Data-driven Assessment of Structural Image Quality

Data quality is increasingly recognized as one of the most important confounders in brain imaging research. It is particularly important for studies of brain development, where age is systematically related to in-scanner motion and data quality. Prior work has demonstrated that in-scanner head motion biases estimates of structural neuroimaging measures. Yet, objective measures of data quality are not available for most structural brain images. Here we sought to identify reliable, quantitative measures of data quality for T1-weighted volumes, describe how such measures of quality relate to common measures of brain structure, and delineate how this in turn may bias inference regarding brain development in youth. Three highly-trained raters provided manual ratings for 1601 T1-weighted volumes acquired as part of the Philadelphia Neurodevelopmental Cohort. Expert manual ratings were compared to automated quality measures, which derived measures from the Preprocessed Connectomes Project’s Quality Assurance Protocol (QAP). Generalized linear mixed-effects models using the automated quality measures were constructed in a training sample (n = 1067) to: 1) identify unusable images with significant artifacts, and 2) quantify subtle artifacts in usable images. These models were then tested in an independent validation dataset (n = 534). Results reveal that unusable images can be detected with a high degree of accuracy: a model including background kurtosis and skewness achieved an AUC of 0.95 in the training dataset and 0.94 in the independent validation dataset. While identification of subtle artifact was more challenging, an 8-parameter model achieved an AUC of 0.80 in the training dataset, and 0.92 in the validation dataset. Notably, quantitative measures of image quality were related to cortical thickness and gray matter density; measures of cortical volume were less affected by artifact. Furthermore, these quantitative measures of image quality demonstrated comparable or superior performance to estimates of motion derived from other imaging sequences acquired during the same protocol. Finally, data quality significantly altered structural brain maturation occurring during adolescent development. Taken together, these results indicate that reliable measures of data quality can be automatically derived from T1-weighted volumes, and that failing to control for data quality can systematically bias the results of studies of brain development.

[1]  Gary H. Glover,et al.  Reducing inter-scanner variability of activation in a multicenter fMRI study: Role of smoothness equalization , 2006, NeuroImage.

[2]  Daniel S. Margulies,et al.  The Neuro Bureau ADHD-200 Preprocessed repository , 2016, NeuroImage.

[3]  Yufeng Zang,et al.  DPABI: Data Processing & Analysis for (Resting-State) Brain Imaging , 2016, Neuroinformatics.

[4]  Christos Davatzikos,et al.  Neuroimaging of the Philadelphia Neurodevelopmental Cohort , 2014, NeuroImage.

[5]  Suzanne E. Welcome,et al.  Longitudinal Mapping of Cortical Thickness and Brain Growth in Normal Children , 2022 .

[6]  E M Haacke,et al.  MR artifacts: a review. , 1986, AJR. American journal of roentgenology.

[7]  Li Qingyang,et al.  Towards Automated Analysis of Connectomes: The Configurable Pipeline for the Analysis of Connectomes (C-PAC) , 2013 .

[8]  D. Mathalon,et al.  A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. , 1994, Archives of neurology.

[9]  E. DeLong,et al.  Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. , 1988, Biometrics.

[10]  K. Saleh,et al.  Comprehensive assessment. , 2012, Nursing older people.

[11]  N. Ryan,et al.  Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. , 1997, Journal of the American Academy of Child and Adolescent Psychiatry.

[12]  W. A. Shewhart,et al.  Quality control , 1927 .

[13]  Jonathan D. Power,et al.  Recent progress and outstanding issues in motion correction in resting state fMRI , 2015, NeuroImage.

[14]  M. Zaitsev,et al.  Motion artifacts in MRI: A complex problem with many partial solutions , 2015, Journal of magnetic resonance imaging : JMRI.

[15]  Melanie Bennett,et al.  Initial development and preliminary validation of a new negative symptom measure: The Clinical Assessment Interview for Negative Symptoms (CAINS) , 2010, Schizophrenia Research.

[16]  A. Toga,et al.  Mapping Continued Brain Growth and Gray Matter Density Reduction in Dorsal Frontal Cortex: Inverse Relationships during Postadolescent Brain Maturation , 2001, The Journal of Neuroscience.

[17]  NeuroData,et al.  Towards Automated Analysis of Connectomes: The Configurable Pipeline for the Analysis of Connectomes , 2015 .

[18]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[19]  J. Giedd Structural Magnetic Resonance Imaging of the Adolescent Brain , 2004, Annals of the New York Academy of Sciences.

[20]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[21]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[22]  M. Dylan Tisdall,et al.  Head motion during MRI acquisition reduces gray matter volume and thickness estimates , 2015, NeuroImage.

[23]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

[24]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[25]  D. Linszen,et al.  Semantic fluency deficits and reduced grey matter before transition to psychosis: A voxelwise correlational analysis , 2011, Psychiatry Research: Neuroimaging.

[26]  Abraham Z. Snyder,et al.  Human Connectome Project informatics: Quality control, database services, and data visualization , 2013, NeuroImage.

[27]  Paul A. Yushkevich,et al.  Multi-Atlas Segmentation with Joint Label Fusion , 2013, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[28]  Christos Davatzikos,et al.  Benchmarking of participant-level confound regression strategies for the control of motion artifact in studies of functional connectivity , 2017, NeuroImage.

[29]  J. Giedd,et al.  Subtle in‐scanner motion biases automated measurement of brain anatomy from in vivo MRI , 2016, Human brain mapping.

[30]  T. Jernigan,et al.  Maturation of human cerebrum observed in vivo during adolescence. , 1991, Brain : a journal of neurology.

[31]  J. Townsend,et al.  Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers. , 2000, Radiology.

[32]  Alan C. Evans,et al.  Brain development during childhood and adolescence: a longitudinal MRI study , 1999, Nature Neuroscience.

[33]  Guido Gerig,et al.  Multisite validation of image analysis methods: assessing intra- and intersite variability , 2002, SPIE Medical Imaging.

[34]  Heath R. Pardoe,et al.  Motion and morphometry in clinical and nonclinical populations , 2016, NeuroImage.

[35]  D. Selkoe Alzheimer's disease. , 2011, Cold Spring Harbor perspectives in biology.

[36]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

[37]  Travis B. Smith,et al.  MRI artifacts and correction strategies , 2010 .

[38]  L. Westlye,et al.  Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. , 2010, Cerebral cortex.

[39]  A. Reiss,et al.  Brain development, gender and IQ in children. A volumetric imaging study. , 1996, Brain : a journal of neurology.

[40]  Brian B. Avants,et al.  An Open Source Multivariate Framework for n-Tissue Segmentation with Evaluation on Public Data , 2011, Neuroinformatics.

[41]  Arno Klein,et al.  Large-scale evaluation of ANTs and FreeSurfer cortical thickness measurements , 2014, NeuroImage.

[42]  Arno Klein,et al.  A reproducible evaluation of ANTs similarity metric performance in brain image registration , 2011, NeuroImage.

[43]  Nancy Kanwisher,et al.  Spurious group differences due to head motion in a diffusion MRI study , 2013, NeuroImage.

[44]  Bennett A. Landman,et al.  Non-local STAPLE: An Intensity-Driven Multi-atlas Rater Model , 2012, MICCAI.

[45]  Justin L. Vincent,et al.  Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. , 2008, Journal of neurophysiology.

[46]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.

[47]  Max Kuhn,et al.  caret: Classification and Regression Training , 2015 .

[48]  Richard F. Betzel,et al.  Human Connectomics across the Life Span , 2017, Trends in Cognitive Sciences.

[49]  Timothy O. Laumann,et al.  Generation and Evaluation of a Cortical Area Parcellation from Resting-State Correlations. , 2016, Cerebral cortex.

[50]  Satrajit S. Ghosh,et al.  Evaluation of volume-based and surface-based brain image registration methods , 2010, NeuroImage.

[51]  Brian B. Avants,et al.  Registration based cortical thickness measurement , 2009, NeuroImage.

[52]  Mark A. Elliott,et al.  Heritability of Subcortical and Limbic Brain Volume and Shape in Multiplex-Multigenerational Families with Schizophrenia , 2015, Biological Psychiatry.

[53]  M. Sobel Asymptotic Confidence Intervals for Indirect Effects in Structural Equation Models , 1982 .

[54]  Ragini Verma,et al.  The impact of quality assurance assessment on diffusion tensor imaging outcomes in a large-scale population-based cohort , 2016, NeuroImage.

[55]  E. Feczko,et al.  Motion‐related artifacts in structural brain images revealed with independent estimates of in‐scanner head motion , 2016, Human brain mapping.

[56]  N. Makris,et al.  Basic principles of MRI and morphometry studies of human brain development , 2002 .

[57]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[59]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[60]  D. Joanes,et al.  Comparing measures of sample skewness and kurtosis , 1998 .

[61]  Lee Friedman,et al.  Measurement of Signal-to-Noise and Contrast-to-Noise in the fBIRN Multicenter Imaging Study , 2006, Journal of Digital Imaging.

[62]  R. Cameron Craddock,et al.  A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics , 2013, NeuroImage.

[63]  Suzanne E. Welcome,et al.  Mapping cortical change across the human life span , 2003, Nature Neuroscience.

[64]  John G. Csernansky,et al.  Open Access Series of Imaging Studies (OASIS): Cross-sectional MRI Data in Young, Middle Aged, Nondemented, and Demented Older Adults , 2007, Journal of Cognitive Neuroscience.

[65]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[66]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[67]  Jeffrey P. Woodard,et al.  No-Reference image quality metrics for structural MRI , 2007, Neuroinformatics.

[68]  Bruce Fischl,et al.  Volumetric navigators for prospective motion correction and selective reacquisition in neuroanatomical MRI , 2012, Magnetic resonance in medicine.

[69]  Qian Luo,et al.  Automated Quality Assessment of Structural Magnetic Resonance Brain Images Based on a Supervised Machine Learning Algorithm , 2016, Front. Neuroinform..

[70]  Xi-Nian Zuo,et al.  A Connectome Computation System for discovery science of brain , 2015 .

[71]  Timothy O. Laumann,et al.  Data Quality Influences Observed Links Between Functional Connectivity and Behavior , 2017, Cerebral cortex.

[72]  Mark A. Elliott,et al.  The Philadelphia Neurodevelopmental Cohort: A publicly available resource for the study of normal and abnormal brain development in youth , 2016, NeuroImage.

[73]  Jessica A. Turner,et al.  Exploration of scanning effects in multi-site structural MRI studies , 2014, Journal of Neuroscience Methods.

[74]  Brian B. Avants,et al.  N4ITK: Improved N3 Bias Correction , 2010, IEEE Transactions on Medical Imaging.

[75]  Efstathios D. Gennatas,et al.  Age-Related Effects and Sex Differences in Gray Matter Density, Volume, Mass, and Cortical Thickness from Childhood to Young Adulthood , 2017, The Journal of Neuroscience.

[76]  David Atkinson,et al.  Automatic correction of motion artifacts in magnetic resonance images using an entropy focus criterion , 1997, IEEE Transactions on Medical Imaging.

[77]  M. Dylan Tisdall,et al.  Prospective motion correction with volumetric navigators (vNavs) reduces the bias and variance in brain morphometry induced by subject motion , 2016, NeuroImage.

[78]  J. Giedd,et al.  Brain development in children and adolescents: Insights from anatomical magnetic resonance imaging , 2006, Neuroscience & Biobehavioral Reviews.

[79]  Mark A. Elliott,et al.  Impact of in-scanner head motion on multiple measures of functional connectivity: Relevance for studies of neurodevelopment in youth , 2012, NeuroImage.

[80]  Jean-Philippe Thiran,et al.  Automatic quality assessment in structural brain magnetic resonance imaging , 2009, Magnetic resonance in medicine.