI-2 using FSL FAST with tissue priors also based on the SRI24 atlas. Gray matter volumes were derived for 10 cortical regions, gray+white matter volumes for 5 subcortical structures, and CSF volumes for 4 ventricular regions and the cortical sulci. Across the 15 tissue regions, the coefficient of variation (CV) of change scores across individuals was significantly lower for the sequential method (CV=3.02), requiring only one inter-subject registration, than for the independent method (CV=9.43), requiring two inter-subject registrations. Volume change based on the sequential method revealed that total supratentorial and CSF volumes increased, while cortical gray matter volumes declined significantly (p<0.01) in anterior (lateral and medial frontal, anterior cingulate, precuneus, and parietal) but not posterior (occipital, calcarine) cortical regions. These volume changes occurred in all boys and girls who advanced a step in Tanner staging. Subcortical structures did not show consistent changes. Thus, longitudinal MRI assessment using robust registration methods is sufficiently sensitive to identify significant regional brain changes over a 7-month interval in boys and girls in early adolescence. Increasing the temporal resolution of the retest interval in longitudinal developmental studies could increase accuracy in timing of peak growth of regional brain tissue and refine our understanding of the neural mechanisms underlying the dynamic changes in brain structure throughout adolescence.

Figure 1

Work flow of the independent (top) and sequential (bottom) registration method.

LLM interpretation

This figure consists of two flow diagrams illustrating "Independent" (top) and "Sequential" (bottom) registration methods for MRI data. In the independent method, two separate MRI scans (MRI 1 and MRI 2) are each registered to the SRI24 Atlas via inter-subject non-linear registration. In the sequential method, MRI 1 is registered to the SRI24 Atlas, and MRI 2 is subsequently registered to MRI 1 via intra-subject non-linear registration.

Figure 2

Top panel in gray scale: Axial slices from the SRI24 atlas of the superior (top left) to inferior (bottom right) reaches of the brain. Bottom panel in color: 15 cortical and subcortical regions of interest (ROIs) overlaid on the SRI24 atlas and color-coded by structure name. LatFrnt=lateral frontal cortex; MedFrnt=medial frontal cortex; Insula; AntCing=anterior cingulate cortex; PostCing=posterior cingulate cortex; Precuneus; HipAmyg=hippocampus and amygdala; Occiput=occipital cortex; Parietal=parietal cortex; CaudPut=caudate and putamen; Thalamus; Temporal=temporal cortex; SupCblm=superior cerebellum; InfCblm=inferior cerebellum; Calcarine=calcarine cortex.

LLM interpretation

This figure consists of two panels showing axial brain slices from the SRI24 atlas. The top panel displays grayscale anatomical slices ranging from superior to inferior reaches of the brain. The bottom panel shows the same slices with 15 color-coded cortical and subcortical regions of interest (ROIs) overlaid, with a corresponding legend identifying each structure by color.

Figure 3

Left panel in gray scale: Coronal slices from the SRI24 atlas at the level of the parcellated example. Right panel: 5 color-coded CSF-filled ROIs. Note that cortical sulcal volume was derived from the CSF volume in the outer 45% rim of the brain.

LLM interpretation

This figure consists of two panels: a grayscale coronal brain slice from the SRI24 atlas (slice 116) on the left and a corresponding color-coded map of cerebrospinal fluid (CSF)-filled regions of interest (ROIs) on the right. The right panel identifies five distinct ROIs: cortical sulci (blue), lateral ventricles (green), Sylvian fissure (red), temporal horn (yellow), and the 3rd ventricle (white).

Figure 4

Mean±SEM % regional volume change (%=(MRI 2 - MRI 1)/MRI 1) for tissue ROIs (top panel) and CSF-filled ROIs and supratentorial volume (SCV) (bottom panel) for the independent and sequential registration methods. Lat Frnt=lateral frontal cortex; Med Frnt=medial frontal cortex; Insula; Ant Cing=anterior cingulate cortex; Post Cing=posterior cingulate cortex; Precuneus; HippAmyg=hippocampus and amygdala; Occipital=occipital cortex; Parietal=parietal cortex; CaudPut=caudate and putamen; Thalamus; Temporal=temporal cortex; Sup Cblm=superior cerebellum; Inf Cblm=inferior cerebellum; Calcarine=calcarine cortex; Lat Vent=lateral ventricles; Temp Horn=temporal horn; 3rd Vent=third ventricle; Sylvian=sylvian fissures; Cort Sulci=cortical sulci; SVol=Supratentorial volume. * and † indicate ROIs showing significant differences of the percentage volume change from 0.

LLM interpretation

This figure consists of two bar charts showing the mean percentage regional volume change between two MRI scans for "Independent" (light gray) and "Sequential" (dark gray) registration methods. The top panel displays tissue ROIs, while the bottom panel displays CSF-filled ROIs and supratentorial volume (SVol). Significant differences from zero are marked with asterisks (*p < .007) and daggers (†p < .02), appearing in several regions including the lateral and medial frontal cortex, precuneus, parietal cortex, lateral ventricles, temporal horn, sylvian fissures, and cortical sulci.

Figure 5

Top panel: Example of one adolescent's MRIs at the initial and follow-up examination. Bottom panel: “Spaghetti” plot of each subject's supratentorial volumes at each MRI by interval. Blue = boys; pink = girls.

LLM interpretation

The figure consists of two panels: the top shows two axial MRI brain scans of a single adolescent at an initial visit and a 6-month follow-up. The bottom panel is a "spaghetti" plot showing supratentorial volume (cc) versus age for multiple subjects, with blue lines representing boys and pink lines representing girls. Most lines show a slight upward trend in volume over time, with boys generally exhibiting higher volumes than girls across the age range of 11 to 15.

Figure 6

“Spaghetti” plots of each subject's tissue volumes for ROIs showing significant change between MRIs. Blue = boys; pink = girls.

LLM interpretation

This figure consists of six "spaghetti" plots showing longitudinal changes in tissue volume (cc) across age (years) for six different brain regions of interest (ROIs). Each line represents an individual subject, with blue lines denoting boys and pink lines denoting girls. The plots illustrate individual trajectories of volume change between two MRI time points for the Lateral Frontal Gray Matter, Medial Frontal, Parietal, Temporal, Anterior Cingulate Gray Matter, and Precuneus Gray Matter.

Figure 7

“Spaghetti” plots of each subject's CSF-filled volumes for ROIs showing significant change between MRIs. Blue = boys; pink = girls.

LLM interpretation

This figure consists of four "spaghetti" plots showing longitudinal changes in CSF-filled volumes (cc) across age (years) for four regions of interest: Lateral Ventricles, Cortical Sulci, Temporal Horn, and Sylvian Fissure. Individual subjects are represented by lines connecting two time points, with blue lines denoting boys and pink lines denoting girls. The plots show varied trajectories of volume change across the different brain regions and subjects.

Figure 8

Four tissue ROIs showing decreases (top panel) and two CSF ROIs showing increases (bottom panel) in the 6 adolescents whose Tanner stage advanced from MRI 1 to MRI 2.

LLM interpretation

This figure consists of two panels of scatter plots showing volume changes (cc) relative to Tanner stage change (0 vs 1) for six adolescents. The top panel displays tissue volumes for four regions (Lat Frontal, Ant Cingulate, Precuneus, and Parietal), showing a general trend toward negative volume change when the Tanner stage advances. The bottom panel displays CSF volumes for the Lateral Ventricles and Cortical Sulci, showing a general trend toward positive volume change with Tanner stage advancement.

#	Section	Preview
0	Introduction	Adolescence is associated with continued growth of head size and substantial changes in regional…
1	Introduction	In general, prospective longitudinal studies (reviewed in Paus, 2010) have verified cross-sectional…
2	Introduction	While trajectories of growth curves provide a basis for estimating peaks in growth, the accuracy of…
3	Introduction	These childhood-to-adolescent years also mark advancement through puberty and its plethora of…
4	Introduction	Accordingly, this study focused on change in regional brain volumes over an average of 7 months in…
5	Introduction	the independent method, rendering differences more reflective of true developmental effects rather…
6	Methods — Subjects	Adolescents (11 to 14 years old) were recruited from the local community through flyers, word of…
7	Methods — Subjects	At their initial and follow-up visits, parents and their children were interviewed by a laboratory…
8	Methods — Subjects	The adolescents were given the self-administered rating scale for pubertal development (Carskadon et…
9	Methods — MRI acquisition	MR data were collected on a GE 3T Signa scanner with an 8-channel phased-array head coil. Brain…
10	Methods — Image preprocessing	All acquired structural images were first corrected for intensity bias by applying a second-order…
11	Methods — Registration and atlas-based parcellation	For each subject, the skull-stripped baseline and follow-up SPGR images were each registered to the…
12	Methods — Registration and atlas-based parcellation	The unstripped but bias-corrected follow-up SPGR image for each subject was then registered to the…
13	Methods — Registration and atlas-based parcellation	The rationale for using direct transformations to parcellate the baseline images, but concatenated…
14	Methods — Registration and atlas-based parcellation	Thus, although the use of a concatenated transformation to parcellate the follow-up data does not…
15	Methods — Tissue segmentation	All bias-corrected and skull-stripped SPGR images were segmented into three tissue compartments…
16	Methods — Regions of interest (ROIs)	This analysis focused on major lobar tissue regions of the cortex, allocortex, and subcortical…
17	Methods — ROI to estimate signal-to-noise ratio (SNR)	We estimated SNR, which could be diminished by subject movement, in a sample of highly coherent…
18	Methods — Statistical analysis for MRI data	Comparison of the two registration methods was based on differences between volumes at MRI 1…
19	Methods — Statistical analysis for MRI data	Coefficients of variation (CV) of change scores across individuals were calculated for each ROI…

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The INIA19 Template and NeuroMaps Atlas for Primate Brain Image Parcellation and Spatial Normalization.	Rohlfing T et al.	—	2012	→
Sleep EEG, the clearest window through which to view adolescent brain development.	Colrain IM et al.	—	2011	→
The brain dynamics of intellectual development: waxing and waning white and gray matter.	Tamnes CK et al.	—	2011	→