Impaired thalamocortical connectivity in autism spectrum disorder: A study of functional and anatomical connectivity

Brain

Volumn 136, Issue 6, 2013, Pages 1942-1955

  Nair, Aarti ^a,b   Treiber, Jeffrey M ^a   Shukla, Dinesh K ^a   Shih, Patricia ^a,c   Müller, Ralph Axel ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b SAN DIEGO STATE UNIVERSITY   (United States)

^c BROWN UNIVERSITY   (United States)

Author keywords

autism; connectivity; diffusion tensor imaging; functional MRI; thalamus

Indexed keywords

ADOLESCENT; ARTICLE; AUTISM; AUTISM DIAGNOSTIC OBSERVATION SCHEDULE; CHILD; CLINICAL ARTICLE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATION ANALYSIS; DIFFUSION TENSOR IMAGING; DISEASE ASSOCIATION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEAD MOVEMENT; HUMAN; MALE; MOTOR CORTEX; MOTOR PERFORMANCE; PRIORITY JOURNAL; RIGHT HEMISPHERE; SENSORIMOTOR FUNCTION; TEMPORAL LOBE; THALAMOCORTICAL CONNECTIVITY; THALAMOCORTICAL TRACT; THALAMUS; TIME SERIES ANALYSIS; TRACTOGRAPHY;

EID: 84878829307     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt079     Document Type: Article

References (95)

1. Allen G, Courchesne E. Attention function and dysfunction in autism. Front Biosci 2001; 6: D105-19.
2. American Psychiatric Association. Diagnostic and statistical manual of mental disorders IV TR. 4th edn. Washington, DC: American Psychiatric Association; 2000.
3. Bailey A, Luthert P, Dean A, Harding B, Janota I, Montgomery M, et al. A clinicopathological study of autism. Brain 1998; 121: 889-905.
4. Beckmann CF, DeLuca M, Devlin JT, Smith SM. Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 2005; 360: 1001-13.
5. Beery KE, Beery NA. Beery-Buktenica developmental test of visual-motor integration-6. 5th edn. Bloomington (MN): NCS Pearson; 2010.
6. Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW. Probabilistic diffusion tractography with multiple fibre orientations: what can we gain Neuroimage 2007; 34: 144-55.
7. Behrens TE, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CA, Boulby PA, et al. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 2003a; 6: 750-7.
8. Behrens TE, Woolrich MW, Jenkinson M, Johansen-Berg H, Nunes RG, Clare S, et al. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 2003b; 50: 1077-88.
9. Boddaert N, Belin P, Chabane N, Poline JB, Barthelemy C, Mouren-Simeoni MC, et al. Perception of complex sounds: abnormal pattern of cortical activation in autism. AJ Psychiatry 2003; 160: 2057-60.
10. Carrera E, Bogousslavsky J. The thalamus and behavior: effects of anatomically distinct strokes. Neurology 2006; 66: 1817-23.
11. Casanova MF, van Kooten IA, Switala AE, van Engeland H, Heinsen H, Steinbusch HW, et al. Minicolumnar abnormalities in autism. Acta Neuropathol (Berl) 2006; 112: 287-303.
12. Cheon KA, Kim YS, Oh SH, Park SY, Yoon HW, Herrington J, et al. Involvement of the anterior thalamic radiation in boys with high functioning autism spectrum disorders: a diffusion tensor imaging study. Brain Res 2011; 1417: 77-86.
13. Cheung C, Chua SE, Cheung V, Khong PL, Tai KS, Wong TK, et al. White matter fractional anisotrophy differences and correlates of diagnostic symptoms in autism. J Child Psychol Psychiatry 2009; 50: 1102-12.
14. Chugani DC, Muzik O, Rothermel RD, Behen ME, Chakraborty PK, Mangner TJ, et al. Altered serotonin synthesis in the dentato-thalamocortical pathway in autistic boys. Ann Neurol 1997; 14: 666-9.
15. Constantino JN, Gruber CP. Social responsiveness scale. Los Angeles, CA: Western Psychological Services; 2005.
16. Cordes D, Haughton VM, Arfanakis K, Carew JD, Turski PA, Moritz CH, et al. Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. AJNR Am J Neuroradiol 2001; 22: 1326-33.
17. Courchesne E, Campbell K, Solso S. Brain growth across the life span in autism: age-specific changes in anatomical pathology. Brain Res 2011a; 1380: 138-45.
18. Courchesne E, Karns CM, Davis HR, Ziccardi R, Carper RA, Tigue ZD, et al. Unusual brain growth patterns in early life in patients with autistic disorder: an MRI study. Neurology 2001; 57: 245-54.
19. Courchesne E, Mouton PR, Calhoun ME, Semendeferi K, Ahrens-Barbeau C, Hallet MJ, et al. Neuron number and size in prefrontal cortex of children with autism. JAMA 2011b; 306: 2001-10.
20. Cox RW. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 1996; 29: 162-73.
21. Cronbach L. Coefficient alpha and teh internal structure of tests. Psychometrika 1951; 16: 297-334.
22. Damasio AR, Maurer RG. A neurological model for childhood autism. Arch Neurol 1978; 35: 777-86.
23. Di Martino A, Kelly C, Grzadzinski R, Zuo XN, Mennes M, Mairena MA, et al. Aberrant striatal functional connectivity in children with autism. Biol Psychiatry 2011; 69: 847-56.
24. Eapen V. Genetic basis of autism: is there a way forward Curr Opin Psychiatry 2011; 24: 226-36.
25. Enticott PG, Bradshaw JL, Iansek R, Tonge BJ, Rinehart NJ. Electrophysiological signs of supplementary-motor-area deficits in high-functioning autism but not Asperger syndrome: an examination of internally cued movement-related potentials. Dev Med Child Neurol 2009; 51: 787-91.
26. Eyler LT, Pierce K, Courchesne E. A failure of left temporal cortex to specialize for language is an early emerging and fundamental property of autism. Brain 2012; 135 (Pt 3): 949-60.
27. Fabbrini G, Pantano P, Totaro P, Calistri V, Colosimo C, Carmellini M, et al. Diffusion tensor imaging in patients with primary cervical dystonia and in patients with blepharospasm. Eur J Neurol 2008; 15: 185-9.
28. Fair DA, Bathula D, Mills KL, Dias TG, Blythe MS, Zhang D, et al. Maturing thalamocortical functional connectivity across development. Front Syst Neurosci 2010; 4: 10.
29. Fair DA, Cohen AL, Dosenbach NU, Church JA, Miezin FM, Barch DM, et al. The maturing architecture of the brain's default network. Proc Natl Acad Sci USA 2008; 105: 4028-32.
30. Fair DA, Cohen AL, Power JD, Dosenbach NU, Church JA, Miezin FM, et al. Functional brain networks develop from a "local to distributed" organization. PLoS Comput Biol 2009; 5: e1000381.
31. Fox MD, Raichle ME. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 2007; 8: 700-11.
32. Friedman SD, Shaw DW, Artru AA, Richards TL, Gardner J, Dawson G, et al. Regional brain chemical alterations in young children with autism spectrum disorder. Neurology 2003; 60: 100-7.
33. Gioia GA, Isquith PK, Guy SC, Kenworthy L. Behavior rating inventory of executive function. Odessa, FL: Psychological Assessment Resources, Inc.; 2000.
34. Goble DJ, Coxon JP, Van Impe A, Geurts M, Van Hecke W, Sunaert S, et al. The neural basis of central proprioceptive processing in older versus younger adults: an important sensory role for right putamen. Hum Brain Mapp 2012; 33: 895-908.
35. Gowen E, Hamilton A. Motor abilities in autism: a review using a computational context. J Autism Dev Disord 2013; 43: 323-44.
36. Harris GJ, Chabris CF, Clark J, Urban T, Aharon I, Steele S, et al. Brain activation during semantic processing in autism spectrum disorders via functional magnetic resonance imaging. Brain Cogn 2006; 61: 54-68.
37. 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: 1366-76.
38. Haznedar MM, Buchsbaum MS, Hazlett EA, LiCalzi EM, Cartwright C, Hollander E. Volumetric analysis and three-dimensional glucose metabolic mapping of the striatum and thalamus in patients with autism spectrum disorders. Am J Psychiatry 2006; 163: 1252-63.
39. Horwitz B, Rumsey JM, Grady CL, Rapoport SI. The cerebral metabolic landscape in autism: intercorrelations of regional glucose utilization. Arch Neurol 1988; 45: 749-55.
40. Hussman JP, Chung RH, Griswold AJ, Jaworski JM, Salyakina D, Ma D, et al. A noise-reduction GWAS analysis implicates altered regulation of neurite outgrowth and guidance in autism. Mol Autism 2011; 2: 1.
41. Jezzard P, Balaban RS. Correction for geometric distortion in echo planar images from B0 field variations. Magn Reson Med 1995; 34: 65-73.
42. Jia L, Jia Lin S, Qin D, Qing L, Yan Z. A diffusion tensor imaging study in essential tremor. J Neuroimaging 2011; 21: 370-4.
43. Johnson MH. Interactive specialization: a domain-general framework for human functional brain development. Dev Cogn Neurosci 2011; 1: 7-21.
44. Jones EG. The thalamus. 2nd edn. Cambridge, UK: Cambridge University Press; 2007.
45. Jones EG. Synchrony in the interconnected circuitry of the thalamus and cerebral cortex. Ann N Y Acad Sci 2009; 1157: 10-23.
46. Jou RJ, Mateljevic N, Kaiser MD, Sugrue DR, Volkmar FR, Pelphrey KA. Structural neural phenotype of autism: preliminary evidence from a diffusion tensor imaging study using tract-based spatial statistics. AJNR Am J Neuroradiol 2011; 32: 1607-13.
47. Just MA, Cherkassky VL, Keller TA, Minshew NJ. Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain 2004; 127 (Pt 8): 1811-21.
48. Klawiter EC, Schmidt RE, Trinkaus K, Liang HF, Budde MD, Naismith RT, et al. Radial diffusivity predicts demyelination in ex vivo multiple sclerosis spinal cords. Neuroimage 2011; 55: 1454-60.
49. Le Bihan D. Looking into the functional architecture of the brain with diffusion MRI. Nat Rev Neurosci 2003; 4: 469-80.
50. Lord C, Rutter M, DiLavore P, Risi S. Autism diagnostic observation schedule. Los Angeles: Western Psychological Services; 1999.
51. Lowe MJ, Dzemidzic M, Lurito JT, Mathews VP, Phillips MD. Correlations in low-frequency BOLD fluctuations reflect cortico-cortical connections. Neuroimage 2000; 12: 582-7.
52. Luo C, Xia Y, Li Q, Xue K, Lai Y, Gong Q, et al. Diffusion and volumetry abnormalities in subcortical nuclei of patients with absence seizures. Epilepsia 2011; 52: 1092-9.
53. Mizuno A, Villalobos ME, Davies MM, Dahl BC, Mü ller RA. Partially enhanced thalamo-cortical functional connectivity in autism. Brain Res 2006; 1104: 160-74.
54. Mostofsky SH, Powell SK, Simmonds DJ, Goldberg MC, Caffo B, Pekar JJ. Decreased connectivity and cerebellar activity in autism during motor task performance. Brain 2009; 132 (Pt 9): 2413-25.
55. Mountcastle VB. The columnar organization of the neocortex. Brain 1997; 120 (Pt 4): 701-22.
56. Mü ller RA. The study of autism as a distributed disorder. Ment Retard Dev Disabil Res Rev 2007; 13: 85-95.
57. Mü ller RA, Behen ME, Rothermel RD, Chugani DC, Muzik O, Mangner TJ, et al Brain mapping of language and auditory perception in high-functioning autistic adults: a PET study. J Autism Dev Disord, 1999, 29, 19-31.
58. Müller RA, Pierce K, Ambrose JB, Allen G, Courchesne E. Atypical patterns of cerebral motor activation in autism: a functional magnetic resonance study. Biol Psychiatry 2001; 49: 665-76.
59. Müller RA, Shih P, Keehn B, Deyoe JR, Leyden KM, Shukla DK. Underconnected, but how A survey of functional connectivity MRI studies in autism spectrum disorders. Cereb Cortex 2011; 21: 2233-43.
60. O'Leary DD, Nakagawa Y. Patterning centers, regulatory genes and extrinsic mechanisms controlling arealization of the neocortex. Curr Opin Neurobiol 2002; 12: 14-25.
61. Palmen SJ, Hulshoff Pol HE, Kemner C, Schnack HG, Durston S, Lahuis BE, et al. Increased gray-matter volume in medication-naive high-functioning children with autism spectrum disorder. Psychol Med 2005; 35: 561-70.
62. Palmen SJ, van Engeland H, Hof PR, Schmitz C. Neuropathological findings in autism. Brain 2004; 127 (Pt 12): 2572-83.
63. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 2012; 59: 2142-54.
64. Rakic P, Ang ES, Breunig J. Setting the stage for cognition: Genesis of the primate cerebral cortex. In: Gazzaniga MS, editor. The cognitive neurosciences. 3rd edn. Cambridge, MA: MIT Press; 2004. p. 33-49.
65. Rippon G, Brock J, Brown C, Boucher J. Disordered connectivity in the autistic brain: challenges for the "new psychophysiology". Int J Psychophysiol 2007; 63: 164-72.
66. Rogers SJ. What are infant siblings teaching us about autism in infancy Autism Res 2009; 2: 125-37.
67. Rutter M, Bailey A, Lord C. Social communication questionnaire. Los Angeles, CA: Western Psychological Services; 2003a.
68. Rutter M, LeCouteur A, Lord C. Autism diagnostic interview-Revised. Los Angeles, CA: Western Psychological Services; 2003b.
69. Ryu YH, Lee JD, Yoon PH, Kim DI, Lee HB, Shin YJ. Perfusion impairments in infantile autism on technetium-99m ethyl cysteinate dimer brain single-photon emission tomography: comparison with findings on magnetic resonance imaging. Eur J Nucl Med 1999; 26: 253-9.
70. Schipul SE, Keller TA, Just MA. Inter-regional brain communication and its disturbance in autism. Front Syst Neurosci 2011; 5: 10.
71. Schlaggar BL, O'Leary D. Potential of visual cortex to develop an array of functional units unique to somatosensory cortex. Science 1991; 252: 1556-60.
72. Sherman SM. The thalamus is more than just a relay. Curr Opin Neurobiol 2007; 17: 417-22.
73. Sherman SM, Guillery RW. Exploring the thalamus. San Diego: Academic Press; 2001.
74. Shih P, Keehn B, Oram JK, Leyden KM, Keown CL, Müller RA. Functional differentiation of posterior superior temporal sulcus in autism: A functional connectivity magnetic resonance imaging study. Biol Psychiatry 2011; 70: 270-7.
75. Shipp S. The brain circuitry of attention. Trends Cogn Sci 2004; 8: 223-30.
76. Shukla DK, Keehn B, Müller RA. Tract-specific analyses of diffusion tensor imaging show widespread white matter compromise in autism spectrum disorder. J Child Psychol Psychiatry 2011; 52: 286-95.
77. Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, et al. Correspondence of the brain's functional architecture during activation and rest. Proc Natl Acad Sci USA 2009; 106: 13040-5.
78. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004; 23 (Suppl 1): S208-19.
79. Starkstein SE, Vazquez S, Vrancic D, Nanclares V, Manes F, Piven J, et al. SPECT findings in mentally retarded autistic individuals. J Neuropsychiatry Clin Neurosci 2000; 12: 370-5.
80. Sundaram SK, Kumar A, Makki MI, Behen ME, Chugani HT, Chugani DC. Diffusion tensor imaging of frontal lobe in autism spectrum disorder. Cereb Cortex 2008; 18: 2659-65.
81. Supekar K, Musen M, Menon V. Development of large-scale functional brain networks in children. PLoS Biol 2009; 7: e1000157.
82. Tamura R, Kitamura H, Endo T, Hasegawa N, Someya T. Reduced thalamic volume observed across different subgroups of autism spectrum disorders. Psychiatry Res 2010; 184: 186-8.
83. Toro R, Konyukh M, Delorme R, Leblond C, Chaste P, Fauchereau F, et al. Key role for gene dosage and synaptic homeostasis in autism spectrum disorders. Trends Genet 2010; 26: 363-72.
84. Townsend J, Courchesne E. Parietal damage and narrow " spotlight" spatial attention. J Cogn Neurosci 1994; 6: 220-32.
85. Tsatsanis KD, Rourke BP, Klin A, Volkmar FR, Cicchetti D, Schultz RT. Reduced thalamic volume in high-functioning individuals with autism. Biol Psychiatry 2003; 53: 121-9.
86. Van Dijk KR, Hedden T, Venkataraman A, Evans KC, Lazar SW, Buckner RL. Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. J Neurophysiol 2010; 103: 297-321.
87. Van Dijk KR, Sabuncu MR, Buckner RL. The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 2012; 59: 431-8.
88. Voineagu I, Wang X, Johnston P, Lowe JK, Tian Y, Horvath S, et al. Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature 2011; 474: 380-4.
89. Webster MJ, Bachevalier J, Ungerleider LG. Transient subcortical connections of inferior temporal areas TE and TEO in infant macaque monkeys. J Comp Neurol 1995; 352: 213-26.
90. Wechsler D. Wechsler Abbreviated Scale of Intelligence (WASI). San Antonio, TX: Psychological Corporation; 1999.
91. Weinstein M, Ben-Sira L, Levy Y, Zachor DA, Ben Itzhak E, Artzi M, et al. Abnormal white matter integrity in young children with autism. Hum Brain Mapp 2011; 32: 534-43.
92. Woodward ND, Karbasforoushan H, Heckers S. Thalamocortical dysconnectivity in schizophrenia. AJ Psychiatry 2012; 169: 1092-9.
93. Yang T, Guo Z, Luo C, Li Q, Yan B, Liu L, et al. White matter impairment in the basal ganglia-thalamocortical circuit of drug-naive childhood absence epilepsy. Epilepsy Res 2012; 99: 267-73.
94. Zhang D, Snyder AZ, Fox MD, Sansbury MW, Shimony JS, Raichle ME. Intrinsic functional relations between human cerebral cortex and thalamus. J Neurophysiol 2008; 100: 1740-8.
95. Zhang D, Snyder AZ, Shimony JS, Fox MD, Raichle ME. Noninvasive functional and structural connectivity mapping of the human thalamocortical system. Cereb Cortex 2010; 20: 1187-94.