Neuroimaging in autism spectrum disorder

Author/s
Brian Hallahan, Kamila Janik
Citation
Issue 4 Summer 2014
CEPiP.2014.1.56-63
Abstract

Modern neuroimaging techniques have provided researchers with invaluable tools to explore anatomical and functional brain abnormalities in individuals with autism spectrum disorder (ASD). Converging evidence from structural MRI studies demonstrates differences in post-natal brain maturation in individuals with ASD compared to healthy controls, with early brain overgrowth followed by a subsequent plateauing of growth through adolescence and specific regional brain volume reductions in adulthood. These brain volume reductions occur in regions (e.g. amygdala, cerebellum, corpus callosum) which have been linked repeatedly to the clinical phenotype. Functional MRI, MRI spectroscopy and diffusion tensor imaging studies have further clarified the neurobiology of ASD, with increasing evidence demonstrating brain dysconnectivity and white matter abnormalities. Future longitudinal neuroimaging studies using a variety of neuroimaging techniques aligned to clinical and behavioural data should further clarify the neurobiology of ASD.

Keywords: autism spectrum disorder, neuroimaging, structural MRI, functional MRI, MRI spectroscopy

Cite as: Cutting Edge Psychiatry in Practice 2014, 4(1):56-63; https://doi.org/10.65031/nutr3684

References

  1. Ecker C, Murphy D. Neuroimaging in autism – from basic science to transitional research. Nat Rev Neuro 2014; 10: 82-91. https://doi.org/10.1038/nrneurol.2013.276
  2. Courchesne E, Carper R, Akshoomoff N. Evidence of brain overgrowth in the first year of life in autism. JAMA 2003; 290: 337–344. https://doi.org/10.1001/jama.290.3.337
  3. Hazlett HC, Poe M, Gerig G, Smith RG, Provenzale J, Ross A, et al. Magnetic resonance imaging and head circumference study of brain size in autism: birth through age 2 years. Arch Gen Psychiatry 2005; 62: 1366–1376. https://doi.org/10.1001/archpsyc.62.12.1366
  4. Carper RA, Moses P, Tigue ZD, Courchesne E. Cerebral lobes in autism: early hyperplasia and abnormal age effects. Neuroimage 2002; 4: 1038-1051. https://doi.org/10.1006/nimg.2002.1099
  5. Ecker C, Suckling J, Deoni SC, Lombardo MV, Bullmore ET, Baron- Cohen S, et al. Brain anatomy and its relationship to behavior in adults with autism spectrum disorder: a multicenter magnetic resonance imaging study. Arch Gen Psychiatry 2012; 69:195-209. https://doi.org/10.1001/archgenpsychiatry.2011.1251
  6. McAlonan GM, Cheung C, Cheung V, Wong N, Suckling J, Chua SE. Differential effects on white- matter systems in high-functioning autism and Asperger’s syndrome. Psychol Med 2009; 39: 1885- 1893. https://doi.org/10.1017/s0033291709005728
  7. Hallahan B, Daly EM, McAlonan G, Loth E, Toal F, O’Brien F, et al. Brian morphometry volume in autistic spectrum disorder: a magnetic resonance imaging study of adults. Psychol Med 2008; 39: 337-346. https://doi.org/10.1017/s0033291708003383
  8. Courchesne E, Campbell K, Solso S. Brain growth across the lifespan in autism: Age-specific changes in anatomical pathology. Brian Research 2011; 1380:138-145. https://doi.org/10.1016/j.brainres.2010.09.101
  9. Herbert MR, Ziegler DA, Deutsch CK, O’Brien LM, Lange N, Bakardjiev A, et al. Dissociations of cerebral cortex, subcortical and cerebral white matter volumes in autistic boys. Brain 2003; 126:1182- 192. https://doi.org/10.1093/brain/awg110
  10. Amaral DG, Schumann CM, Nordahl CW. Neuroanatomy of autism. Trends Neurosci 2008; 31:137-145. https://doi.org/10.1016/j.tins.2007.12.005
  11. Aylward EH, Minshew NJ, Goldstein G et al. MRI volumes of amygdala and hippocampus in non-mentally retarded autistic adolescents and adults. Neurology 1999; 53: 2145-2150. https://doi.org/10.1212/wnl.53.9.2145
  12. Via E, Radua J, Cardoner N, Happe F, Mataix-Cols D. Meta-analysis of gray matter abnormalities in Autism Spectrum Disorder. Arch Gen Psychiatry 2011; 68: 409-418. https://doi.org/10.1001/archgenpsychiatry.2011.27
  13. Toal, F, Daly EM, Page L, Deeley Q, Hallahan B, Bloemen O, et al. Clinical and anatomical heterogeneity in autistic spectrum disorder: a structural MRI study. Psychol Med 2010; 40: 1171-1181. https://doi.org/10.1017/s0033291709991541
  14. McAlonan GM, Cheung V, Cheung C, Suckling J, Lam GY, Tai KS, et al. Mapping the brain in autism. A voxel-based morphometry study of volumetric differences and intercorrelations in autism. Brain 2005; 128: 268-276. https://doi.org/10.1093/brain/awh332
  15. Stanfield AC, McIntosh AM, Spencer MD, Philip R, Gaur S, Lawrie SM. Towards a neuroanatomy of autism: a systematic review and meta-analysis of structural magnetic resonance imaging studies. Eur Psychiatry 2008; 23: 289-299. https://doi.org/10.1016/j.eurpsy.2007.05.006
  16. Frazier TW, Hardan AY. A meta-analysis of the corpus callosum in autism. Biol Psychiatry 2009; 66: 935-941. https://doi.org/10.1016/j.biopsych.2009.07.022
  17. Wallace GL, Dankner N, Kenworthy L, Giedd JN, Martin A. Age-related temporal and parietal cortical thinning in autism spectrum disorders. Brain 2010; 133: 3745–3754. https://doi.org/10.1093/brain/awq279
  18. Wallace GL, Robustelli B, Danker N, Kenworthy L, Gledd JN, Martin A. Increased gyrification, but comparable surface area in adolescents with autism spectrum disorders. Brain 2013; 136: 1956-1967. https://doi.org/10.1093/brain/awt106
  19. Ecker C, Ginest C, Feng Y, Johnston P, Lombardo MV, Lai MC, et al. Brain surface anatomy in adults with autism: the relationship between surface area, cortical thickness, and autistic symptoms. JAMA Psychiatry 2013; 70: 59-70. https://doi.org/10.1001/jamapsychiatry.2013.265
  20. Kates WR, Ikuta I, Burnette CP. Gyrification patterns in monozygotic twin pairs varying in discordance for autism. Autism Res 2009; 2: 267-278. https://doi.org/10.1002/aur.98
  21. Nelson KB, Grether JK, Croen LA, Dambrosia JM Dickens BF, Jelliffe LL, et al. Neuropeptides and neurotrophins in neonatal blood of children with autism or mental retardation. Annals Neurol 2001; 49: 597-606. https://doi.org/10.1002/ana.1024.abs
  22. Morrison ME, Massone CA. Granule neuron regulation of Purkinje cell development: striking a balance between neurotrophin and glutamate signaling. J Neurosci 1998; 18: 3563-3573. https://doi.org/10.1523/jneurosci.18-10-03563.1998
  23. Hobbs K, Kennedy A, Dubray M, et al. A retrospective fetal ultrasound study of brain size in autism Biol Psychiatry 2007; 62: 1048-1055. https://doi.org/10.1016/j.biopsych.2007.03.020
  24. Allen G, Buxton R Wong EC, Courchesne E. Attentional activation of the cerebellum independent of motor involvement, Science 1997;275: 1940-1943. https://doi.org/10.1126/science.275.5308.1940
  25. Townsend J, Courchesne E, Covington J, Westerfield M, Harris NS, Lyden P, et al. Spatial attention deficits in patients with acquired or developmental cerebellar abnormality. J Neurosci 1999; 19: 5632-5643. https://doi.org/10.1523/jneurosci.19-13-05632.1999
  26. Ronning C, Sundet K, Due-Tonnessen B, Lundar T, Helseth E. Persistent cognitive dysfunction secondary to cerebellar injury in patients treated for posterior fossa tumours in childhood. Pediatr Neurosurg 2005; 41: 15-21. https://doi.org/10.1159/000084860
  27. Schmahann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain 1998; 121: 561-579. 
  28. Levisohn L, Cronin-Golomb A, Schmahann JD. Neuropsychological consequences of cerebellar tumour resection in children. Cerebellar cognitive affective syndrome in a paediatric population. Brain 2000; 123: 1041-1050. https://doi.org/10.1093/brain/123.5.1041
  29. Allen G, Muller RA, Courchesne E. Cerebellar function in Autism: Functional Magnetic Resonance Image activation during a simple motor task. Biol Psychiatry 2004; 56: 269-278. https://doi.org/10.1016/j.biopsych.2004.06.005
  30. Critchley HD, Daly E, Bullmore ET, Williams SC, Van Amelsvoort T, Robertson DM, et al. The functional neuroanatomy of social behaviour. Changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain 2000; 1: 2203-2212. https://doi.org/10.1093/brain/123.11.2203
  31. Grelotti DJ, Gauthier I, Schultz RT. Social interest and the development of cortical face specialization: what autism teaches us about face processing. Dev Psychbiol 2002; 40: 213-225. https://doi.org/10.1002/dev.10028
  32. Burgess N, Maguire EA, O’Keefe J. The human hippocampus and spatial and episodic memory. Neuron 2002; 35: 625-641. https://doi.org/10.1016/s0896-6273(02)00830-9
  33. Richter-Levin G. The amygdala, the hippocampus, and emotional modulation of memory. Neuroscientist 2004; 10: 31-39. https://doi.org/10.1177/1073858403259955
  34. Rizzolatti G, Fabbri-Destro M. Mirror neurons: from discovery to autism. Exp Brain Res. 2010; 200: 223-237. https://doi.org/10.1007/s00221-009-2002-3
  35. Simmons DR, Robertson AE, McKay LS, Toal E, McAleer P, Pollick FE. Vision in autism spectrum disorders. Vision Res. 2009; 49: 2705-2739. https://doi.org/10.1016/j.visres.2009.08.005
  36. Lind SE, Bowler DM. Recognition memory, self-other source memory, and theory-of-mind in children with autism spectrum disorder. J Autism Dev Disord. 2009; 39: 1231-1239. https://doi.org/10.1007/s10803-009-0735-2
  37. Paul LK Brown WS, Adolphs R, Tyszka JM, Richards LJ, Mukherjee P, Sherr EH. Agenesis of the corpus callosum: genetic, developmental and functional aspects of connectivity. Nat Rev Neurosci 2007; 8: 287-299. https://doi.org/10.1038/nrn2107
  38. Keary CJ, Minshew NJ, Bansal R, Goradia D, Fedorov S, Keshaven MS, Hardan AY. Corpus callosum volume and neurocognition in autism. J Autism Dev Disord. 2009; 39: 839-841. https://doi.org/10.1007/s10803-009-0689-4
  39. Idring S, Rai D, Dal H, Dalman C, Sturm H, Zander E, et al. Autism spectrum disorders in the Stockholm Youth Cohort: design, prevalence and validity. PLoS One 2012; 7: 241280. https://doi.org/10.1371/journal.pone.0041280
  40. Kopp S, Gillberg C. The Autism Spectrum Screening Questionnaire (ASSQ)-Revised Extended Version (ASSQ-REV) and instrument for better capturing the autism phenotype in girls? A preliminary study involving 191 clinical cases and community controls. Res Dev Disabil 2011; 32: 2875-2888. https://doi.org/10.1016/j.ridd.2011.05.017
  41. Lai MC, Lombardo MV, Suckling J, Ruigrok AN, Chakrabarti B, Ecker C, et al. Biological sex affects the neurobiology of autism. Brain 2013; 136:2799-815. https://doi.org/10.1093/brain/awt216
  42. Craig MC, Zaman SH, Daly EM, Cutter WJ, Robertson DMW, Hallahan B et al., Women with autistic- spectrum disorder: magnetic resonance imaging study of brain anatomy. Br J Psychiatry 2007; 191:224-228. https://doi.org/10.1192/bjp.bp.106.034603
  43. Greimel E, Schulte-Rüther M, Kircher T, Kamp-Becker I, Remschmidt H, Fink GR, Herpertz-Dahlmann B, Konrad K: Neural mechanisms of empathy in adolescents with autism spectrum disorder and their fathers. NeuroImage 2010, 49: 1055-1065. https://doi.org/10.1016/j.neuroimage.2009.07.057
  44. Koshino H, Kana RK, Keller TA, Cherkassky VL, Minshew NJ, Just MA: fMRI investigation of working memory for faces in autism: visual coding and underconnectivity with frontal areas. Cereb Cortex 2008, 18: 289-300. https://doi.org/10.1093/cercor/bhm054
  45. Wang AT, Lee SS, Sigman M, Dapretto M: Reading affect in the face and voice: neural correlates of interpreting communicative intent in children and adolescents with autism spectrum disorders. Arch Gen Psychiatry 2007, 64: 698-708. https://doi.org/10.1001/archpsyc.64.6.698
  46. Just MA, Cherkassky VL, Keller TA, Minshew MJ. Cortical activation and synchronization during sentence comprehension in high- functioning autism: evidence of underconnectivity. Brain 2004; 127: 1811-1821. https://doi.org/10.1093/brain/awh199
  47. Sahyoun CP, Belliveau JW, Soulières I, Schwartz S, Mody M. Neuroimaging of the functional and structural networks underlying visuospatial vs. linguistic reasoning in high-functioning autism. Neuropsychologia 2010; 48: 86-95. https://doi.org/10.1016/j.neuropsychologia.2009.08.013
  48. Ebish SJ, Gallese V, Willems RM, Mantini D, Groen WB, Romani GL, et al. Altered intrinsic functional connectivity of anterior and posterior insula regions in high-functioning participants with autism spectrum disorder. Hum Brain Mapp 2011; 32: 1013-1028. https://doi.org/10.1002/hbm.21085
  49. Solomon M, Ozonoff SJ, Ursu S, Ravizza S, Cummings N, Ly S, et al. The neural substrates of cognitive control deficits in autism spectrum disorders. Neuropsychologia 2009; 47: 2515-2526. https://doi.org/10.1016/j.neuropsychologia.2009.04.019
  50. Deeley Q, Daly EM, Surguladze S, Page L, Toal F, Robertson D, Curran S, et al. An event related functional magnetic resonance imaging study of facial emotion processing in Asperger syndrome. Biol Psychiatry. 2007; 62: 207-217. https://doi.org/10.1016/j.biopsych.2006.09.037
  51. Pelphrey KA, Morris JP, McCarthy G, Labar KS. Perception of dynamic changes in facial affect and identity in autism. Soc Cogn Affect Neurosci 2007; 2: 140-149. https://doi.org/10.1093/scan/nsm010
  52. Daly EM, Deeley Q, Ecker C, Craig M, Hallahan B, Murphy C, et al. Serotonin and the neural processing of facial emotions in adults with autism: An fMRI study using acute tryptophan depletion. Arch Gen Psychiatry 2012; 69: 1003-1013. https://doi.org/10.1001/archgenpsychiatry.2012.513
  53. Anagnostou E, Taylor MJ. Review of neuroimaging in autism spectrum disorders: what have we learned and where we go from here. Mol Autism 2011; 2:4. https://doi.org/10.1186/2040-2392-2-4
  54. Fletcher PT Whitaker RT, Tao R, DuBray MB, Froehlich A, Ravichandan C, et al. Microstructural connectivity of the arcuate fasciculus in adolescents with high-functioning autism. Neuroimage 2010; 51: 1117-1125. https://doi.org/10.1016/j.neuroimage.2010.01.083
  55. Barnea-Goraly N, Lotspeich LJ, Reiss AL: Similar white matter aberrations in children with autism and their unaffected siblings: a diffusion tensor imaging study using tract-based spatial statistics. Arch Gen Psychiatry 2010, 67:1052-1060. https://doi.org/10.1001/archgenpsychiatry.2010.123
  56. Sivaswamy L, Kumar A, Rajan D, Behen M, Muzik O, Chugani D, Chugani H. A. Diffusion Tensor Imaging study of the cerebellar pathways in children with Autism Spectrum Disorder. J Child Neurol 2010, 25:1223-1231. https://doi.org/10.1177/0883073809358765
  57. Cheung C, Chua SE, Cheung V, Khong PL, Tai KS, Wong TK, et al. White matter fractional anisotropy differences and correlates of diagnostic symptoms in autism. J Child Psychol Psychiatry; 50: 1102-1112. https://doi.org/10.1111/j.1469-7610.2009.02086.x
  58. Lee JE, Bigler ED, Alexander AL, Lazar M, DuBray MB, Chung MK, et al. Diffusion tensor imaging of white matter in the superior temporal gyrus and temporal stem in autism. Neurosci Lett 2007; 434: 127-32. https://doi.org/10.1016/j.neulet.2007.07.042
  59. Ben Bashat D, Kronfeld-Duenias V, Zachor DA, Ekstein PM, Hendler T, Tarrasch R, et al. Accelerated maturation of white matter in young children with autism: a high b value DWI study. Neuroimage 2007; 37: 40-47. https://doi.org/10.1016/j.neuroimage.2007.04.060
  60. Cheng Y, Chou KH, Chen IY, Fan YT, Decety J, Lin CP. Atypical development of white matter microstructure in adolescents with autism spectrum disorders. Neuroimage 2010; 50: 873-882. https://doi.org/10.1016/j.neuroimage.2010.01.011
  61. O’Brien F, Page L, O’Gorman RL, Bolton P, Sharma A, Baird G, et al. Maturation of limbic regions in Asperger syndrome: a preliminary study using proton magnetic resonance spectroscopy and structural magnetic resonance imaging. Psychiatry Res Neuroimaging 2010; 184: 77-85. https://doi.org/10.1016/j.pscychresns.2010.08.007
  62. Fujii E, Mori K, Miyazaki M, Hashimoto T, Harada M, Kagami S. Function of the frontal lobe in autistic individuals: a proton magnetic resonance spectroscopic study. J Med Invest 2010; 57: 35-44. https://doi.org/10.2152/jmi.57.35
  63. Bernardi S, Anagnostou E, Shen J Kolevzon A, Buxbaum JD, Hollander E, Hof PR, Fan J. In vivo 1-H-magnetic resonance spectroscopy study of the attentional network in autism. Brain Res 2011; 1380: 198-205.CEPiP.org Issue 4 September 2014 https://doi.org/10.1016/j.brainres.2010.12.057