Neuroimaging in autism-from basic science to translational research

Nature Reviews Neurology

Volumn 10, Issue 2, 2014, Pages 82-91

  Ecker, Christine ^a   Murphy, Declan ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; AUTISTIC DISORDER; HUMANS; NEUROIMAGING; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84893830237     PISSN: 17594758     EISSN: 17594766     Source Type: Journal    
DOI: 10.1038/nrneurol.2013.276     Document Type: Review

References (97)

1. Wing, L. The autistic spectrum. Lancet 350, 1761-1766 (1997). (Pubitemid 28036684)
2. Abrahams, B. S. & Geschwind, D. H. Advances in autism genetics: on the threshold of a new neurobiology. Nat. Rev. Genet. 9, 341-355 (2008). (Pubitemid 351556064)
3. Ecker, C. et al. 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 (2012).
4. Amaral, D. G., Schumann, C. M. & Nordahl, C. W. Neuroanatomy of autism. Trends Neurosci. 31, 137-145 (2008).
5. Lombardo, M. V., Chakrabarti, B., Bullmore, E. T., MRC AIMS Consortium & Baron-Cohen, S. Specialization of right temporo-parietal junction for mentalizing and its relation to social impairments in autism. Neuroimage 56, 1832-1838 (2011).
6. Langen, M., Durston, S., Staal, W. G., Palmen, S. J. & van Engeland, H. Caudate nucleus is enlarged in high-functioning medication-naive subjects with autism. Biol. Psychiatry 62, 262-266 (2007). (Pubitemid 47042019)
7. Waiter, G. D. et al. A voxel-based investigation of brain structure in male adolescents with autistic spectrum disorder. Neuroimage 22, 619-625 (2004). (Pubitemid 38759424)
8. Carper, R. A. & Courchesne, E. Localized enlargement of the frontal cortex in early autism. Biol. Psychiatry 57, 126-133 (2005). (Pubitemid 40094712)
9. Courchesne, E. et al. Unusual brain growth patterns in early life in patients with autistic disorder: an MRI study. Neurology 57, 245-254 (2001). (Pubitemid 32667357)
10. Ecker, C., Spooren, W. & Murphy, D. Developing new pharmacotherapies for autism. J. Intern. Med. 274, 308-320 (2013).
11. Williams, K. et al. Selective serotonin reuptake inhibitors (SSRIs) for autism spectrum disorders (ASD). Cochrane Database of Systematic Reviews, Issue 8. Art. No.: CD004677 http://dx.doi.org/10.1002/14651858.CD004677.pub3.
12. Geschwind, D. H. & Levitt, P. Autism spectrum disorders: developmental disconnection syndromes. Curr. Opin. Neurobiol. 17, 103-111 (2007). (Pubitemid 46237744)
13. Belmonte, M. K. et al. Autism and abnormal development of brain connectivity. J. Neurosci. 24, 9228-9231 (2004). (Pubitemid 39426157)
14. McAlonan, G. M. et al. Differential effects on white-matter systems in high-functioning autism and Asperger's syndrome. Psychol. Med. 39, 1885-1893 (2009).
15. Pugliese, L. et al. The anatomy of extended limbic pathways in Asperger syndrome: a preliminary diffusion tensor imaging tractography study. Neuroimage 47, 427-434 (2009).
16. Langen, M. et al. Fronto-striatal circuitry and inhibitory control in autism: findings from diffusion tensor imaging tractography. Cortex 48, 183-193 (2011).
17. Shukla, D. K., Keehn, B. & Müller, R.?A. Tract-specific analyses of diffusion tensor imaging show widespread white matter compromise in autism spectrum disorder. J. Child Psychol. Psychiatry 52, 286-295 (2011).
18. Koshino, H. et al. Functional connectivity in an fMRI working memory task in high-functioning autism. Neuroimage 24, 810-821 (2005). (Pubitemid 40094563)
19. Koshino, H. et al. fMRI investigation of working memory for faces in autism: visual coding and underconnectivity with frontal areas. Cereb. Cortex 18, 289-300 (2008). (Pubitemid 351197787)
20. Lewis, D. A., Melchitzky, D. S. & Burgos, G.?G. Specificity in the functional architecture of primate prefrontal cortex. J. Neurocytol. 31, 265-276 (2002). (Pubitemid 36877375)
21. Melchitzky, D. S., González-Burgos, G., Barrionuevo, G. & Lewis, D. A. Synaptic targets of the intrinsic axon collaterals of supragranular pyramidal neurons in monkey prefrontal cortex. J. Comp. Neurol. 430, 209-221 (2001). (Pubitemid 32052658)
22. Ecker, C. et al. Intrinsic gray-matter connectivity of the brain in adults with autism spectrum disorder. Proc. Natl Acad. Sci. USA 110, 13222-13227 (2013).
23. Griffin, L. D. The intrinsic geometry of the cerebral cortex. J. Theor. Biol. 166, 261-273 (1994). (Pubitemid 24095568)
24. Klöppel, S. et al. Diagnostic neuroimaging across diseases. Neuroimage 61, 457-463 (2011).
25. Schumann, C. M. et al. Longitudinal magnetic resonance imaging study of cortical development through early childhood in autism. J. Neurosci. 30, 4419-4427 (2010).
26. Hazlett, H. C. et al. Early brain overgrowth in autism associated with an increase in cortical surface area before age 2 years. Arch. Gen. Psychiatry 68, 467-476 (2011).
27. Carper, R. A., Moses, P., Tigue, Z. D. & Courchesne, E. Cerebral lobes in autism: early hyperplasia and abnormal age effects. Neuroimage 16, 1038-1051 (2002).
28. Hardan, A. Y., Libove, R. A., Keshavan, M. S., Melhem, N. M. & Minshew, N. J. A preliminary longitudinal magnetic resonance imaging study of brain volume and cortical thickness in autism. Biol. Psychiatry 66, 320-326 (2009).
29. Courchesne, E. Abnormal early brain development in autism. Mol. Psychiatry 7 (Suppl. 2), S21-S23 (2002).
30. Herbert, M. R. Large brains in autism: the challenge of pervasive abnormality. Neuroscientist 11, 417-440 (2005). (Pubitemid 41339228)
31. Ecker, C. et al. Describing the brain in autism in five dimensions-magnetic resonance imaging-assisted diagnosis of autism spectrum disorder using a multiparameter classification approach. J. Neurosci. 30, 10612-10623 (2010).
32. Ecker, C. et al. Investigating the predictive value of whole-brain structural MR scans in autism: a pattern classification approach. Neuroimage 49, 44-56 (2010).
33. Jiao, Y. et al. Predictive models of autism spectrum disorder based on brain regional cortical thickness. Neuroimage 50, 589-599 (2010).
34. Uddin, L. Q. et al. Multivariate searchlight classification of structural magnetic resonance imaging in children and adolescents with autism. Biol. Psychiatry 70, 833-841 (2011).
35. Anderson, J. S. et al. Functional connectivity magnetic resonance imaging classification of autism. Brain 134, 3739-3751 (2011).
36. Ingalhalikar, M., Parker, D., Bloy, L., Roberts, T. P. & Verma, R. Diffusion based abnormality markers of pathology: toward learned diagnostic prediction of ASD. Neuroimage 57, 918-927 (2011).
37. Lange, N. et al. Atypical diffusion tensor hemispheric asymmetry in autism. Autism Res. 3, 350-358 (2010).
38. Coutanche, M. N., Thompson-Schill, S. L. & Schultz, R. T. Multi-voxel pattern analysis of fMRI data predicts clinical symptom severity. Neuroimage 57, 113-123 (2011).
39. Calderoni, S. et al. Female children with autism spectrum disorder: an insight from mass-univariate and pattern classification analyses. Neuroimage 59, 1013-1022 (2012).
40. Corrigan, N. M. et al. Atypical developmental patterns of brain chemistry in children with autism spectrum disorder. JAMA Psychiatry 70, 964-974 (2013).
41. Ecker, C. Autism biomarkers for more efficacious diagnosis. Biomark. Med. 5, 193-195 (2011).
42. Mak-Fan, K. M., Taylor, M. J., Roberts, W. & Lerch, J. P. Measures of cortical grey matter structure and development in children with autism spectrum disorder. J. Autism Dev. Disord. 42, 419-427 (2011).
43. Hardan, A. Y., Muddasani, S., Vemulapalli, M., Keshavan, M. S. & Minshew, N. J. An MRI study of increased cortical thickness in autism. Am. J. Psychiatry 163, 1290-1292 (2006). (Pubitemid 44464463)
44. Scheel, C. et al. Imaging derived cortical thickness reduction in high-functioning autism: key regions and temporal slope. Neuroimage 58, 391-400 (2011).
45. Hyde, K. L., Samson, F., Evans, A. C. & Mottron, L. 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 (2010).
46. Wallace, G. L., Dankner, N., Kenworthy, L., Giedd, J. N. & Martin, A. Age-related temporal and parietal cortical thinning in autism spectrum disorders. Brain 133, 3745-3754 (2010).
47. Lainhart, J. E. et al. Head circumference and height in autism: a study by the Collaborative Program of Excellence in Autism. Am. J. Med. Genet. A 140, 2257-2274 (2006). (Pubitemid 44684952)
48. Ecker, C. et al. Brain surface anatomy in adults with autism: the relationship between surface area, cortical thickness, and autistic symptoms. JAMA Psychiatry 70, 59-70 (2013).
49. Pontious, A., Kowalczyk, T., Englund, C. & Hevner, R. F. Role of intermediate progenitor cells in cerebral cortex development. Dev. Neurosci. 30, 24-32 (2008). (Pubitemid 350256680)
50. Miyata, T. et al. Asymmetric production of surface-dividing and non?surface?dividing cortical progenitor cells. Development 131, 3133-3145 (2004). (Pubitemid 39077437)
51. Noctor, S. C., Martínez-Cerdeño, V., Ivic, L. & Kriegstein, A. R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7, 136-144 (2004). (Pubitemid 38129789)
52. Rakic, P. Defects of neuronal migration and the pathogenesis of cortical malformations. Prog. Brain Res. 73, 15-37 (1988).
53. Joyner, A. H. et al. A common MECP2 haplotype associates with reduced cortical surface area in humans in two independent populations. Proc. Natl Acad. Sci. USA 106, 15483-15488 (2009).
54. Crawley, J. N. Translational animal models of autism and neurodevelopmental disorders. Dialogues Clin. Neurosci. 14, 293-305 (2012).
55. Bailey, A. et al. Autism as a strongly genetic disorder: evidence from a British twin study. Psychol. Med. 25, 63-77 (1995).
56. Hallmayer, J. et al. Genetic heritability and shared environmental factors among twin pairs with autism. Arch. Gen. Psychiatry 68, 1095-1102 (2011).
57. Lichtenstein, P., Carlström, E., Råstam, M., Gillberg, C. & Anckarsäter, H. The genetics of autism spectrum disorders and related neuropsychiatric disorders in childhood. Am. J. Psychiatry 167, 1357-1363 (2010).
58. Betancur, C., Sakurai, T. & Buxbaum, J. D. The emerging role of synaptic cell-adhesion pathways in the pathogenesis of autism spectrum disorders. Trends Neurosci. 32, 402-412 (2009).
59. Betancur, C. Etiological heterogeneity in autism spectrum disorders: more than 100 genetic and genomic disorders and still counting. Brain Res. 1380, 42-77 (2011).
60. Spooren, W., Lindemann, L., Ghosh, A. & Santarelli, L. Synapse dysfunction in autism: a molecular medicine approach to drug discovery in neurodevelopmental disorders. Trends Pharmacol. Sci. 33, 669-684 (2012).
61. Baudouin, S. J. et al. Shared synaptic pathophysiology in syndromic and nonsyndromic rodent models of autism. Science 338, 128-132 (2012).
62. Gilman, S. R. et al. Rare de novo variants associated with autism implicate a large functional network of genes involved in formation and function of synapses. Neuron 70, 898-907 (2011).
63. Dalva, M. B., McClelland, A. C. & Kayser, M. S. Cell adhesion molecules: signalling functions at the synapse. Nat. Rev. Neurosci. 8, 206-220 (2007). (Pubitemid 46294663)
64. Lowery, L. A. & Van Vactor, D. The trip of the tip: understanding the growth cone machinery. Nat. Rev. Mol. Cell Biol. 10, 332-343 (2009).
65. Jamain, S. et al. Mutations of the X?linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat. Genet. 34, 27-29 (2003). (Pubitemid 36548785)
66. Laumonnier, F. et al. X?linked mental retardation and autism are associated with a mutation in the NLGN4 gene, a member of the neuroligin family. Am. J. Hum. Genet. 74, 552-557 (2004). (Pubitemid 38325925)
67. Chih, B., Engelman, H. & Scheiffele, P. Control of excitatory and inhibitory synapse formation by neuroligins. Science 307, 1324-1328 (2005). (Pubitemid 40299984)
68. Graf, E. R., Zhang, X., Jin, S.?X., Linhoff, M. W. & Craig, A. M. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119, 1013-1026 (2004). (Pubitemid 40037614)
69. Rubenstein, J. L. & Merzenich, M. M. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2, 255-267 (2003). (Pubitemid 37345664)
70. Page, L. A. et al. In vivo 1H-magnetic resonance spectroscopy study of amygdala-hippocampal and parietal regions in autism. Am. J. Psychiatry 163, 2189-2192 (2006). (Pubitemid 46114244)
71. Mendez, M. A. et al. The brain GABA-benzodiazepine receptor alpha?5 subtype in autism spectrum disorder: a pilot [11C]Ro15-4513 positron emission tomography study. Neuropharmacology 68, 195-201 (2012).
72. Poliak, S. et al. Juxtaparanodal clustering of Shaker-like K+ channels in myelinated axons depends on Caspr2 and TAG?1. J. Cell Biol. 162, 1149-1160 (2003). (Pubitemid 37174196)
73. Corfas, G., Velardez, M. O., Ko, C.?P., Ratner, N. & Peles, E. Mechanisms and roles of axon-Schwann cell interactions. J. Neurosci. 24, 9250-9260 (2004). (Pubitemid 39426161)
74. Peñagarikano, O. et al. Absence of CNTNAP2 leads to epilepsy, neuronal migration abnormalities, and core autism-related deficits. Cell 147, 235-246 (2011).
75. Tuchman, R. & Rapin, I. Epilepsy in autism. Lancet Neurol. 1, 352-358 (2002). (Pubitemid 37159160)
76. Strauss, K. A. et al. Recessive symptomatic focal epilepsy and mutant contactin-associated protein-like 2. N. Engl. J. Med. 354, 1370-1377 (2006).
77. Peippo, M. M. et al. Pitt-Hopkins syndrome in two patients and further definition of the phenotype. Clin. Dysmorphol. 15, 47-54 (2006). (Pubitemid 44481235)
78. Dennis, E. L. et al. Altered structural brain connectivity in healthy carriers of the autism risk gene, CNTNAP2. Brain Connect. 1, 447-459 (2011).
79. Scott-Van Zeeland, A. A. et al. Altered functional connectivity in frontal lobe circuits is associated with variation in the autism risk gene CNTNAP2. Sci. Transl. Med. 2, 56ra80 (2010).
80. Guilmatre, A., Huguet, G., Delorme, R. & Bourgeron, T. The emerging role of SHANK genes in neuropsychiatric disorders. Dev. Neurobiol. http://dx.doi.org/10.1002/dneu.22128.
81. Renner, M., Specht, C. G. & Triller, A. Molecular dynamics of postsynaptic receptors and scaffold proteins. Curr. Opin. Neurobiol. 18, 532-540 (2008).
82. Durand, C. M. et al. Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Nat. Genet. 39, 25-27 (2007). (Pubitemid 46026497)
83. Durand, C. M. et al. SHANK3 mutations identified in autism lead to modification of dendritic spine morphology via an actin-dependent mechanism. Mol. Psychiatry 17, 71-84 (2012).
84. Peça, J. et al. Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature 472, 437-442 (2011).
85. Anderson, G. M., Horne, W. C., Chatterjee, D. & Cohen, D. J. The hyperserotonemia of autism. Ann. N. Y. Acad. Sci. 600, 331-342 (1990).
86. Hranilovic, D. et al. Hyperserotonemia in adults with autistic disorder. J. Autism Dev. Disord. 37, 1934-1940 (2007). (Pubitemid 47609349)
87. Schain, R. J. & Freedman, D. X. Studies on 5?hydroxyindole metabolism in autistic and other mentally retarded children. J. Pediatr. 58, 315-320 (1961).
88. Chugani, D. C. et al. Developmental changes in brain serotonin synthesis capacity in autistic and nonautistic children. Ann. Neurol. 45, 287-295 (1999). (Pubitemid 29120032)
89. Murphy, D. G. et al. Cortical serotonin 5?HT2A receptor binding and social communication in adults with Asperger's syndrome: an in vivo SPECT study. Am. J. Psychiatry 163, 934-936 (2006). (Pubitemid 44464547)
90. Fatemi, S. H. The hyperglutamatergic hypothesis of autism. Prog. Neuropsychopharmacol. Biol. Psychiatry 32, 911 (2008). (Pubitemid 351312357)
91. Fatemi, S. H. et al. Glutamic acid decarboxylase 65 and 67 kDa proteins are reduced in autistic parietal and cerebellar cortices. Biol. Psychiatry 52, 805-810 (2002).
92. Horder, J. et al. Reduced subcortical glutamate/glutamine in adults with autism spectrum disorders: a [1H]MRS study. Transl. Psychiatry 3, e279 (2013).
93. Herbert, M. R. et al. Dissociations of cerebral cortex, subcortical and cerebral white matter volumes in autistic boys. Brain 126, 1182-1192 (2003). (Pubitemid 36522960)
94. Schumann, C. M. et al. The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. J. Neurosci. 24, 6392-6401 (2004). (Pubitemid 38944230)
95. Waiter, G. D. et al. Structural white matter deficits in high-functioning individuals with autistic spectrum disorder: a voxel-based investigation. Neuroimage 24, 455-461 (2005). (Pubitemid 41359041)
96. Nordahl, C. W. et al. Cortical folding abnormalities in autism revealed by surface-based morphometry. J. Neurosci. 27, 11725-11735 (2007). (Pubitemid 350006915)
97. Wallace, G. L. et al. Increased gyrification, but comparable surface area in adolescents with autism spectrum disorders. Brain 136, 1956-1967 (2013).