The effect of age, diagnosis, and their interaction on vertex-based measures of cortical thickness and surface area in autism spectrum disorder

Journal of Neural Transmission

Volumn 121, Issue 9, 2014, Pages 1157-1170

  Ecker, C ^a   Shahidiani, A ^a   Feng, Y ^a   Daly, E ^a   Murphy, C ^a   D'Almeida, V ^a   Deoni, S ^b   Williams, S C ^a   Gillan, N ^a   Gudbrandsen, M ^a   Wichers, R ^a   Andrews, D ^a   Van Hemert, L ^a   Murphy, D G M ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b Brown University   (United States)

Author keywords

Autism; Cortical thickness; Neuroanatomy; Neurodevelopment; Surface area

Indexed keywords

ADOLESCENT; ADULT; ADULTHOOD; AGE; ANTERIOR CINGULATE; ARTICLE; AUTISM; BRAIN MATURATION; CHILD; CHILDHOOD; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); CROSS-SECTIONAL STUDY; FRONTAL LOBE; GROUP DYNAMICS; HUMAN; IMAGING SOFTWARE; MAJOR CLINICAL STUDY; MALE; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; ORBITAL CORTEX; POSTCENTRAL GYRUS; PREDICTION; PREFRONTAL CORTEX; PRIORITY JOURNAL; REDUCTION; RIGHT HEMISPHERE; SURFACE AREA; SURFACE PROPERTY; TEMPORAL LOBE; AGING; BRAIN CORTEX; GROWTH, DEVELOPMENT AND AGING; IMAGE PROCESSING; NEUROPSYCHOLOGICAL TEST; ORGAN SIZE; PATHOLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; AGING; CEREBRAL CORTEX; CHILD; CHILD DEVELOPMENT DISORDERS, PERVASIVE; CROSS-SECTIONAL STUDIES; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; NEUROPSYCHOLOGICAL TESTS; ORGAN SIZE; YOUNG ADULT;

EID: 84907598540     PISSN: 03009564     EISSN: 14351463     Source Type: Journal    
DOI: 10.1007/s00702-014-1207-1     Document Type: Article

References (57)

1. Amaral DG, Schumann CM, Nordahl CW (2008) Neuroanatomy of autism. Trends Neurosci 31:137-145. doi:10.1016/j.tins.2007.12.005
2. Blakemore S-J (2008) The social brain in adolescence. Nat Rev Neurosci 9:267-277. doi:10.1038/nrn2353
3. Carper RA, Courchesne E (2005) Localized enlargement of the frontal cortex in early autism. Biol Psychiatry 57:126-133. doi:10.1016/j.biopsych.2004. 11.005 (Pubitemid 40094712)
4. Casanova MF, van Kooten IAJ, Switala AE et al (2006) Minicolumnar abnormalities in autism. Acta Neuropathol 112:287-303. doi:10.1007/s00401-006- 0085-5 (Pubitemid 44275884)
5. Castelli F, Frith C, Happé F, Frith U (2002) Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. Brain 125:1839-1849
6. Courchesne E, Pierce K (2005) Brain overgrowth in autism during a critical time in development: implications for frontal pyramidal neuron and interneuron development and connectivity. Int J Dev Neurosci 23:153-170. doi:10.1016/j.ijdevneu.2005.01.003 (Pubitemid 40313549)
7. Courchesne E, Mouton PR, Calhoun ME et al (2011) Neuron number and size in prefrontal cortex of children with autism. JAMA 306:2001-2010. doi:10.1001/jama.2011.1638
8. Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179-194. doi:10.1006/nimg.1998.0395 (Pubitemid 29369874)
9. Doyle-Thomas KAR, Kushki A, Duerden EG et al (2013) The effect of diagnosis, age, and symptom severity on cortical surface area in the cingulate cortex and insula in autism spectrum disorders. J Child Neurol 28:732-739. doi:10.1177/0883073812451496
10. Ecker C, Suckling J, Deoni SC et al (2012) Brain anatomy and its relationship to behavior in adults with autism spectrum disorder: a multicenter magnetic resonance imaging study. Arch Gen Psychiatry 69:195-209. doi:10.1001/archgenpsychiatry.2011.1251
11. Ecker C, Ginestet C, Feng Y et al (2013a) Brain surface anatomy in adults with autism: the relationship between surface area, cortical thickness, and autistic symptoms. JAMA Psychiatry 70:59-70. doi:10.1001/jamapsychiatry.2013.265
12. Ecker C, Ronan L, Feng Y et al (2013b) Intrinsic gray-matter connectivity of the brain in adults with autism spectrum disorder. Proc Natl Acad Sci USA. doi:10.1073/pnas.1221880110
13. Fischl B, Sereno MI, Dale AM (1999a) Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195-207. doi:10.1006/nimg.1998.0396 (Pubitemid 29369875)
14. Fischl B, Sereno MI, Tootell RB, Dale AM (1999b) High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 8:272-284
15. Gaffrey MS, Kleinhans NM, Haist F et al (2007) Atypical [corrected] participation of visual cortex during word processing in autism: an fMRI study of semantic decision. Neuropsychologia 45:1672-1684. doi:10.1016/j. neuropsychologia.2007.01.008 (Pubitemid 46386125)
16. Geschwind DH, Levitt P (2007) Autism spectrum disorders: developmental disconnection syndromes. Curr Opin Neurobiol 17:103-111. doi:10.1016/j.conb. 2007.01.009 (Pubitemid 46237744)
17. Giedd JN, Blumenthal J, Jeffries NO et al (1999) Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 2:861-863. doi:10.1038/13158 (Pubitemid 30602596)
18. Hardan AY, Muddasani S, Vemulapalli M et al (2006) An MRI study of increased cortical thickness in autism. Am J Psychiatry 163:1290-1292. doi:10.1176/appi.ajp.163.7.1290 (Pubitemid 44464463)
19. Hardan AY, Libove RA, Keshavan MS et al (2009) A preliminary longitudinal magnetic resonance imaging study of brain volume and cortical thickness in autism. Biol Psychiatry 66:320-326. doi:10.1016/j.biopsych.2009.04.024
20. Hazlett HC, Poe MD, Gerig G et al (2011) Early brain overgrowth in autism associated with an increase in cortical surface area before age 2 years. Arch Gen Psychiatry 68:467-476. doi:10.1001/ archgenpsychiatry.2011.39
21. Huttenlocher PR, Dabholkar AS (1997) Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 387:167-178 (Pubitemid 27430343)
22. Hyde KL, Samson F, Evans AC, Mottron L (2010) Neuroanatomical differences in brain areas implicated in perceptual and other core features of autism revealed by cortical thickness analysis and voxel-based morphometry. Hum Brain Mapp 31:556-566. doi:10.1002/hbm.20887
23. Langen M, Durston S, Staal WG et al (2007) Caudate nucleus is enlarged in high-functioning medication-naive subjects with autism. Biol Psychiatry 62:262-266. doi:10.1016/j.biopsych.2006.09.040 (Pubitemid 47042019)
24. Langen M, Leemans A, Johnston P et al (2011) Fronto-striatal circuitry and inhibitory control in autism: findings from diffusion tensor imaging tractography. Cortex. doi:10.1016/j.cortex.2011.05.018
25. Lombardo MV, Barnes JL, Wheelwright SJ, Baron-Cohen S (2007) Self-referential cognition and empathy in autism. PLoS One 2:e883. doi:10.1371/journal.pone.0000883
26. Lombardo MV, Chakrabarti B, Bullmore ET et al (2010) Atypical neural self-representation in autism. Brain 133:611-624. doi:10.1093/brain/awp306
27. Lord C, Rutter M, Goode S et al (1989) Autism diagnostic observation schedule: a standardized observation of communicative and social behavior. J Autism Dev Disord 19:185-212 (Pubitemid 19176529)
28. Lord C, Rutter M, Le Couteur A (1994) Autism diagnostic interviewrevised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord 24:659-685 (Pubitemid 24309810)
29. Mak-Fan KM, Taylor MJ, Roberts W, Lerch JP (2011) Measures of cortical grey matter structure and development in children with autism spectrum disorder. J Autism Dev Disord. doi:10.1007/s10803-011-1261-6
30. McAlonan GM, Cheung V, Cheung C et al (2005) Mapping the brain in autism. A voxel-based MRI study of volumetric differences and intercorrelations in autism. Brain 128:268-276. doi:10.1093/brain/awh332 (Pubitemid 40222596)
31. Miyata T, Kawaguchi A, Saito K et al (2004) Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131:3133-3145. doi:10.1242/dev.01173 (Pubitemid 39077437)
32. Mundy P, Gwaltney M, Henderson H (2010) Self-referenced processing, neurodevelopment and joint attention in autism. Autism 14:408-429. doi:10.1177/1362361310366315
33. Noctor SC, Martínez-Cerdeño V, Ivic L, Kriegstein AR (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7:136-144. doi:10.1038/nn1172 (Pubitemid 38129789)
34. Nordahl CW, Scholz R, Yang X et al (2012) Increased rate of amygdala growth in children aged 2 to 4 years with autism spectrum disorders: a longitudinal study. Arch Gen Psychiatry 69:53-61. doi:10.1001/archgenpsychiatry. 2011.145
35. Panizzon MS, Fennema-Notestine C, Eyler LT et al (2009) Distinct genetic influences on cortical surface area and cortical thickness. Cereb Cortex 19:2728-2735. doi:10.1093/cercor/bhp026
36. Patterson K, Nestor PJ, Rogers TT (2007) Where do you know what you know? The representation of semantic knowledge in the human brain. Nat Rev Neurosci 8:976-987. doi:10.1038/nrn2277 (Pubitemid 350146937)
37. Paus T (2005) Mapping brain maturation and cognitive development during adolescence. Trends Cogn Sci (Regul Ed) 9:60-68. doi:10.1016/j.tics.2004.12.008
38. Pessoa L (2008) On the relationship between emotion and cognition. Nat Rev Neurosci 9:148-158. doi:10.1038/nrn2317
39. Pontious A, Kowalczyk T, Englund C, Hevner RF (2008) Role of intermediate progenitor cells in cerebral cortex development. Dev Neurosci 30:24-32. doi:10.1159/000109848 (Pubitemid 350256680)
40. Rakic P (1995) A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci 18:383-388
41. Raznahan A, Toro R, Daly E et al (2010) Cortical anatomy in autism spectrum disorder: an in vivo MRI study on the effect of age. Cereb Cortex 20:1332-1340. doi:10.1093/cercor/bhp198
42. Raznahan A, Shaw P, Lalonde F et al (2011) How does your cortex grow? J Neurosci 31:7174-7177. doi:10.1523/JNEUROSCI.0054-11.2011
43. Redcay E, Courchesne E (2008) Deviant functional magnetic resonance imaging patterns of brain activity to speech in 2-3-year-old children with autism spectrum disorder. Biol Psychiatry 64:589-598. doi:10.1016/j.biopsych. 2008.05.020
44. Scheel C, Rotarska-Jagiela A, Schilbach L et al (2011) Imaging derived cortical thickness reduction in high-functioning autism: key regions and temporal slope. Neuroimage 58:391-400. doi:10.1016/j.neuroimage.2011.06.040
45. Schumann CM, Barnes CC, Lord C, Courchesne E (2009) Amygdala enlargement in toddlers with autism related to severity of social and communication impairments. Biol Psychiatry 66:942-949. doi:10.1016/j.biopsych.2009.07.007
46. Schumann CM, Bloss CS, Barnes CC et al (2010) Longitudinal magnetic resonance imaging study of cortical development through early childhood in autism. J Neurosci 30:4419-4427. doi:10.1523/JNEUROSCI.5714-09.2010
47. Ségonne F, Dale AM, Busa E et al (2004) A hybrid approach to the skull stripping problem in MRI. Neuroimage 22:1060-1075. doi:10.1016/j. neuroimage.2004.03.032 (Pubitemid 38829195)
48. Shaw P, Lerch J, Greenstein D et al (2006) Longitudinal mapping of cortical thickness and clinical outcome in children and adolescents with attention-deficit/hyperactivity disorder. Arch Gen Psychiatry 63:540-549. doi:10.1001/archpsyc.63.5.540
49. Silani G, Bird G, Brindley R et al (2008) Levels of emotional awareness and autism: an fMRI study. Soc Neurosci 3:97-112. doi:10.1080/17470910701577020
50. Waiter GD, Williams JHG, Murray AD et al (2004) A voxel-based investigation of brain structure in male adolescents with autistic spectrum disorder. Neuroimage 22:619-625. doi:10.1016/j.neuroimage.2004.02.029 (Pubitemid 38759424)
51. Wallace GL, Dankner N, Kenworthy L et al (2010) Age-related temporal and parietal cortical thinning in autism spectrum disorders. Brain 133:3745-3754. doi:10.1093/brain/awq279
52. Wallace GL, Robustelli B, Dankner N et al (2013) Increased gyrification, but comparable surface area in adolescents with autism spectrum disorders. Brain 136:1956-1967. doi:10.1093/brain/awt106
53. Wang K, Zhang H, Ma D et al (2009) Common genetic variants on 5p14.1 associate with autism spectrum disorders. Nature 459:528-533. doi:10.1038/nature07999
54. Wechsler D (1999) Wechsler abbreviated scale of intelligence (WASI). Harcourt Assessment, San Antonio
55. Wing L (1997) The autistic spectrum. Lancet 350:1761-1766. doi:10.1016/S0140-6736(97)09218-0
56. Winkler AM, Sabuncu MR, Yeo BTT et al (2012) Measuring and comparing brain cortical surface area and other areal quantities. Neuroimage. doi:10.1016/j.neuroimage.2012.03.026
57. Worsley KJ, Andermann M, Koulis T et al (1999) Detecting changes in nonisotropic images. Hum Brain Mapp 8:98-101 (Pubitemid 29480295)