Longitudinal Volumetric Brain Changes in Autism Spectrum Disorder Ages 6-35 Years

Autism Research

Volumn 8, Issue 1, 2015, Pages 82-93

  Lange, Nicholas ^a,b   Travers, Brittany G ^c   Bigler, Erin D ^d   Prigge, Molly B D ^e,f   Froehlich, Alyson L ^g   Nielsen, Jared A ^f   Cariello, Annahir N ^g   Zielinski, Brandon A ^e,f   Anderson, Jeffrey S ^f   Fletcher, P Thomas ^g,h   Alexander, Andrew A ^c,i   Lainhart, Janet E ^c,i  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MCLEAN HOSPITAL   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d BRIGHAM YOUNG UNIVERSITY   (United States)

^e PRIMARY CHILDREN'S MEDICAL CENTER   (United States)

^f UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF UTAH   (United States)

^h Department of Electrical and Computer Engineering   (United States)

ⁱ UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Adolescents; Adults; Children; Growth curve; Mixed effects; MRI; Variance

Indexed keywords

ADOLESCENT; ARTICLE; AUTISM; BODY MASS; BRAIN DEVELOPMENT; BRAIN REGION; BRAIN SIZE; BRAIN VENTRICLE; CAUDATE NUCLEUS; CEREBELLUM; CONTROLLED STUDY; CORPUS CALLOSUM; FOLLOW UP; GRAY MATTER; HUMAN; MAJOR CLINICAL STUDY; MALE; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; RIGHT HANDEDNESS; SEX DIFFERENCE; THALAMUS; WHITE MATTER; ADULT; AGE; BRAIN; BRAIN MAPPING; CHILD; CHILD DEVELOPMENT; LONGITUDINAL STUDY; ORGAN SIZE; PATHOLOGY; PROCEDURES; YOUNG ADULT;

ADOLESCENT; ADULT; AGE FACTORS; AUTISM SPECTRUM DISORDER; BRAIN; BRAIN MAPPING; CHILD; CHILD DEVELOPMENT; FOLLOW-UP STUDIES; HUMANS; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; ORGAN SIZE; YOUNG ADULT;

EID: 84923522624     PISSN: 19393792     EISSN: 19393806     Source Type: Journal    
DOI: 10.1002/aur.1427     Document Type: Article

References (64)

1. Akaike, H. (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control, 19, 716-723.
2. American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders: DSM-IV (4th ed.). Washington, DC: American Psychiatric Association.
3. Barnea-Goraly, N., Frazier, T.W., Piacenza, L., Minshew, N.J., Keshavan, M.S., etal. (2013). A preliminary longitudinal volumetric MRI study of amygdala and hippocampal volumes in autism. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 48C, 124-128. doi:10.1016/j.pnpbp.2013.09.010
4. Brain Development Cooperative Group, & Lange, N. (2012). Total and regional brain volumes in a population-based normative sample from 4 to 18 years: The NIH MRI Study of Normal Brain Development. Cerebral Cortex, 22, 1-12.
5. Buxhoeveden, D.P., Semendeferi, K., Buckwalter, J., Schenker, N., Switzer, R., & Courchesne, E. (2006). Reduced minicolumns in the frontal cortex of patients with autism. Neuropathology and Applied Neurobiology, 32, 483-491.
6. Carper, R.A., Moses, P., Tigue, Z.D., & Courchesne, E. (2002). Cerebral lobes in autism: Early hyperplasia and abnormal age effects. Neuroimage, 16, 1038-1051.
7. Casanova, M.F., Buxhoeveden, D.P., Switala, A.E., & Roy, E. (2002). Minicolumnar pathology in autism. Neurology, 58, 428-432.
8. Courchesne, E., Campbell, K., & Solso, S. (2011). Brain growth across the life span in autism: Age-specific changes in anatomical pathology. Brain Research, 1380, 138-145. doi:10.1016/j.brainres.2010.09.101
9. Courchesne, E., Karns, C.M., Davis, H.R., Ziccardi, R., Carper, R.A., etal. (2001). Unusual brain growth patterns in early life in patients with autistic disorder: An MRI study. Neurology, 57, 245-254.
10. Courchesne, E., Pierce, K., Schumann, C.M., Redcay, E., Buckwalter, J.A., etal. (2007). Mapping early brain development in autism. Neuron, 56, 399-413. doi:10.1016/j.neuron.2007.10.016
11. Di Martino, A., Yan, C.-G., Li, Q., Denio, E., Castellanos, F.X., etal. (2013). The autism brain imaging data exchange: Towards a large-scale evaluation of the intrinsic brain architecture in autism. Molecular Psychiatry, 2013, 1-9. doi:10.1038/mp.2013.78
12. Ecker, C., Suckling, J., Deoni, S.C., Lombardo, M.V., Bullmore, E.T., etal. (2012). Brain anatomy and its relationship to behavior in adults with autism spectrum disorder: A multicenter magnetic resonance imaging study. Archives of General Psychiatry, 69, 195-209. doi:10.1001/archgenpsychiatry.2011.1251
13. Fischl, B., Salat, D.H., Busa, E., Albert, M., Dieterich, M., etal. (2002). Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron, 33, 341-355.
14. Fischl, B., van der Kouwe, A., Destrieux, C., Halgren, E., Ségonne, F., etal. (2004). Automatically parcellating the human cerebral cortex. Cerebral Cortex, 14, 11-22.
15. Frazier, T.W., Keshavan, M.S., Minshew, N.J., & Hardan, A.Y. (2012). A two-year longitudinal MRI study of the corpus callosum in autism. Journal of Autism and Developmental Disorders, 42, 2312-2322. doi:10.1007/s10803-012-1478-z
16. Giedd, J.N., Blumenthal, J., Jeffries, N.O., Castellanos, F.X., Liu, H., etal. (1999). Brain development during childhood and adolescence: A longitudinal MRI study. Nature Neuroscience, 2, 861-863.
17. Giedd, J.N., & Rapoport, J.L. (2010). Structural MRI of pediatric brain development: What have we learned and where are we going? Neuron, 67, 728-734. doi:10.1016/j.neuron.2010.08.040
18. Giedd, J.N., Snell, J.W., Lange, N., Rajapakse, J.C., Casey, B.J., etal. (1996). Quantitative magnetic resonance imaging of human brain development: Ages 4-18. Cerebral Cortex, 6, 551-560.
19. Gronenschild, E.H., Habets, P., Jacobs, H.I., Mengelers, R., Rozendaal, N., etal. (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
20. Hardan, A.Y., Libove, R.A., Keshavan, M.S., Melhem, N.M., & Minshew, N.J. (2009). A preliminary longitudinal magnetic resonance imaging study of brain volume and cortical thickness in autism. Biological Psychiatry, 66, 320-326. doi:10.1016/j.biopsych.2009.04.024
21. Harezlak, J., Ryan, L.M., Giedd, J.N., & Lange, N. (2005). Individual and population penalized regression splines for accelerated longitudinal designs. Biometrics, 61, 1037-1048. doi:10.1111/j.1541-0420.2005.00376.x
22. Hazlett, H.C., Poe, M., Gerig, G., Smith, R.G., Provenzale, J., etal. (2005). Magnetic resonance imaging and head circumference study of brain size in autism: Birth through age 2 years. Archives of General Psychiatry, 62, 1366-1376.
23. Howlin, P. (2013). Social disadvantage and exclusion: Adults with autism lag far behind in employment prospects. Journal of the American Academy of Child and Adolescent Psychiatry, 52, 897-899. doi:10.1016/j.jaac.2013.06.010
24. Hua, X., Thompson, P.M., Leow, A.D., Madsen, S.K., Caplan, R., etal. (2013). Brain growth rate abnormalities visualized in adolescents with autism. Human Brain Mapping, 34, 425-436. doi:10.1002/hbm.21441
25. Jou, R.J., Frazier, T.W., Keshavan, M.S., Minshew, N.J., & Hardan, A.Y. (2013). A two-year longitudinal pilot MRI study of the brainstem in autism. Behavioural Brain Research, 251, 163-167. doi:10.1016/j.bbr.2013.04.021
26. Kanner, L. (1971). Follow-up study of eleven autistic children originally reported in 1943. Journal of Autism and Childhood Schizophrenia, 1, 119-145.
27. Kuzawa, C.W., Grossman, L.I., Lipovich, L., Muzik, O., Hof, P.R., etal. (2014). Energetic costs and evolutionary implications of human brain development. Proceedings of the National Academy of Sciences of the United States of America, 111, 13010-13015. doi: 10.1073/pnas.1323099111
28. Lainhart, J.E., Bigler, E.D., Bocian, M., Coon, H., Dinh, E., etal. (2006). Head circumference and height in autism: A study by the Collaborative Program of Excellence in Autism. American Journal of Medical Genetics. Part A, 140, 2257-2274.
29. Laird, N.M., & Ware, J.H. (1982). Random-effects models for longitudinal data. Biometrics, 38, 963-974.
30. Lange, N., Froimowitz, M.P., Bigler, E.D., Lainhart, J.E., & Brain Development Cooperative Group. (2010). Associations between IQ, total and regional brain volumes, and demography in a large normative sample of healthy children and adolescents. Developmental Neuropsychology, 35, 296-317. doi:10.1080/87565641003696833
31. Lange, N., Giedd, J.N., Castellanos, F.X., Vaituzis, A.C., & Rapoport, J.L. (1997). Variability of human brain structure size: Ages 4-20 years. Psychiatry Research: Neuroimaging, 74, 1-12.
32. Lange, N., & Laird, N.M. (1989). The effect of covariance structure on variance estimation in balanced growth curve models with random parameters. Journal of the American Statistical Association, 1989, 241-247.
33. Lange, N., & Ryan, L. (1989). Assessing normality in random effects models. Annals of Statistics, 17, 624-642.
34. Langen, M., Bos, D., Noordermeer, S.D.S., Nederveen, H., van Engeland, H., & Durston, S. (2014). Changes in the development of striatum are involved in repetitive behavior in autism. Biol Psychiatry, 76, 405-411. doi:10.1016/j.biopsych.2013.08.013
35. Lenroot, R.K., Gogtay, N., Greenstein, D.K., Wells, E.M., Wallace, G.L., etal. (2007). Sexual dimorphism of brain developmental trajectories during childhood and adolescence. Neuroimage, 36, 1065-1073. doi:10.1016/j.neuroimage.2007.03.053
36. Leyfer, O.T., Folstein, S.E., Bacalman, S., Davis, N.O., Dinh, E., etal. (2006). Comorbid psychiatric disorders in children with autism: Interview development and rates of disorders. Journal of Autism and Developmental Disorders, 36, 849-861.
37. Lord, C., Risi, S., Lambrecht, L., Cook, E.H. Jr., Leventhal, B.L., etal. (2000). The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30, 205-223.
38. Lord, M., Rutter, A., & LeCouteur, A. (1994). Autism diagnostic interview-revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24, 659-685.
39. Luders, E., Narr, K.L., Thompson, P.M., & Toga, A.W. (2009). Neuroanatomical correlates of intelligence. Intelligence, 37, 156-163. doi:10.1016/j.intell.2008.07.002
40. Nordahl, C.W., Lange, N., Li, D.D., Barnett, L.A., Lee, A., etal. (2011). Brain enlargement is associated with regression in preschool-age boys with autism spectrum disorders. Proceedings of the National Academy of Sciences of the United States of America, 108, 20195-20200. doi:10.1073/pnas.1107560108
41. Oldfield, R.C. (1971). The assessment and analysis of handedness: The Edinburgh Inventory. Neuropsychologia, 9, 97-113.
42. Paus, T. (2005). Mapping brain maturation and cognitive development during adolescence. Trends in Cognitive Sciences, 9, 60-68.
43. R Core Team. (2013). R: A Language and Environment for Statistical Computing. Vienna, Austria. Retrieved from http://www.R-project.org
44. Raznahan, A., Toro, R., Daly, E., Robertson, D., Murphy, C., etal. (2010). Cortical anatomy in autism spectrum disorder: An in vivo MRI study on the effect of age. Cerebral Cortex, 20, 1332-1340. doi:10.1093/cercor/bhp198
45. Reuter, M., Schmansky, N.J., Rosas, H.D., & Fischl, B. (2012). Within-subject template estimation for unbiased longitudinal image analysis. Neuroimage, 61, 1402-1418. doi:10.1016/j.neuroimage.2012.02.084
46. Rutter, M., Kim-Cohen, J., & Maughan, B. (2006). Continuities and discontinuities in psychopathology between childhood and adult life. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 47, 276-295. doi:10.1111/j.1469-7610.2006.01614.x
47. Saito, N., Sakai, O., Ozonoff, A., & Jara, H. (2009). Relaxo-volumetric multispectral quantitative magnetic resonance imaging of the brain over the human lifespan: Global and regional aging patterns. Magnetic Resonance Imaging, 27, 895-906. doi:10.1016/j.mri.2009.05.006; Epub 2009 June 10, PubMed PMID: 19520539.
48. Schumann, C.M., Bloss, C.S., Barnes, C.C., Wideman, G.M., Carper, R.A., etal. (2010). Longitudinal magnetic resonance imaging study of cortical development through early childhood in autism. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 30, 4419-4427. doi:10.1523/JNEUROSCI.5714-09.2010
49. Shaw, P., Greenstein, D., Lerch, J., Clasen, L., Lenroot, R., etal. (2006). Intellectual ability and cortical development in children and adolescents. Nature, 440, 676-679. doi:10.1038/nature04513
50. Snedecor, G.W., & Cochran, W.G. (1989). Statistical methods (8th ed.). Ames, IA: Blackwell Publishing.
51. Sowell, E.R., Trauner, D.A., Gamst, A., & Jernigan, T.L. (2002). Development of cortical and subcortical brain structures in childhood and adolescence: A structural MRI study. Developmental Medicine and Child Neurology, 44, 4-16.
52. Sparks, B.F., Friedman, S.D., Shaw, D.W., Aylward, E.H., Echelard, D., etal. (2002). Brain structural abnormalities in young children with autism spectrum disorder. Neurology, 59, 184-192.
53. Stanfield, A.C., McIntosh, A.M., Spencer, M.D., Philip, R., Gaur, S., & Lawrie, S.M. (2008). Towards a neuroanatomy of autism: A systematic review and meta-analysis of structural magnetic resonance imaging studies. European Psychiatry, 23, 289-299. doi:10.1016/j.eurpsy.2007.05.006
54. Stoner, R., Chow, M.L., Boyle, M.P., Sunkin, S.M., Mouton, P.R., etal. (2014). Patches of disorganization in the neocortex of children with autism. New England Journal of Medicine, 370, 1209-1219. doi:10.1056/NEJMoa1307491
55. Taylor, J.L., & Seltzer, M.M. (2010). Changes in the autism behavioral phenotype during the transition to adulthood. Journal of Autism and Developmental Disorders, 40, 1431-1446. doi:10.1007/s10803-010-1005-z
56. Tiemeier, H., Lenroot, R.K., Greenstein, D.K., Tran, L., Pierson, R., & Giedd, J.N. (2010). Cerebellum development during childhood and adolescence: A longitudinal morphometric MRI study. Neuroimage, 49, 63-70. doi:10.1016/j.neuroimage.2009.08.016
57. Trefethen, L.N., & Bau, D. (1997). Numerical linear algebra. Philadelphia, PA: Society for Industrial and Applied Mathematics.
58. Venables, W.N., & Ripley, B.D. (2002). Modern applied statistics with S. New York: Springer-Verlag.
59. Wallace, G.L., Dankner, N., Kenworthy, L., Giedd, J.N., & Martin, A. (2010). Age-related temporal and parietal cortical thinning in autism spectrum disorders. Brain: A Journal of Neurology, 133, 3745-3754. doi:10.1093/brain/awq279
60. Wechsler, D. (1991). Wechsler intelligence scale for children (WISC-III) (3rd ed.). San Antonio, TX: The Psychological Corporation.
61. Wechsler, D. (1997). Wechsler adult intelligence scale (WAIS-III) (3rd ed.). San Antonio, TX: The Psychological Corporation.
62. Westlye, L.T., Walhovd, K.B., Dale, A.M., Bjørnerud, A., Due-Tønnessen, P., etal. (2010). Differentiating maturational and aging-related changes of the cerebral cortex by use of thickness and signal intensity. Neuroimage, 52, 172-185. doi:10.1016/j.neuroimage.2010.03.056; Epub 2010 March 27, PubMed PMID: 20347997.
63. Willett, J.B., Singer, J.D., & Martin, N.C. (1998). The design and analysis of longitudinal studies of development and psychopathology in context: Statistical models and methodological recommendations. Development and Psychopathology, 10, 395-426.
64. Zielinski, B.A., Gennatas, E.D., Zhou, J., & Seeley, W.W. (2010). Network-level structural covariance in the developing brain. Proceedings of the National Academy of Sciences, 107, 18191-18196. doi:10.1073/pnas.1003109107