Test–retest reliability of brain morphology estimates
© The Author(s) 2017
Received: 19 September 2016
Accepted: 26 December 2016
Published: 5 January 2017
Metrics of brain morphology are increasingly being used to examine inter-individual differences, making it important to evaluate the reliability of these structural measures. Here we used two open-access datasets to assess the intersession reliability of three cortical measures (thickness, gyrification, and fractal dimensionality) and two subcortical measures (volume and fractal dimensionality). Reliability was generally good, particularly with the gyrification and fractal dimensionality measures. One dataset used a sequence previously optimized for brain morphology analyses and had particularly high reliability. Examining the reliability of morphological measures is critical before the measures can be validly used to investigate inter-individual differences.
A growing number of studies have investigated relationships between brain morphology and inter-individual differences. An important assumption that underlies these studies is that estimates of brain morphology are reliable. While numerous studies have investigated the test–retest reliability for estimates of cortical thickness (e.g., [1–7]) and subcortical volume (e.g., [7–12]), the reliability of other measures of brain morphology has been less established and is an important topic of future research . Here we measured the reliability of several measures of cortical and subcortical structures; in addition to cortical thickness and subcortical volume, we examined the reliability of estimates of cortical gyrification and fractal dimensionality.
Gyrification index is a measure of the ratio between the surface area of the cortex, relative to a simulated enclosing surface that surrounds the cortex (e.g., [14–18]). Generally, gyrification has been suggested to be an important characteristic of the human brain [15–19]. In addition to the well-known differences in cortical thickness associated with age, gyrification also differs with age [20–22]; however, age-related differences in gyrification appear to have a distinct topological distribution than thickness [20, 21]. Gyrification has also been associated with a myriad of other inter-individual measures, as reviewed by Mietchen and Gaser .
Structural complexity is measured as fractal dimensionality, which uses fractal geometry principles  to measure the complexity of brain structures (see ). We recently demonstrated robust age differences in the structural complexity of cortical  and subcortical structures . Less work has been done examining the relationship between inter-individual differences and variance in complexity of cortical and subcortical regions; however, these approaches have been found to be useful in a variety of disciplines within neuroscience [25, 26].
Here we examined the test–retest reliability of several measures of brain morphology. While volumetric measures—cortical thickness and subcortical volume—have been evaluated previously, we additionally evaluated the reliability of shape-related measures, specifically gyrification and fractal dimensionality. We evaluated the FreeSurfer implementation of gyrification, as implemented by Schaer et al. . This approach generates an enclosing surface around each hemisphere and computes the ‘local’ difference in surface between this surface and the pial surface of the cortex. As such, gyrification is highest over the insula and lowest over medial cortical regions. Fractal dimensionality was evaluated based on the calcFD toolbox , which computes fractal dimensionality using intermediate files generated as part of the standard FreeSurfer pipeline. Madan and Kensinger  previously compared different algorithms for calculating fractal dimensionality using simulated 3D structures, but here we instead used multiple anatomical volumes acquired from the same participant (i.e., test–retest reliability).
Structural measurements are often used to assess longitudinal changes or inter-individual differences. For instance, advancements in measuring relationships between brain morphology and inter-individual differences have become increasingly relevant as a complementary approach to fMRI, due to aging-related confounds in group comparisons . More recently, age-related differences have been identified in BOLD signal variability [29, 30], which may be related to differences in cerebrovascular reactivity [31, 32]. As brain morphology research advances, it is critical to measure the reliability of these metrics using multiple volume acquisitions. For instance, if the effect of age on a morphological measure is small, poorer reliability may make the effect difficult to detect due to noise in the measure. A number of open-access databases include multiple scans on the same participants, enabling such reliability to be calculated. Appendix 1 summarizes a number of additional open-access datasets—in addition to those we consider here—that also include intersession test–retest reliability data.
Here we examined test–retest reliability from two open-access datasets in which participants were scanned several times over a short interval (i.e., intersession, intrascanner). In the first dataset, 30 participants were scanned 10 times within a 1-month period . In the original work, Chen et al. sought to estimate test–retest reliability of resting-state networks across intra- and inter-individual variability of six rs-fMRI measures (CCBD [Center for Cognition and Brain Disorders] dataset). In the second dataset, 69 participants were scanned twice within a 6-month period . Holmes et al. collected data for a large-scale exploration (N = 1570) of the relations among brain function, behavior, and genetics (GSP [Brain Genomics Superstruct Project] dataset). As one demonstration of the uses of this dataset, Holmes et al.  examined the relationship between cortical thickness and several measures of cognitive control.
In each of these datasets, we examined the reliability of three cortical measures: cortical thickness, gyrification, and fractal dimensionality—both of the entire cortical ribbon and across regional measures of parcellated cortex (62 regions, based on the DKT atlas; ). We additionally evaluated different approaches to calculating fractal dimensionality to establish the reliability of each of these approaches. Finally, reliability of volume and fractal dimensionality of segmented subcortical and ventricular structures also was evaluated. We consider each dataset separately, as would be the typical approach for examining test–retest reliability, and then discuss the conclusions reached using both datasets in the general discussion.
2 Study 1: CCBD
MR images were acquired using a GE MR750 3 T scanner at the Centre for Cognition and Brain Disorders (CCBD) at Hangzhou Normal University . Thirty participants aged 20–30 years old were each scanned for 10 sessions, occurring 2–3 days apart over a 1-month period. T1-weighted data were acquired using a FSPGR sequence (TR: 8.06 s; TE: 3.1 ms; flip angle: 8°; voxel size: 1.0 × 1.0 × 1.0 mm). This dataset is included as part of the Consortium for Reliability and Reproducibility (CoRR; ) as HNU1.
2.1.2 Preprocessing of the structural data
Data were analyzed using FreeSurfer 5.3.0 (https://surfer.nmr.mgh.harvard.edu) on a machine running CentOS 6.6. FreeSurfer was used to automatically volumetrically segment and parcellate cortical and subcortical structures from the T1-weighted images [37–40]. FreeSurfer’s standard pipeline was used (i.e., recon-all ). No manual edits were made to the surface meshes, but surfaces were visually inspected.
Cortical thickness is calculated as the distance between the white matter surface (white–gray interface) and pial surface (gray–CSF interface) . Thickness estimates have previously been found to be in agreement with manual measurements from MRI images [41, 42], as well as ex vivo tissue measurements [43, 44]. Subcortical volume estimates have also been found to correspond well with manual segmentation protocols, particularly in young adults [45–52].
Gyrification was also calculated using FreeSurfer, as described in Schaer et al. . Cortical regions were delineated based on the Desikan–Killiany–Tourville (DKT) atlas, also part of the standard FreeSurfer analysis pipeline . Intracranial volume (ICV) was also calculated using FreeSurfer .
Fractal dimensionality was quantified using the calcFD toolbox (http://cmadan.github.io/calcFD/), which we previously developed and distribute freely [21, 24]. calcFD is a MATLAB toolbox that calculates the fractal dimensionality of 3D structures and was developed to work with intermediate files from the standard FreeSurfer pipeline. Apart from when otherwise stated, FD was calculated for filled structures (FD f ) using the dilation algorithm. Here we additionally modified calcFD in two ways. First, we improved it to additionally calculate the fractal dimensionality of cortical parcellations for all regions delineated in the DKT atlas (see Appendix 2). An important consideration in decreasing the size of cortical parcellations, however, is that they inherently have decreased fractal dimensionality, i.e., becoming closer to a ‘truncated rectangular pyramid.’ Second, we adjusted the toolbox to calculate fractal dimensionality using the spherical harmonics (e.g., [54–58]). Additional details about this spherical harmonics approach are outlined in Appendix 3.
2.1.3 Measuring reliability
Reliability was calculated as intraclass correlation coefficient (ICC), which can be used to quantify the relationship between multiple measurements [59–62]. McGraw and Wong  provide a comprehensive review of the various ICC formulas and their applicability to different research questions. ICC was calculated as the one-way random effects model for the consistency of single measurements, i.e., ICC(1). As a general guideline, ICC values between .75 and 1.00 are considered ‘excellent,’ .60–.74 is ‘good,’ .40–.59 is ‘fair,’ and below .40 is ‘poor’ . For the cortical parcellated regions, distributions of mean reliability measures (e.g., lower panel of Fig. 4) were compared using a Mann–Whitney U test, a nonparametric for testing whether two sets of values belong to the same distribution.
In the current study, we focused on regional estimates of brain morphology; a complimentary approach that we did not evaluate here is the reliability in spatial segmentation. This alternative approach evaluates the volumetric overlap between 3D structures within the same space, often quantified as a Dice coefficient (e.g., [5, 10, 48, 50, 65]). This overlap approach is often used when comparing manual and automatic segmentation protocols of the same anatomical volume; however, it can be applied to test–retest reliability by co-registering the individual anatomical volumes from the same participant to each other and comparing the resulting segmented structures’ overlap. In contrast, the present goal was to evaluate ‘summary statistics’ of the structures, such as thickness, volume, and fractal dimensionality.
2.2.1 Cortical ribbon
Test–retest reliability (ICC) for each measure and dataset, for the cortical ribbon data
Dilation filled (FD f )
Fractal dimensionality We computed the reliability of five calculations of fractal dimensionality. First, we used both the dilation and box-counting algorithms, as implemented in the calcFD toolbox, for both the filled volumes and surfaces only. We additionally used a spherical harmonics (SPHARM) approach (surface only). See Appendix 3 for further details about calculating fractal dimensionality using spherical harmonics. Figure 1 shows estimates of fractal dimensionality based on the dilation-filled approach.
As shown in Table 1, we consistently found higher reliability for the dilation algorithm than the box-counting algorithm, though this difference was not statistically significant. We found higher reliability for the spherical harmonics approach; however, this approach can only be used for surfaces of structures (rather than filled volumes).
2.2.2 Cortical parcellations
As expected (as in ), gyrification was highest in the insula and lowest over medial cortical regions (Fig. 2). Beyond this, we additionally observed greater gyrification over parietal regions, convergent with prior studies (e.g., [20, 21]). Test–retest reliability of regional gyrification was generally quite high (Figs. 3, 4) and was significantly higher for gyrification than cortical thickness [Z = 5.98, p < .001].
Regional fractal dimensionality is shown in Fig. 2. Smaller regions had lower fractal dimensionality, as smaller segmented structures inherently have less structural complexity due to both limitations MRI acquisition precision and biological constraints (also see ). Intraclass correlations (ICCs) are shown for each structural measure and brain region in Fig. 3; Fig. 4 shows the 95% confidence intervals of the inter-class correlations (ICCs) for each measure and region. Across regions, mean ICC was not significantly related to the size of the region for any of the measures [thickness: r(60) = .206, p = .11; gyrification: r(60) = .154, p = .23; fractal dimensionality: r(60) = .251, p = .05]. Test–retest reliability of regional fractal dimensionality was generally high (Figs. 3, 4) and was also significantly higher than for cortical thickness [Z = 5.46, p < .001]. Reliability did not differ between gyrification and fractal dimensionality [Z = .31, p = .75].
2.2.3 Subcortical structures
The results indicate that gyrification and fractal dimensionality have high test–retest reliability. Indeed, reliability using these measures was higher than for cortical thickness.
3 Study 2: GSP
To further assess the replicability of these findings, we calculated these same measures in a second dataset. While this dataset had only two MRI sessions, rather than 10, this dataset used an anatomical MRI sequence that was optimized for brain morphology research (based on prior validation work assessing cortical thickness and subcortical volume) [7, 68]. While this prior validation work suggests that reliability for cortical thickness and subcortical volume should be higher for this dataset, it is not clear how these improvements to volumetric measures may influence shape-related measures of morphology (i.e., gyrification and fractal dimensionality).
MR images were acquired on Siemens Trio 3 T scanners at Harvard University and Massachusetts General Hospital, as part of the Brain Genome Superstruct Project (GSP; ). This dataset includes 1570 participants from aged 18 to 25 years old. Test–retest reliability data were available for 69 participants who were scanned within 6 months of their first session (also see ). T1-weighted data were acquired using a MEMPRAGE sequence optimized for brain morphology (TR: 2.20 s; TE: 1.5, 3.4, 5.2, 7.0 ms; flip angle: 7°; voxel size: 1.2 × 1.2 × 1.2 mm) [7, 68].
3.1.2 Data analysis
The MR images were processed using an identical procedure as in Study 1. ICC was also evaluated using the same approach.
3.2.1 Cortical ribbon
3.2.2 Cortical parcellations
3.2.3 Subcortical structures
As shown in Fig. 8c, test–retest reliability was near perfect for both volume and fractal dimensionality of the subcortical structures. The regions that had relatively lower reliability (pallidum, amygdala, accumbens) were also relatively lower in Study 1, demonstrating the replicability of lower test–retest reliability in these regions—at least when segmented using FreeSurfer’s automated algorithms. Reliability was particularly high for the hippocampus and was significantly higher than in the CCBD dataset (Study 1).
Here we evaluated the test–retest reliability of several brain morphology measures using open-access datasets. Prior work had examined the reliability of volumetric measures—cortical thickness and subcortical volume; however, the present study is the first to assess reliability of shape-related measures, gyrification and fractal dimensionality.
Both datasets showed relatively high reliability for all morphology measures and additionally revealed that reliability was particularly good for the gyrification and fractal dimensionality measures. Additionally, we provide empirical evidence that the dilation approach for calculating fractal dimensionality was superior in reliability to the ‘standard’ box-counting method. These findings held across two datasets, but reliability was particularly good in the GSP dataset, where the anatomical sequence had been previously optimized for use in brain morphology studies.
Although reliability was good in these datasets, there is still the question of how reliability may be increased in future studies. A number of factors have been found to influence estimates of brain morphology. Broadly, these factors can be divided into three categories: MR acquisition, biological, and analysis related. For MR acquisition, there are not yet enough datasets available to systematically examine how reliability is affected by the particular acquisition protocols, although the current data suggest that sequences previously optimized for brain morphology analyses (i.e., those used in GSP dataset) will have better reliability. Another acquisition-related factor is head movement; movement has been shown to lead to decreased estimates of cortical thickness [69–72], though it is unclear how movement would affect measures of gyrification and fractal dimensionality. This issue may become less critical in future studies, as recent advances in structural imaging have been able to attenuate movement-related artifacts (e.g., [73–76]). Morphological measures can also be influenced by biological confounds, such as hydration [77–80] or circadian rhythms [81, 82]. Additionally, it is important to control for variations in analysis software and operating system, which can also affect brain morphology estimates [65, 83, 84].
While the surface reconstructions were visually inspected, the surfaces were not manually edited, for two reasons. First and foremost, the quality of the automatic reconstructions was judged to be acceptable and did not require manual intervention. While manual editing is more necessary with older adult and patient populations, all of the individuals included in the present work were young adults. Additionally, manual editing introduces a subjective component and is often not conducted in studies of reconstruction reliability [2, 5, 6, 46], though some reliability studies have included minimal manual editing [4, 7]. Given that no manual editing was conducted, the reliability estimates presented here may serve as a lower bound, where manual editing would be expected to increase reliability [4, 6]; however, there is evidence that editing may not sufficiently influence regional estimates [85, 86].
Fractal dimensionality was used here as a measure of the complexity in the shape of a structure. Results indicate that this measure was generally more reliable than volumetric morphological measures, likely because fractal dimensionality is influenced by both shape and volumetric characteristics that often covary [21, 24, 87–89]. By pooling from both of these characteristics, fractal dimensionality appears to be more reliable and should be considered in future research investigating the relationship between brain morphology and inter-individual differences.
In sum, here we evaluated the reliability of several brain morphology estimates using two open-access datasets. Reliability was generally high, providing support for using gyrification and fractal dimensionality measures to evaluate inter-individual or between-sample differences in morphology.
Portions of this research were supported by a grant from the National Institutes of Health (MH080833; to E.A.K.) and by funding provided by Boston College. C.R.M. was supported by a fellowship from the Canadian Institutes of Health Research (FRN-146793). MRI data used in the preparation of this article were obtained from several sources, data were provided in part by: (1) the Center for Cognition and Brain Disorders (CCBD; ) as dataset HNU1 in the Consortium for Reliability and Reproducibility (CoRR; ); and (2) the Brain Genomics Superstruct Project (GSP; ) of Harvard University and the Massachusetts General Hospital (Principal Investigators: Randy Buckner, Joshua Roffman, and Jordan Smoller), with support from the Center for Brain Science Neuroinformatics Research Group, the Athinoula A. Martinos Center for Biomedical Imaging, and the Center for Human Genetic Research, and 20 individual investigators at Harvard and MGH generously contributed data to the overall project.
Compliance with ethical standards
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
- Dickerson BC, Fenstermacher E, Salat DH, Wolk DA, Maguire RP, Desikan R et al (2008) Detection of cortical thickness correlates of cognitive performance: reliability across MRI scan sessions, scanners, and field strengths. NeuroImage 39:10–18. doi:10.1016/j.neuroimage.2007.08.042 View ArticleGoogle Scholar
- Han X, Jovicich J, Salat D, van der Kouwe A, Quinn B, Czanner S et al (2006) Reliability of MRI-derived measurements of human cerebral cortical thickness: the effects of field strength, scanner upgrade and manufacturer. NeuroImage 32:180–194. doi:10.1016/j.neuroimage.2006.02.051 View ArticleGoogle Scholar
- Holmes AJ, Hollinshead MO, Roffman JL, Smoller JW, Buckner RL (2016) Individual differences in cognitive control circuit anatomy link sensation seeking, impulsivity, and substance use. J Neurosci 36:4038–4049. doi:10.1523/jneurosci.3206-15.2016 View ArticleGoogle Scholar
- Iscan Z, Jin TB, Kendrick A, Szeglin B, Lu H, Trivedi M et al (2015) Test–retest reliability of FreeSurfer measurements within and between sites: effects of visual approval process. Hum Brain Mapp 36:3472–3485. doi:10.1002/hbm.22856 View ArticleGoogle Scholar
- Jovicich J, Marizzoni M, Sala-Llonch R, Bosch B, Bartrés-Faz D, Arnold J et al (2013) Brain morphometry reproducibility in multi-center 3T MRI studies: a comparison of cross-sectional and longitudinal segmentations. NeuroImage 83:472–484. doi:10.1016/j.neuroimage.2013.05.007 View ArticleGoogle Scholar
- Liem F, Mérillat S, Bezzola L, Hirsiger S, Philipp M, Madhyastha T, Jäncke L (2015) Reliability and statistical power analysis of cortical and subcortical FreeSurfer metrics in a large sample of healthy elderly. NeuroImage 108:95–109. doi:10.1016/j.neuroimage.2014.12.035 View ArticleGoogle Scholar
- Wonderlick JS, Ziegler DA, Hosseini-Varnamkhasti P, Locascio J, Bakkour J, van der Kouwe A et al (2009) Reliability of MRI-derived cortical and subcortical morphometric measures: effects of pulse sequence, voxel geometry, and parallel imaging. NeuroImage 44:1324–1333. doi:10.1016/j.neuroimage.2008.10.037 View ArticleGoogle Scholar
- Bartzokis G, Mintz J, Marx P, Osborn D, Gutkind D, Chiang F et al (1993) Reliability of in vivo volume measures of hippocampus and other brain structures using MRI. Magn Reson Imaging 11:993–1006. doi:10.1016/0730-725x(93)90218-3 View ArticleGoogle Scholar
- Goodro M, Sameti M, Patenaude B, Fein G (2012) Age effect on subcortical structures in healthy adults. Psychiatry Res Neuroimaging 203:38–45. doi:10.1016/j.pscychresns.2011.09.014 View ArticleGoogle Scholar
- Jovicich J, Czanner S, Han X, Salat D, van der Kouwe A, Quinn B et al (2009) MRI-derived measurements of human subcortical, ventricular and intracranial brain volumes: reliability effects of scan sessions, acquisition sequences, data analyses, scanner upgrade, scanner vendors and field strengths. NeuroImage 46:177–192. doi:10.1016/j.neuroimage.2009.02.010 View ArticleGoogle Scholar
- Morey RA, Selgrade ES, Wagner HR, Huettel SA, Wang L, McCarthy G (2010) Scan-rescan reliability of subcortical brain volumes derived from automated segmentation. Hum Brain Mapp 31:1751–1762. doi:10.1002/hbm.20973 Google Scholar
- Nugent AC, Luckenbaugh DA, Wood SE, Bogers W, Zarate CA, Drevets WC (2013) Automated subcortical segmentation using FIRST: test–retest reliability, interscanner reliability, and comparison to manual segmentation. Hum Brain Mapp 34:2313–2329. doi:10.1002/hbm.22068 View ArticleGoogle Scholar
- Pestilli F (2015) Test–retest measurements and digital validation for in vivo neuroscience. Sci Data 2:140057. doi:10.1038/sdata.2014.57 View ArticleGoogle Scholar
- Mietchen D, Gaser C (2009) Computational morphometry for detecting changes in brain structure due to development, aging, learning, disease and evolution. Front Neuroinf 3:25. doi:10.3389/neuro.11.025.2009 View ArticleGoogle Scholar
- Toro R, Perron M, Pike B, Richer L, Veillette S, Pausova Z, Paus T (2008) Brain size and folding of the human cerebral cortex. Cereb Cortex 18:2352–2357. doi:10.1093/cercor/bhm261 View ArticleGoogle Scholar
- Armstrong E, Schleicher A, Omran H, Curtis M, Zilles K (1995) The ontogeny of human gyrification. Cereb Cortex 5:56–63. doi:10.1093/cercor/5.1.56 View ArticleGoogle Scholar
- Zilles K, Armstrong E, Schleicher A, Kretschmann H-J (1988) The human pattern of gyrification in the cerebral cortex. Anat Embryol 179:173–179. doi:10.1007/BF00304699
- Zilles K, Armstrong E, Moser KH, Schleicher A, Stephan H (1989) Gyrification in the cerebral cortex of primates. Brain Behav Evol 34:143–150. doi:10.1159/000116500
- Toro R (2012) On the possible shapes of the brain. Evol Biol 39:600–612. doi:10.1007/s11692-012-9201-8 View ArticleGoogle Scholar
- Hogstrom LJ, Westlye LT, Walhovd KB, Fjell AM (2013) The structure of the cerebral cortex across adult Life: age-related patterns of surface area, thickness, and gyrification. Cereb Cortex 23:2521–2530. doi:10.1093/cercor/bhs231 View ArticleGoogle Scholar
- Madan CR, Kensinger EA (2016) Cortical complexity as a measure of age-related brain atrophy. NeuroImage 134:617–629. doi:10.1016/j.neuroimage.2016.04.029 View ArticleGoogle Scholar
- Magnotta VA, Andreasen NC, Schultz SK, Harris G, Cizadlo T, Heckel D et al (1999) Quantitative in vivo measurement of gyrification in the human brain: changes associated with aging. Cereb Cortex 9:151–160. doi:10.1093/cercor/9.2.151
- Mandelbrot BB (1967) How long is the coast of Britain? Statistical self-similarity and fractional dimension. Science 156:636–638. doi:10.1126/science.156.3775.636 View ArticleGoogle Scholar
- Madan CR, Kensinger EA (2017) Age-related differences in the structural complexity of subcortical and ventricular structures. Neurobiol Aging 50:87–95. doi:10.1016/j.neurobiolaging.2016.10.023 View ArticleGoogle Scholar
- Di Ieva A, Esteban FJ, Grizzi F, Klonowski W, Martin-Landrove M (2015) Fractals in the neurosciences, part II: clinical applications and future perspectives. Neuroscientist 21:30–43. doi:10.1177/1073858413513928 View ArticleGoogle Scholar
- Di Ieva A, Grizzi F, Jelinek H, Pellionisz AJ, Losa GA (2014) Fractals in the neurosciences, part I: general principles and basic neurosciences. Neuroscientist 20:403–417. doi:10.1177/1073858413513927 View ArticleGoogle Scholar
- Schaer M, Cuadra MB, Schmansky N, Fischl B, Thiran J-P, Eliez S (2012) How to measure cortical folding from MR images: a step-by-step tutorial to compute local gyrification index. J Vis Exp 59:e3417. doi:10.3791/3417 Google Scholar
- Samanez-Larkin GR, D’Esposito M (2008) Group comparisons: imaging the aging brain. Soc Cognit Affect Neurosci 3:290–297. doi:10.1093/scan/nsn029 View ArticleGoogle Scholar
- Garrett DD, Samanez-Larkin GR, MacDonald SWS, Lindenberger U, McIntosh AR, Grady CL (2013) Moment-to-moment brain signal variability: a next frontier in human brain mapping? Neurosci Biobehav Rev 37:610–624. doi:10.1016/j.neubiorev.2013.02.015 View ArticleGoogle Scholar
- McIntosh AR, Vakorin V, Kovacevic N, Wang H, Diaconescu A, Protzner AB (2014) Spatiotemporal dependency of age-related changes in brain signal variability. Cereb Cortex 24:1806–1817. doi:10.1093/cercor/bht030 View ArticleGoogle Scholar
- Thomas BP, Liu P, Park DC, van Osch MJ, Lu H (2014) Cerebrovascular reactivity in the brain white matter: magnitude, temporal characteristics, and age effects. J Cereb Blood Flow Metab 34:242–247. doi:10.1038/jcbfm.2013.194 View ArticleGoogle Scholar
- Tsvetanov KA, Henson RNA, Tyler LK, Davis SW, Shafto MA, Taylor JR et al (2015) The effect of ageing on fMRI: correction for the confounding effects of vascular reactivity evaluated by joint fMRI and MEG in 335 adults. Hum Brain Mapp 36:2248–2269. doi:10.1002/hbm.22768 View ArticleGoogle Scholar
- Chen B, Xu T, Zhou C, Wang L, Yang N, Wang Z et al (2015) Individual variability and test–retest reliability revealed by ten repeated resting-state brain scans over one month. PLoS ONE 10:e0144963. doi:10.1371/journal.pone.0144963 View ArticleGoogle Scholar
- Holmes AJ, Hollinshead MO, O’Keefe TM, Petrov VI, Fariello GR, Wald LL et al (2015) Brain Genomics Superstruct Project initial data release with structural, functional, and behavioral measures. Sci Data 2:150031. doi:10.1038/sdata.2015.31 View ArticleGoogle Scholar
- Klein A, Tourville J (2012) 101 labeled brain images and a consistent human cortical labeling protocol. Front Neurosci 6:171. doi:10.3389/fnins.2012.00171 View ArticleGoogle Scholar
- Zuo X-N, Anderson JS, Bellec P, Birn RM, Biswal BB, Blautzik J et al (2014) An open science resource for establishing reliability and reproducibility in functional connectomics. Sci Data 1:140049. doi:10.1038/sdata.2014.49 View ArticleGoogle Scholar
- Fischl B (2012) FreeSurfer. NeuroImage 62:774–781. doi:10.1016/j.neuroimage.2012.01.021 View ArticleGoogle Scholar
- Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97:11050–11055. doi:10.1073/pnas.200033797 View ArticleGoogle Scholar
- Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C et al (2002) Whole brain segmentation: automated labelling of neuroanatomical structures in the human brain. Neuron 33:341–355. doi:10.1016/s0896-6273(02)00569-x View ArticleGoogle Scholar
- Fischl B, Salat DH, van der Kouwe AJW, Makris N, Ségonne F, Quinn BT, Dale AM (2004) Sequence-independent segmentation of magnetic resonance images. NeuroImage 23:S69–S84. doi:10.1016/j.neuroimage.2004.07.016 View ArticleGoogle Scholar
- Kuperberg GR, Broome MR, McGuire PK, David AS, Eddy M, Ozawa F et al (2003) Regionally localized thinning of the cerebral cortex in Schizophrenia. Arch Gen Psychiatry 60:878. doi:10.1001/archpsyc.60.9.878 View ArticleGoogle Scholar
- Salat DH, Buckner RL, Snyder AZ, Greve DN, Desikan RSR et al (2004) Thinning of the cerebral cortex in aging. Cereb Cortex 14:721–730. doi:10.1093/cercor/bhh032 View ArticleGoogle Scholar
- Cardinale F, Chinnici G, Bramerio M, Mai R, Sartori I, Cossu M et al (2014) Validation of FreeSurfer-estimated brain cortical thickness: comparison with histologic measurements. Neuroinformatics 12:535–542. doi:10.1007/s12021-014-9229-2 View ArticleGoogle Scholar
- Rosas HD, Liu AK, Hersch S, Glessner M, Ferrante RJ, Salat DH et al (2002) Regional and progressive thinning of the cortical ribbon in Huntington’s disease. Neurology 58:695–701. doi:10.1212/wnl.58.5.695 View ArticleGoogle Scholar
- Grimm O, Pohlack S, Cacciaglia R, Winkelmann T, Plichta MM, Demirakca T, Flor H (2015) Amygdalar and hippocampal volume: a comparison between manual segmentation, Freesurfer and VBM. J Neurosci Methods 253:254–261. doi:10.1016/j.jneumeth.2015.05.024 View ArticleGoogle Scholar
- Keller SS, Gerdes JS, Mohammadi S, Kellinghaus C, Kugel H, Deppe K et al (2012) Volume estimation of the thalamus using FreeSurfer and stereology: consistency between methods. Neuroinformatics 10:341–350. doi:10.1007/s12021-012-9147-0 View ArticleGoogle Scholar
- Lehmann M, Douiri A, Kim LG, Modat M, Chan D, Ourselin S et al (2010) Atrophy patterns in Alzheimer’s disease and semantic dementia: a comparison of FreeSurfer and manual volumetric measurements. NeuroImage 49:2264–2274. doi:10.1016/j.neuroimage.2009.10.056 View ArticleGoogle Scholar
- Morey RA, Petty CM, Xu Y, Pannu Hayes J, Wagner HR, Lewis DV et al (2009) A comparison of automated segmentation and manual tracing for quantifying hippocampal and amygdala volumes. NeuroImage 45:855–866. doi:10.1016/j.neuroimage.2008.12.033 View ArticleGoogle Scholar
- Mulder ER, de Jong RA, Knol DL, van Schijndel RA, Cover KS, Visser PJ et al (2014) Hippocampal volume change measurement: quantitative assessment of the reproducibility of expert manual outlining and the automated methods FreeSurfer and FIRST. NeuroImage 92:169–181. doi:10.1016/j.neuroimage.2014.01.058 View ArticleGoogle Scholar
- Pardoe HR, Pell GS, Abbott DF, Jackson GD (2009) Hippocampal volume assessment in temporal lobe epilepsy: how good is automated segmentation? Epilepsia 50:2586–2592. doi:10.1111/j.1528-1167.2009.02243.x View ArticleGoogle Scholar
- Tae WS, Kim SS, Lee KU, Nam E-C, Kim KW (2008) Validation of hippocampal volumes measured using a manual method and two automated methods (FreeSurfer and IBASPM) in chronic major depressive disorder. Neuroradiology 50:569–581. doi:10.1007/s00234-008-0383-9 View ArticleGoogle Scholar
- Wenger E, Mårtensson J, Noack H, Bodammer NC, Kühn S, Schaefer S et al (2014) Comparing manual and automatic segmentation of hippocampal volumes: reliability and validity issues in younger and older brains. Hum Brain Mapp 35:4236–4248. doi:10.1002/hbm.22473 View ArticleGoogle Scholar
- Buckner RL, Head D, Parker J, Fotenos AF, Marcus D, Morris JC, Snyder AZ (2004) A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume. NeuroImage 23:724–738. doi:10.1016/j.neuroimage.2004.06.018 View ArticleGoogle Scholar
- Chung MK (2014) Statistical and computational methods in brain image analysis. CRC Press, New YorkGoogle Scholar
- Chung MK, Dalton KM, Davidson RJ (2008) Tensor-based cortical surface morphometry via weighted spherical harmonic representation. IEEE Trans Med Imaging 27:1143–1151. doi:10.1109/tmi.2008.918338 View ArticleGoogle Scholar
- Chung MK, Dalton KM, Shen L, Evans AC, Davidson RJ (2007) Weighted Fourier series representation and its application to quantifying the amount of gray matter. IEEE Trans Med Imaging 26:566–581. doi:10.1109/tmi.2007.892519 View ArticleGoogle Scholar
- Shen L, Firpi HA, Saykin AJ, West JD (2009) Parametric surface modeling and registration for comparison of manual and automated segmentation of the hippocampus. Hippocampus 19:588–595. doi:10.1002/hipo.20613 View ArticleGoogle Scholar
- Yotter RA, Nenadic I, Ziegler G, Thompson PM, Gaser C (2011) Local cortical surface complexity maps from spherical harmonic reconstructions. NeuroImage 56:961–973. doi:10.1016/j.neuroimage.2011.02.007 View ArticleGoogle Scholar
- Asendorpf J, Wallbott HG (1979) Maße der Beobachterübereinstimmung: ein systematischer Vergleich. Zeitschrift für Sozialpsychologie 10:243–252Google Scholar
- Bartko JJ (1966) The intraclass correlation coefficient as a measure of reliability. Psychol Rep 19:3–11. doi:10.2466/pr0.19188.8.131.52 View ArticleGoogle Scholar
- Rajaratnam N (1960) Reliability formulas for independent decision data when reliability data are matched. Psychometrika 25:261–271. doi:10.1007/bf02289730 MathSciNetMATHView ArticleGoogle Scholar
- Shrout PE, Fleiss JL (1979) Intraclass correlations: uses in assessing rater reliability. Psychol Bull 86:420–428. doi:10.1037/0033-2909.86.2.420 View ArticleGoogle Scholar
- McGraw KO, Wong SP (1996) Forming inferences about some intraclass correlation coefficients. Psychol Methods 1:30–46. doi:10.1037/1082-989x.1.1.30 View ArticleGoogle Scholar
- Cicchetti DV (1994) Guidelines, criteria, and rules of thumb for evaluating normed and standardized assessment instruments in psychology. Psychol Assess 6:284–290. doi:10.1037/1040-35184.108.40.2064 View ArticleGoogle Scholar
- Glatard T, Lewis LB, Ferreira da Silva R, Adalat R, Beck N, Lepage C et al (2015) Reproducibility of neuroimaging analyses across operating systems. Front Neuroinf. doi:10.3389/fninf.2015.00012 Google Scholar
- Fjell AM, Westlye LT, Amlien I, Espeseth T, Reinvang I, Raz N et al (2009) High consistency of regional cortical thinning in aging across multiple samples. Cereb Cortex 19:2001–2012. doi:10.1093/cercor/bhn232 View ArticleGoogle Scholar
- Hutton C, Draganski B, Ashburner J, Weiskopf N (2009) A comparison between voxel-based cortical thickness and voxel-based morphometry in normal aging. NeuroImage 48:371–380. doi:10.1016/j.neuroimage.2009.06.043 View ArticleGoogle Scholar
- van der Kouwe AJW, Benner T, Salat DH, Fischl B (2008) Brain morphometry with multiecho MPRAGE. NeuroImage 40:559–569. doi:10.1016/j.neuroimage.2007.12.025 View ArticleGoogle Scholar
- Alexander-Bloch A, Clasen L, Stockman M, Ronan L, Lalonde F, Giedd J, Raznahan A (2016) Subtle in-scanner motion biases automated measurement of brain anatomy from in vivo MRI. Hum Brain Mapp 36:2385–2397. doi:10.1002/hbm.23180 View ArticleGoogle Scholar
- Pardoe HR, Kucharsky Hiess R, Kuzniecky R (2016) Motion and morphometry in clinical and nonclinical populations. NeuroImage 135:177–185. doi:10.1016/j.neuroimage.2016.05.005 View ArticleGoogle Scholar
- Reuter M, Tisdall MD, Qureshi A, Buckner RL, van der Kouwe AJW, Fischl B (2015) Head motion during MRI acquisition reduces gray matter volume and thickness estimates. NeuroImage 107:107–115. doi:10.1016/j.neuroimage.2014.12.006 View ArticleGoogle Scholar
- Savalia NK, Agres PF, Chan MY, Feczko EJ, Kennedy KM, Wig GS (2017) Motion-related artifacts in structural brain images revealed with independent estimates of in-scanner head motion. Hum Brain Mapp 38:472–492. doi:10.1002/hbm.23397 View ArticleGoogle Scholar
- Federau C, Gallichan D (2016) Motion-correction enabled ultra-high resolution in vivo 7T-MRI of the brain. PLoS ONE 11:e0154974. doi:10.1371/journal.pone.0154974 View ArticleGoogle Scholar
- Maclaren J, Herbst M, Speck O, Zaitsev M (2013) Prospective motion correction in brain imaging: a review. Magn Reson Med 69:621–636. doi:10.1002/mrm.24314 View ArticleGoogle Scholar
- Stucht D, Danishad KA, Schulze P, Godenschweger F, Zaitsev M, Speck O (2015) Highest resolution in vivo human brain MRI using prospective motion correction. PLoS ONE 10:e0133921. doi:10.1371/journal.pone.0133921 View ArticleGoogle Scholar
- Tisdall MD, Reuter M, Qureshi A, Buckner RL, Fischl B, van der Kouwe AJW (2016) Prospective motion correction with volumetric navigators (vNavs) reduces the bias and variance in brain morphometry induced by subject motion. NeuroImage 127:11–22. doi:10.1016/j.neuroimage.2015.11.054 View ArticleGoogle Scholar
- Duning T, Kloska S, Steinstrater O, Kugel H, Heindel W, Knecht S (2005) Dehydration confounds the assessment of brain atrophy. Neurology 64:548–550. doi:10.1212/01.wnl.0000150542.16969.cc View ArticleGoogle Scholar
- Kempton MJ, Ettinger U, Schmechtig A, Winter EM, Smith L, McMorris T et al (2009) Effects of acute dehydration on brain morphology in healthy humans. Hum Brain Mapp 30:291–298. doi:10.1002/hbm.20500 View ArticleGoogle Scholar
- Nakamura K, Brown RA, Araujo D, Narayanan S, Arnold DL (2014) Correlation between brain volume change and T2 relaxation time induced by dehydration and rehydration: implications for monitoring atrophy in clinical studies. NeuroImage Clin 6:166–170. doi:10.1016/j.nicl.2014.08.014 View ArticleGoogle Scholar
- Streitbürger D-P, Möller HE, Tittgemeyer M, Hund-Georgiadis M, Schroeter ML, Mueller K (2012) Investigating structural brain changes of dehydration using voxel-based morphometry. PLoS ONE 7:e44195. doi:10.1371/journal.pone.0044195 View ArticleGoogle Scholar
- Nakamura K, Brown RA, Narayanan S, Collins DL, Arnold DL (2015) Diurnal fluctuations in brain volume: statistical analyses of MRI from large populations. NeuroImage 118:126–132. doi:10.1016/j.neuroimage.2015.05.077 View ArticleGoogle Scholar
- Trefler A, Sadeghi N, Thomas AG, Pierpaoli C, Baker CI, Thomas C (2016) Impact of time-of-day on brain morphometric measures derived from T1-weighted magnetic resonance imaging. NeuroImage 133:41–52. doi:10.1016/j.neuroimage.2016.02.034 View ArticleGoogle Scholar
- Chepkoech J-L, Walhovd KB, Grydeland H, Fjell AM (2016) Effects of change in FreeSurfer version on classification accuracy of patients with Alzheimer’s disease and mild cognitive impairment. Hum Brain Mapp 37:1831–1841. doi:10.1002/hbm.23139 View ArticleGoogle Scholar
- Gronenschild EHBM, Habets P, Jacobs HIL, Mengelers R, Rozendaal N, van Os J, Marcelis M (2012) The effects of FreeSurfer version, workstation type, and Macintosh operating system version on anatomical volume and cortical thickness measurements. PLoS ONE 7:e38234. doi:10.1371/journal.pone.0038234 View ArticleGoogle Scholar
- McCarthy CS, Ramprashad A, Thompson C, Botti J-A, Coman IL, Kates WR (2015) A comparison of FreeSurfer-generated data with and without manual intervention. Front Neurosci 9:379. doi:10.3389/fnins.2015.00379 View ArticleGoogle Scholar
- Ronan L, Alexander-Bloch AF, Wagstyl K, Farooqi S, Brayne C, Tyler LK et al (2016) Obesity associated with increased brain age from midlife. Neurobiol Aging 47:63–70. doi:10.1016/j.neurobiolaging.2016.07.010 View ArticleGoogle Scholar
- Gerig G, Styner M, Jones D, Weinberger D, Lieberman J (2001b) Shape analysis of brain ventricles using SPHARM. In: Proceedings of the IEEE workshop on mathematical methods in biomedical image analysis (MMBIA 2001), pp 171–178. doi:10.1109/mmbia.2001.991731
- King RD, George AT, Jeon T, Hynan LS, Youn TS, Kennedy DN, Dickerson B (2009) Characterization of atrophic changes in the cerebral cortex using fractal dimensional analysis. Brain Imaging Behav 3:154–166. doi:10.1007/s11682-008-9057-9 View ArticleGoogle Scholar
- Nitzken MJ, Casanova MF, Gimelfarb G, Inanc T, Zurada JM, El-Baz A (2014) Shape analysis of the human brain: a brief survey. IEEE J Biomed Health Inf 18:1337–1354. doi:10.1109/jbhi.2014.2298139 View ArticleGoogle Scholar
- Chung MK (2013) Computational neuroanatomy: the methods. World Scientific Publishing, HackensackMATHGoogle Scholar
- Chung MK, Nacewicz BM, Wang S, Dalton KM, Pollak S, Davidson RJ (2008) Amygdala surface modeling with weighted spherical harmonics. Lect Notes Comput Sci 5128:177–184. doi:10.1007/978-3-540-79982-5_20 View ArticleGoogle Scholar
- Chung MK, Worsley KJ, Nacewicz BM, Dalton KM, Davidson RJ (2010) General multivariate linear modeling of surface shapes using SurfStat. NeuroImage 53:491–505. doi:10.1016/j.neuroimage.2010.06.032 View ArticleGoogle Scholar
- Dombroski B, Nitzken M, Elnakib A, Khalifa F, Switala A, El-Baz A, Casanova M (2014) Cortical surface complexity in a population-based normative sample. Transl Neurosci. doi:10.2478/s13380-014-0202-1 Google Scholar
- Gerig G, Styner M, Shenton ME, Lieberman JA (2001) Shape versus size: improved understanding of the morphology of brain structures. Lect Notes Comput Sci 2208:24–32. doi:10.1007/3-540-45468-3_4 MATHView ArticleGoogle Scholar
- Gong Z, Lu J, Chen J, Wang Y, Yuan Y, Zhang T et al (2011) Ventricle shape analysis for centenarians, elderly subjects, MCI and AD patients. Lect Notes Comput Sci 7012:84–92. doi:10.1007/978-3-642-24446-9_11 View ArticleGoogle Scholar
- Shen L, Saykin AJ, Kim S, Firpi HA, West JD, Risacher SL et al (2010) Comparison of manual and automated determination of hippocampal volumes in MCI and early AD. Brain Imaging Behav 4:86–95. doi:10.1007/s11682-010-9088-x View ArticleGoogle Scholar
- Styner M, Oguz I, Xu S, Brechbühler C, Pantazis D, Levitt JJ et al (2006) Framework for the statistical shape analysis of brain structures using SPHARM-PDM. Insight Journal 1071:242–250Google Scholar
- Yu P, Yeo BTT, Grant PE, Fischl B, Golland P (2007) Cortical folding development study based on over-complete spherical wavelets. In: International Conference on Computer Vision 2007 proceedings of the workshop on mathematical methods in biomedical image analysis (MMBIA). doi:10.1109/iccv.2007.4409137
- Boekel W, Keuken MC, Forstmann BU (2017) A test–retest reliability analysis of diffusion measures of white matter tracts relevant for cognitive control. Psychophysiology 54:24–33. doi:10.1111/psyp.12769 View ArticleGoogle Scholar
- Marcus DS, Wang TH, Parker J, Csernansky JG, Morris JC, Buckner RL (2007) Open Access Series of Imaging Studies (OASIS): cross-sectional MRI Data in young, middle aged, nondemented, and demented older adults. J Cogn Neurosci 19:1498–1507. doi:10.1162/jocn.2007.19.9.1498 View ArticleGoogle Scholar
- Gorgolewski KJ, Mendes N, Wilfing D, Wladimirow E, Gauthier CJ et al (2015) A high resolution 7-Tesla resting-state fMRI test–retest dataset with cognitive and physiological measures. Sci Data 2:140054. doi:10.1038/sdata.2014.54 View ArticleGoogle Scholar
- Landman BA, Huang AJ, Gifford A, Vikram DS, Lim IAL, Farrell JAD et al (2011) Multi-parametric neuroimaging reproducibility: a 3-T resource study. NeuroImage 54:2854–2866. doi:10.1016/j.neuroimage.2010.11.047 View ArticleGoogle Scholar
- Gorgolewski KJ, Storkey AJ, Bastin ME, Whittle I, Pernet C (2013) Single subject fMRI test–retest reliability metrics and confounding factors. NeuroImage 69:231–243. doi:10.1016/j.neuroimage.2012.10.085 View ArticleGoogle Scholar
- Maclaren J, Han Z, Vos SB, Fischbein N, Bammer R (2014) Reliability of brain volume measurements: a test–retest dataset. Sci Data 1:140037. doi:10.1038/sdata.2014.37 View ArticleGoogle Scholar
- Poldrack RA, Laumann TO, Koyejo O, Gregory B, Hover A, Chen M-Y et al (2015) Long-term neural and physiological phenotyping of a single human. Nat Commun 6:8885. doi:10.1038/ncomms9885 View ArticleGoogle Scholar
- Laumann TO, Gordon EM, Adeyemo B, Snyder AZ, Joo SJ, Chen M-Y et al (2015) Functional system and areal organization of a highly sampled individual human brain. Neuron 87:657–670. doi:10.1016/j.neuron.2015.06.037 View ArticleGoogle Scholar
- Choe AS, Jones CK, Joel SE, Muschelli J, Belegu V, Caffo BS et al (2015) Reproducibility and temporal structure in weekly resting-state fMRI over a period of 3.5 years. PLoS ONE 10:e0140134. doi:10.1371/journal.pone.0140134 View ArticleGoogle Scholar
- Froeling M, Tax CMW, Vos SB, Luijten PR, Leemans A (in press) “MASSIVE” brain dataset: multiple acquisitions for standardization of structural imaging validation and evaluation. Magn Reson Med. doi:10.1002/mrm.26259
- Orban P, Madjar C, Savard M, Dansereau C, Tam A, Das S et al (2015) Test–retest resting-state fMRI in healthy elderly persons with a family history of Alzheimer’s disease. Sci Data 2:150043. doi:10.1038/sdata.2015.43 View ArticleGoogle Scholar
- Lin Q, Dai Z, Xia M, Han Z, Huang R, Gong G et al (2015) A connectivity-based test–retest dataset of multi-modal magnetic resonance imaging in young healthy adults. Sci Data 2:150056. doi:10.1038/sdata.2015.56 View ArticleGoogle Scholar
- Huang L, Huang T, Zhen Z, Liu J (2016) A test–retest dataset for assessing long-term reliability of brain morphology and resting-state brain activity. Sci Data 3:160016. doi:10.1038/sdata.2016.16 View ArticleGoogle Scholar