Development and validation of a brain maturation index using longitudinal neuroanatomical scans

NeuroImage

Volumn 117, Issue , 2015, Pages 311-318

  Cao, Bo ^a   Mwangi, Benson ^a   Hasan, Khader M ^a   Selvaraj, Sudhakar ^a   Zeni, Cristian P ^a   Zunta Soares, Giovana B ^a   Soares, Jair C ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Brain maturation index; Longitudinal brain imaging; Machine learning; Neurodevelopmental trajectories; Neuroimaging

Indexed keywords

ADULT; AGE; ARTICLE; BRAIN MATURATION; BRAIN MATURATION INDEX; BRAIN SIZE; CAUDATE NUCLEUS; CHILD; CINGULATE GYRUS; CONTROLLED STUDY; DIENCEPHALON; FEMALE; GLOBUS PALLIDUS; GRAY MATTER; HUMAN; IMAGE ANALYSIS; ISTHMUS CINGULATE; LATERAL BRAIN VENTRICLE; LEFT HEMISPHERE; MALE; MEASUREMENT ACCURACY; MEASUREMENT ERROR; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PRECUNEUS; PREDICTIVE VALUE; PRIORITY JOURNAL; PUTAMEN; RIGHT HEMISPHERE; VALIDATION PROCESS; ADOLESCENT; ANATOMY AND HISTOLOGY; BRAIN; GROWTH, DEVELOPMENT AND AGING; HEALTH STATUS INDICATOR; LONGITUDINAL STUDY; MACHINE LEARNING; PRESCHOOL CHILD; PROCEDURES; VALIDATION STUDY;

ADOLESCENT; BRAIN; CHILD; CHILD, PRESCHOOL; FEMALE; HEALTH STATUS INDICATORS; HUMANS; LONGITUDINAL STUDIES; MACHINE LEARNING; MAGNETIC RESONANCE IMAGING; MALE;

EID: 84936863475     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.05.071     Document Type: Article

References (60)

1. Ashburner J., Friston K.J. Voxel-based morphometry-the methods. NeuroImage 2000, 11:805-821. 10.1006/nimg.2000.0582.
2. Ashburner J., Csernansky J.G., Davatzikos C., Fox N.C., Frisoni G.B., Thompson P.M. Computer-assisted imaging to assess brain structure in healthy and diseased brains. Lancet Neurol. 2003, 10.1016/S1474-4422(03)00304-1.
3. Brown T.T., Kuperman J.M., Chung Y., Erhart M., McCabe C., Hagler D.J., Dale A.M. Neuroanatomical assessment of biological maturity. Curr. Biol. 2012, 22:1693-1698. 10.1016/j.cub.2012.07.002.
4. Casey B.J., Giedd J.N., Thomas K.M. Structural and functional brain development and its relation to cognitive development. Biol. Psychol. 2000, 54:241-257. 10.1016/s0301-0511(00)00058-2.
5. Chen C.H., Ridler K., Suckling J., Williams S., Fu C.H.Y., Merlo-Pich E., Bullmore E. Brain imaging correlates of depressive symptom severity and predictors of symptom improvement after antidepressant treatment. Biol. Psychiatry 2007, 62:407-414. 10.1016/j.biopsych.2006.09.018.
6. Dale A.M., Sereno M.I. Improved localizadon of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach. J. Cogn. Neurosci. 1993, 10.1162/jocn.1993.5.2.162.
7. Dale A.M., Fischl B., Sereno M.I. Cortical surface-based analysis I. Segmentation and surface reconstruction. NeuroImage 1999, 9:179-194. 10.1006/nimg.1998.0395.
8. Desikan R.S., Ségonne F., Fischl B., Quinn B.T., Dickerson B.C., Blacker D., Killiany R.J. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 2006, 31:968-980. 10.1016/j.neuroimage.2006.01.021.
9. Dosenbach N.U.F., Nardos B., Cohen A.L., Fair D.A., Power J.D., Church J.A., Schlaggar B.L. Prediction of individual brain maturity using fMRI. Science (New York, N.Y.) 2010, 329:1358-1361. 10.1126/science.1194144.
10. Douaud G., MacKay C., Andersson J., James S., Quested D., Ray M.K., James A. Schizophrenia delays and alters maturation of the brain in adolescence. Brain 2009, 132:2437-2448. 10.1093/brain/awp126.
11. Erus G., Battapady H., Satterthwaite T.D., Hakonarson H., Gur R.E., Davatzikos C., Gur R.C. Imaging Patterns of Brain Development and their Relationship to Cognition. Cereb. Cortex 2014, New York, N.Y.: 1991. 10.1093/cercor/bht425.
12. Evans A.C. The NIH MRI study of normal brain development. NeuroImage 2006, 30:184-202. 10.1016/j.neuroimage.2005.09.068.
13. Fedorov A., Beichel R., Kalpathy-Cramer J., Finet J., Fillion-Robin J.C., Pujol S., Kikinis R. 3D slicer as an image computing platform for the Quantitative Imaging Network. Magn. Reson. Imaging 2012, 30:1323-1341. 10.1016/j.mri.2012.05.001.
14. Fischl B., Dale A.M. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:11050-11055. 10.1073/pnas.200033797.
15. Fischl B., Sereno M.I., Dale A.M. Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. NeuroImage 1999, 9:195-207. 10.1006/nimg.1998.0396.
16. Fischl B., Sereno M.I., Tootell R.B.H., Dale A.M. High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum. Brain Mapp. 1999, 8:272-284. 10.1002/(SICI)1097-0193(1999)8:4<272:AID-HBM10>3.0.CO;2-4.
17. Fischl B., Liu A., Dale A.M. Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans. Med. Imaging 2001, 20:70-80. 10.1109/42.906426.
18. Fischl B., Salat D.H., Busa E., Albert M., Dieterich M., Haselgrove C., Dale A.M. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002, 33:341-355. 10.1016/S0896-6273(02)00569-X.
19. Fischl B., Salat D.H., Van Der Kouwe A.J.W., Makris N., Ségonne F., Quinn B.T., Dale A.M. Sequence-independent segmentation of magnetic resonance images. NeuroImage 2004, 23. 10.1016/j.neuroimage.2004.07.016.
20. Fischl B., Van Der Kouwe A., Destrieux C., Halgren E., Ségonne F., Salat D.H., Dale A.M. Automatically parcellating the human cerebral cortex. Cereb. Cortex 2004, 14:11-22. 10.1093/cercor/bhg087.
21. Franke K., Gaser C. Longitudinal changes in individual BrainAGE in healthy aging, mild cognitive impairment, and Alzheimer's disease. GeroPsych. J. Gerontopsychology Geriatr. Psychiatry 2012, 25(4):235-245. 10.1024/1662-9647/a000074.
22. Franke K., Ziegler G., Klöppel S., Gaser C. Estimating the age of healthy subjects from T1-weighted MRI scans using kernel methods: exploring the influence of various parameters. NeuroImage 2010, 50:883-892. 10.1016/j.neuroimage.2010.01.005.
23. Franke K., Luders E., May A., Wilke M., Gaser C. Brain maturation: predicting individual BrainAGE in children and adolescents using structural MRI. NeuroImage 2012, 63:1305-1312. 10.1016/j.neuroimage.2012.08.001.
24. Friedman J., Hastie T., Tibshirani R. Regularization paths for generalized linear models via coordinate descent. J. Stat. Softw. 2010, 33:1-22. 10.1359/JBMR.0301229.
25. Gaser C., Franke K., Klöppel S., Koutsouleris N., Sauer H. BrainAGE in mild cognitive impaired patients: predicting the conversion to Alzheimer's disease. PLoS One 2013, 8. 10.1371/journal.pone.0067346.
26. Giedd J.N., Rapoport J.L. Structural MRI of pediatric brain development: what have we learned and where are we going?. Neuron 2010, 10.1016/j.neuron.2010.08.040.
27. Giedd J.N., Blumenthal J., Jeffries N.O., Castellanos F.X., Liu H., Zijdenbos A., Rapoport J.L. Brain development during childhood and adolescence: a longitudinal MRI study. Nat. Neurosci. 1999, 2:861-863. 10.1038/13158.
28. Giedd J.N., Lalonde F.M., Celano M.J., White S.L., Wallace G.L., Lee N.R., Lenroot R.K. Anatomical brain magnetic resonance imaging of typically developing children and adolescents. J. Am. Acad. Child Adolesc. Psychiatry 2009, 48:465-470. 10.1097/CHI.0b013e31819f2715.
29. Giedd J.N., Raznahan A., Alexander-Bloch A., Schmitt E., Gogtay N., Rapoport J.L. Child Psychiatry Branch of the National Institute of Mental Health longitudinal structural magnetic resonance imaging study of human brain development. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 2014, 1-7. 10.1038/npp.2014.236.
30. Gogtay N., Giedd J.N., Lusk L., Hayashi K.M., Greenstein D., Vaituzis A.C., Thompson P.M. Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:8174-8179. 10.1073/pnas.0402680101.
31. Gur R.C., Calkins M.E., Satterthwaite T.D., Ruparel K., Bilker W.B., Moore T.M., Gur R.E. Neurocognitive growth charting in psychosis spectrum youths. JAMA Psychiatry 2014, 71:366-374. 10.1001/jamapsychiatry.2013.4190.
32. Han X., Jovicich J., Salat D., van der Kouwe A., Quinn B., Czanner S., Fischl B. Reliability of MRI-derived measurements of human cerebral cortical thickness: the effects of field strength, scanner upgrade and manufacturer. NeuroImage 2006, 32:180-194. 10.1016/j.neuroimage.2006.02.051.
33. Hendren R.L., De Backer I., Pandina G.J. Review of neuroimaging studies of child and adolescent psychiatric disorders from the past 10years. J. Am. Acad. Child Adolesc. Psychiatry 2000, 39:815-828. 10.1097/00004583-200007000-00010.
34. Jovicich J., Czanner S., Greve D., Haley E., Van Der Kouwe A., Gollub R., Dale A. Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data. NeuroImage 2006, 30:436-443. 10.1016/j.neuroimage.2005.09.046.
35. Kessler R.C., Berglund P., Demler O., Jin R., Merikangas K.R., Walters E.E. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch. Gen. Psychiatry 2005, 62:593-602. 10.1001/archpsyc.62.6.593.
36. Khundrakpam B.S., Tohka J., Evans A.C. Prediction of brain maturity based on cortical thickness at different spatial resolutions. NeuroImage 2015, 111:350-359. 10.1016/j.neuroimage.2015.02.046.
37. Lenroot R.K., Giedd J.N. Brain development in children and adolescents: Insights from anatomical magnetic resonance imaging. Neurosci. Biobehav. Rev. 2006, 10.1016/j.neubiorev.2006.06.001.
38. Lenroot R.K., Gogtay N., Greenstein D.K., Wells E.M., Wallace G.L., Clasen L.S., Giedd J.N. Sexual dimorphism of brain developmental trajectories during childhood and adolescence. NeuroImage 2007, 36:1065-1073. 10.1016/j.neuroimage.2007.03.053.
39. Matsuzawa J., Matsui M., Konishi T., Noguchi K., Gur R.C., Bilker W., Miyawaki T. Age-related volumetric changes of brain gray and white matter in healthy infants and children. Cereb. Cortex 2001, 11(4):335-342. 10.1093/cercor/11.4.335.
40. Mwangi B., Hasan K.M., Soares J.C. Prediction of individual subject's age across the human lifespan using diffusion tensor imaging: a machine learning approach. NeuroImage 2013, 75:58-67. 10.1016/j.neuroimage.2013.02.055.
41. Mwangi B., Tian T.S., Soares J.C. A review of feature reduction techniques in neuroimaging. Neuroinformatics 2014, 10.1007/s12021-013-9204-3.
42. Olkin I., Finn J.D. Psychol. Bull. 1995, 118(1):155-164. 10.1037/0033-2909.118.1.155.
43. Paus T. Mapping brain maturation and cognitive development during adolescence. Trends Cogn. Sci. 2005, 9:60-68. 10.1016/j.tics.2004.12.008.
44. Paus T., Zijdenbos A., Worsley K., Collins D.L., Blumenthal J., Giedd J.N., Evans A.C. Structural maturation of neural pathways in children and adolescents: in vivo study. Science (New York, N.Y.) 1999, 283:1908-1911. 10.1126/science.283.5409.1908.
45. Qian J., Hastie T., Friedman J., Tibshirani R., Simon N. Glmnet for Matlab (2013) http://www.stanford.edu/~hastie/glmnet_matlab/.
46. Rapoport J.L., Addington A.M., Frangou S., Psych M.R.C. The neurodevelopmental model of schizophrenia: update 2005. Mol. Psychiatry 2005, 10:434-449. 10.1038/sj.mp.4001673.
47. Raznahan A., Shaw P., Lalonde F., Stockman M., Wallace G.L., Greenstein D., Giedd J.N. How does your cortex grow?. J. Neurosci.: The Official Journal of the Society for Neuroscience 2011, 31:7174-7177. 10.1523/JNEUROSCI.0054-11.2011.
48. Rosset S., Zhu J. Piecewise linear regularized solution paths. Ann. Stat. 2007, 35:1012-1030. 10.1214/009053606000001370.
49. Roybal D.J., Singh M.K., Cosgrove V.E., Howe M., Kelley R., Barnea-Goraly N., Chang K.D. Biological evidence for a neurodevelopmental model of pediatric bipolar disorder. Isr. J. Psychiatry Relat. Sci. 2012, 49:28-43.
50. Ségonne F., Dale A.M., Busa E., Glessner M., Salat D., Hahn H.K., Fischl B. A hybrid approach to the skull stripping problem in MRI. NeuroImage 2004, 22:1060-1075. 10.1016/j.neuroimage.2004.03.032.
51. Shaw P., Eckstrand K., Sharp W., Blumenthal J., Lerch J.P., Greenstein D., Rapoport J.L. Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:19649-19654. 10.1073/pnas.0707741104.
52. Shaw P., Malek M., Watson B., Sharp W., Evans A., Greenstein D. Development of cortical surface area and gyrification in attention-deficit/hyperactivity disorder. Biol. Psychiatry 2012, 72:191-197. 10.1016/j.biopsych.2012.01.031.
53. Sowell E.R., Trauner D.A., Gamst A., Jernigan T.L. Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study. Dev. Med. Child Neurol. 2002, 44:4-16. 10.1111/j.1469-8749.2002.tb00253.x.
54. Thompson P.M., Sowell E.R., Gogtay N., Giedd J.N., Vidal C.N., Hayashi K.M., Toga A.W. Structural MRI and brain development. International Review of Neurobiology 2005.
55. Tibshirani R. Regression and shrinkage via the Lasso. J. R. Stat. Soc. Ser. B 1996, 58:267-288.
56. Toga A.W., Thompson P.M., Sowell E.R. Mapping brain maturation. Trends Neurosci. 2006, 10.1016/j.tins.2006.01.007.
57. Wang H., Leng C. A note on adaptive group lasso. Comput. Stat. Data Anal. 2008, 52:5277-5286. 10.1016/j.csda.2008.05.006.
58. Whiteford H.A., Degenhardt L., Rehm J., Baxter A.J., Ferrari A.J., Erskine H.E., Vos T. Global burden of disease attributable to mental and substance use disorders: findings from the Global Burden of Disease Study 2010. Lancet 2013, 382:1575-1586. 10.1016/S0140-6736(13)61611-6.
59. Yeo R.A., Hodde-Vargas J., Hendren R.L., Vargas L.A., Brooks W.M., Ford C.C., Hart B.L. Brain abnormalities in schizophrenia-spectrum children: implications for a neurodevelopmental perspective. Psychiatry Res. Neuroimaging 1997, 76:1-13. 10.1016/S0925-4927(97)00056-5.
60. Yuan M., Lin Y. Model selection and estimation in regression with grouped variables. J. R. Stat. Soc. Ser. B Stat Methodol. 2006, 68:49-67. 10.1111/j.1467-9868.2005.00532.x.