Alterations of local spontaneous brain activity and connectivity in adults with high-functioning autism spectrum disorder

Molecular Autism

Volumn 6, Issue 1, 2015, Pages

  Itahashi, Takashi ^a   Yamada, Takashi ^a,b   Watanabe, Hiromi ^a   Nakamura, Motoaki ^a,c   Ohta, Haruhisa ^a   Kanai, Chieko ^a   Iwanami, Akira ^a   Kato, Nobumasa ^a   Hashimoto, Ryu Ichiro ^a,d  

^a SHOWA UNIVERSITY   (Japan)

^b ADVANCED TELECOMMUNICATIONS RESEARCH INSTITUTE INTERNATIONAL   (Japan)

^c Kinko Hospital   (Japan)

^d TOKYO METROPOLITAN UNIVERSITY   (Japan)

Author keywords

Amplitude of low frequency fluctuation; Autism spectrum disorder; Local connectivity; Resting state functional magnetic resonance imaging; Spontaneous activity

Indexed keywords

ADULT; AMPLITUDE MODULATION; ARTICLE; AUTISM; AUTISM SPECTRUM QUOTIENT; CLINICAL ARTICLE; CONCEPTUAL FRAMEWORK; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUSIFORM GYRUS; HUMAN; LEFT HEMISPHERE; LINGUAL GYRUS; MALE; MIDDLE FRONTAL GYRUS; MIDDLE OCCIPITAL GYRUS; MIDDLE TEMPORAL GYRUS; OCCIPITAL GYRUS; PARAHIPPOCAMPAL GYRUS; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; RESTING STATE NETWORK; RIGHT HEMISPHERE; SCORING SYSTEM; SOCIAL INTERACTION; SUPERIOR FRONTAL GYRUS;

EID: 84930205807     PISSN: None     EISSN: 20402392     Source Type: Journal    
DOI: 10.1186/s13229-015-0026-z     Document Type: Article

References (91)

1. Vissers ME, Cohen MX, Geurts HM. Brain connectivity and high functioning autism: a promising path of research that needs refined models, methodological convergence, and stronger behavioral links. Neurosci Biobehav Rev. 2012;36(1):604-25.
2. Padmanabhan A, Lynn A, Foran W, Luna B, O'Hearn K. Age related changes in striatal resting state functional connectivity in autism. Front Hum Neurosci. 2013;7:814.
3. Uddin LQ, Supekar K, Menon V. Reconceptualizing functional brain connectivity in autism from a developmental perspective. Front Hum Neurosci. 2013;7:458.
4. You X, Norr M, Murphy E, Kuschner ES, Bal E, Gaillard WD, et al. Atypical modulation of distant functional connectivity by cognitive state in children with autism spectrum disorders. Front Hum Neurosci. 2013;7:482.
5. 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.
6. Muller RA. The study of autism as a distributed disorder. Ment Retard Dev Disabil Res Rev. 2007;13(1):85-95.
7. Just MA, Cherkassky VL, Keller TA, Kana RK, Minshew NJ. Functional and anatomical cortical underconnectivity in autism: evidence from an FMRI study of an executive function task and corpus callosum morphometry. Cereb Cortex. 2007;17(4):951-61.
8. Assaf M, Jagannathan K, Calhoun VD, Miller L, Stevens MC, Sahl R, et al. Abnormal functional connectivity of default mode sub-networks in autism spectrum disorder patients. Neuroimage. 2010;53(1):247-56.
9. Kennedy DP, Redcay E, Courchesne E. Failing to deactivate: resting functional abnormalities in autism. Proc Natl Acad Sci U S A. 2006;103(21):8275-80.
10. Kana RK, Keller TA, Cherkassky VL, Minshew NJ, Just MA. Sentence comprehension in autism: thinking in pictures with decreased functional connectivity. Brain. 2006;129(Pt 9):2484-93.
11. 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(9):847-56.
12. Monk CS, Peltier SJ, Wiggins JL, Weng SJ, Carrasco M, Risi S, et al. Abnormalities of intrinsic functional connectivity in autism spectrum disorders. Neuroimage. 2009;47(2):764-72.
13. Delmonte S, Gallagher L, O'Hanlon E, McGrath J, Balsters JH. Functional and structural connectivity of frontostriatal circuitry in autism spectrum disorder. Front Hum Neurosci. 2013;7:430.
14. Noonan SK, Haist F, Muller RA. Aberrant functional connectivity in autism: evidence from low-frequency BOLD signal fluctuations. Brain Res. 2009;1262:48-63.
15. Kana RK, Libero LE, Moore MS. Disrupted cortical connectivity theory as an explanatory model for autism spectrum disorders. Phys Life Rev. 2011;8(4):410-37.
16. Wiggins JL, Peltier SJ, Ashinoff S, Weng SJ, Carrasco M, Welsh RC, et al. Using a self-organizing map algorithm to detect age-related changes in functional connectivity during rest in autism spectrum disorders. Brain Res. 2011;1380:187-97.
17. Vargas DL, Nascimbene C, Krishnan C, Zimmerman AW, Pardo CA. Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann Neurol. 2005;57(1):67-81.
18. Courchesne E, Pierce K. Why the frontal cortex in autism might be talking only to itself: local over-connectivity but long-distance disconnection. Curr Opin Neurobiol. 2005;15(2):225-30.
19. Zang Y, Jiang T, Lu Y, He Y, Tian L. Regional homogeneity approach to fMRI data analysis. Neuroimage. 2004;22(1):394-400.
20. Paakki JJ, Rahko J, Long X, Moilanen I, Tervonen O, Nikkinen J, et al. Alterations in regional homogeneity of resting-state brain activity in autism spectrum disorders. Brain Res. 2010;1321:169-79.
21. Shukla DK, Keehn B, Muller RA. Regional homogeneity of fMRI time series in autism spectrum disorders. Neurosci Lett. 2010;476(1):46-51.
22. Sepulcre J, Liu H, Talukdar T, Martincorena I, Yeo BT, Buckner RL. The organization of local and distant functional connectivity in the human brain. PLoS Comput Biol. 2010;6(6), e1000808.
23. Maximo JO, Keown CL, Nair A, Muller RA. Approaches to local connectivity in autism using resting state functional connectivity MRI. Front Hum Neurosci. 2013;7:605.
24. Keown CL, Shih P, Nair A, Peterson N, Mulvey ME, Muller RA. Local functional overconnectivity in posterior brain regions is associated with symptom severity in autism spectrum disorders. Cell Rep. 2013;5(3):567-72.
25. Biswal BB, Mennes M, Zuo XN, Gohel S, Kelly C, Smith SM, et al. Toward discovery science of human brain function. Proc Natl Acad Sci U S A. 2010;107(10):4734-9.
26. Han Y, Wang J, Zhao Z, Min B, Lu J, Li K, et al. Frequency-dependent changes in the amplitude of low-frequency fluctuations in amnestic mild cognitive impairment: a resting-state fMRI study. Neuroimage. 2011;55(1):287-95.
27. Liu Y, Yu C, Zhang X, Liu J, Duan Y, Alexander-Bloch AF, et al. Impaired long distance functional connectivity and weighted network architecture in Alzheimer's disease. Cerebral Cortex. 2013;24:1422-35.
28. Wang L, Dai W, Su Y, Wang G, Tan Y, Jin Z, et al. Amplitude of low-frequency oscillations in first-episode, treatment-naive patients with major depressive disorder: a resting-state functional MRI study. PLoS One. 2012;7(10), e48658.
29. Zang YF, He Y, Zhu CZ, Cao QJ, Sui MQ, Liang M, et al. Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev. 2007;29(2):83-91.
30. Di Martino A, Yan CG, Li Q, Denio E, Castellanos FX, Alaerts K, et al. The autism brain imaging data exchange: towards a large-scale evaluation of the intrinsic brain architecture in autism. Mol Psychiatry. 2013;19:569-67.
31. Supekar K, Uddin LQ, Khouzam A, Phillips J, Gaillard WD, Kenworthy LE, et al. Brain hyperconnectivity in children with autism and its links to social deficits. Cell Rep. 2013;5(3):738-47.
32. Bos DJ, van Raalten TR, Oranje B, Smits AR, Kobussen NA, Belle J, et al. Developmental differences in higher-order resting-state networks in autism spectrum disorder. Neuroimage Clin. 2014;4:820-7.
33. Matsuoka K, Uno M, Kasai K, Koyama K, Kim Y. Estimation of premorbid IQ in individuals with Alzheimer's disease using Japanese ideographic script (Kanji) compound words: Japanese version of national adult reading test. Psychiatry Clin Neurosci. 2006;60(3):332-9.
34. Wakabayashi A, Baron-Cohen S, Wheelwright S, Tojo Y. The autism-spectrum quotient (AQ) in Japan: a cross-cultural comparison. J Autism Dev Disord. 2006;36(2):263-70.
35. Hoekstra RA, Bartels M, Cath DC, Boomsma DI. Factor structure, reliability and criterion validity of the autism-spectrum quotient (AQ): a study in Dutch population and patient groups. J Autism Dev Disord. 2008;38(8):1555-66.
36. Cox RW. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res. 1996;29(3):162-73.
37. 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.
38. Behzadi Y, Restom K, Liau J, Liu TT. A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage. 2007;37(1):90-101.
39. Murphy K, Birn RM, Handwerker DA, Jones TB, Bandettini PA. The impact of global signal regression on resting state correlations: are anti-correlated networks introduced? Neuroimage. 2009;44(3):893-905.
40. 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(3):2142-54.
41. Van Dijk KR, Sabuncu MR, Buckner RL. The influence of head motion on intrinsic functional connectivity MRI. Neuroimage. 2012;59(1):431-8.
42. Carp J. Optimizing the order of operations for movement scrubbing: comment on Power et al. Neuroimage. 2013;76:436-8.
43. Di Martino A, Zuo XN, Kelly C, Grzadzinski R, Mennes M, Schvarcz A, et al. Shared and distinct intrinsic functional network centrality in autism and attention-deficit/hyperactivity disorder. Biol Psychiatry. 2013;74(8):623-32.
44. Zuo XN, Ehmke R, Mennes M, Imperati D, Castellanos FX, Sporns O, et al. Network centrality in the human functional connectome. Cereb Cortex. 2012;22(8):1862-75.
45. Buckner RL, Sepulcre J, Talukdar T, Krienen FM, Liu H, Hedden T, et al. Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. J Neurosci. 2009;29(6):1860-73.
46. Hwang K, Hallquist MN, Luna B. The development of hub architecture in the human functional brain network. Cereb Cortex. 2013;23(10):2380-93.
47. Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, et al. Mapping the structural core of human cerebral cortex. PLoS Biol. 2008;6(7), e159.
48. Mueller S, Wang D, Fox MD, Yeo BT, Sepulcre J, Sabuncu MR, et al. Individual variability in functional connectivity architecture of the human brain. Neuron. 2013;77(3):586-95.
49. Song XW, Dong ZY, Long XY, Li SF, Zuo XN, Zhu CZ, et al. REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One. 2011;6(9), e25031.
50. Nichols T, Brett M, Andersson J, Wager T, Poline JB. Valid conjunction inference with the minimum statistic. Neuroimage. 2005;25(3):653-60.
51. Lombardo MV, Ashwin E, Auyeung B, Chakrabarti B, Taylor K, Hackett G, et al. Fetal testosterone influences sexually dimorphic gray matter in the human brain. J Neurosci. 2012;32(2):674-80.
52. Lai MC, Lombardo MV, Suckling J, Ruigrok AN, Chakrabarti B, Ecker C, et al. Biological sex affects the neurobiology of autism. Brain. 2013;136(Pt 9):2799-815.
53. Abrams DA, Lynch CJ, Cheng KM, Phillips J, Supekar K, Ryali S, et al. Underconnectivity between voice-selective cortex and reward circuitry in children with autism. Proc Natl Acad Sci. 2013;110(29):12060-5.
54. Ebisch 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(7):1013-28.
55. Kennedy DP, Courchesne E. The intrinsic functional organization of the brain is altered in autism. Neuroimage. 2008;39(4):1877-85.
56. Uddin LQ, Supekar K, Lynch CJ, Khouzam A, Phillips J, Feinstein C, et al. Salience network-based classification and prediction of symptom severity in children with autism. JAMA Psychiatry. 2013;70(8):869-79.
57. Lynch CJ, Uddin LQ, Supekar K, Khouzam A, Phillips J, Menon V. Default mode network in childhood autism: posteromedial cortex heterogeneity and relationship with social deficits. Biol Psychiatry. 2013;74(3):212-9.
58. Mottron L, Burack JA, Iarocci G, Belleville S, Enns JT. Locally oriented perception with intact global processing among adolescents with high-functioning autism: evidence from multiple paradigms. J Child Psychol Psychiatry. 2003;44(6):904-13.
59. O'Riordan MA, Plaisted KC, Driver J, Baron-Cohen S. Superior visual search in autism. J Exp Psychol Hum Percept Perform. 2001;27(3):719-30.
60. Muth A, Honekopp J, Falter CM. Visuo-spatial performance in autism: a meta-analysis. J Autism Dev Disord. 2014;44(12):3245-63.
61. Blaser E, Eglington L, Carter AS, Kaldy Z. Pupillometry reveals a mechanism for the autism spectrum disorder (ASD) advantage in visual tasks. Sci Rep. 2014;4:4301.
62. Mottron L, Dawson M, Soulieres I, Hubert B, Burack J. Enhanced perceptual functioning in autism: an update, and eight principles of autistic perception. J Autism Dev Disord. 2006;36(1):27-43.
63. Corbetta M, Kincade JM, Shulman GL. Neural systems for visual orienting and their relationships to spatial working memory. J Cogn Neurosci. 2002;14(3):508-23.
64. Liu Y, Bengson J, Huang H, Mangun GR, Ding M. Top-down modulation of neural activity in anticipatory visual attention: control mechanisms revealed by simultaneous EEG-fMRI. Cereb Cortex. 2014. doi:10.1093/cercor/bhu204.
65. Hopfinger JB, Buonocore MH, Mangun GR. The neural mechanisms of top-down attentional control. Nat Neurosci. 2000;3(3):284-91.
66. Hahn B, Ross TJ, Stein EA. Neuroanatomical dissociation between bottom-up and top-down processes of visuospatial selective attention. Neuroimage. 2006;32(2):842-53.
67. Gadgil M, Peterson E, Tregellas J, Hepburn S, Rojas DC. Differences in global and local level information processing in autism: an fMRI investigation. Psychiatry Res. 2013;213(2):115-21.
68. Avidan G, Tanzer M, Hadj-Bouziane F, Liu N, Ungerleider LG, Behrmann M. Selective dissociation between core and extended regions of the face processing network in congenital prosopagnosia. Cereb Cortex. 2013;24:1565-78.
69. Behrmann M, Plaut DC. Distributed circuits, not circumscribed centers, mediate visual recognition. Trends Cogn Sci. 2013;17(5):210-9.
70. Cohen Kadosh K, Johnson MH. Developing a cortex specialized for face perception. Trends Cogn Sci. 2007;11(9):367-9.
71. Kitada R, Johnsrude IS, Kochiyama T, Lederman SJ. Brain networks involved in haptic and visual identification of facial expressions of emotion: an fMRI study. Neuroimage. 2010;49(2):1677-89.
72. Pelphrey KA, Morris JP, McCarthy G. Grasping the intentions of others: the perceived intentionality of an action influences activity in the superior temporal sulcus during social perception. J Cogn Neurosci. 2004;16(10):1706-16.
73. Sugiura M, Yomogida Y, Mano Y, Sassa Y, Kambara T, Sekiguchi A, et al. From social-signal detection to higher social cognition: an fMRI approach. Social Cognitive and Affective Neuroscience. 2013;9:1303-9.
74. Deeley Q, Daly EM, Surguladze S, Page L, Toal F, Robertson D, et al. An event related functional magnetic resonance imaging study of facial emotion processing in Asperger syndrome. Biol Psychiatry. 2007;62(3):207-17.
75. von dem Hagen EA, Stoyanova RS, Rowe JB, Baron-Cohen S, Calder AJ. Direct gaze elicits atypical activation of the theory-of-mind network in autism spectrum conditions. Cereb Cortex. 2013;24:1485-92.
76. Georgescu AL, Kuzmanovic B, Schilbach L, Tepest R, Kulbida R, Bente G, et al. Neural correlates of "social gaze" processing in high-functioning autism under systematic variation of gaze duration. Neuroimage Clin. 2013;3:340-51.
77. Nummenmaa L, Engell AD, von dem Hagen E, Henson RN, Calder AJ. Autism spectrum traits predict the neural response to eye gaze in typical individuals. Neuroimage. 2012;59(4):3356-63.
78. Zou QH, Zhu CZ, Yang Y, Zuo XN, Long XY, Cao QJ, et al. An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF. J Neurosci Methods. 2008;172(1):137-41.
79. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature. 2001;412(6843):150-7.
80. Mukamel R, Gelbard H, Arieli A, Hasson U, Fried I, Malach R. Coupling between neuronal firing, field potentials, and FMRI in human auditory cortex. Science. 2005;309(5736):951-4.
81. Siero JC, Hermes D, Hoogduin H, Luijten PR, Ramsey NF, Petridou N. BOLD matches neuronal activity at the mm scale: a combined 7T fMRI and ECoG study in human sensorimotor cortex. Neuroimage. 2014;101:177-84.
82. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, O'Shea DJ, et al. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature. 2011;477(7363):171-8.
83. van Kooten IA, Palmen SJ, von Cappeln P, Steinbusch HW, Korr H, Heinsen H, et al. Neurons in the fusiform gyrus are fewer and smaller in autism. Brain. 2008;131(Pt 4):987-99.
84. Suzuki K, Sugihara G, Ouchi Y, Nakamura K, Futatsubashi M, Takebayashi K, et al. Microglial activation in young adults with autism spectrum disorder. JAMA Psychiatry. 2013;70(1):49-58.
85. Suzuki K, Sugihara G, Ouchi Y, Nakamura K, Tsujii M, Futatsubashi M, et al. Reduced acetylcholinesterase activity in the fusiform gyrus in adults with autism spectrum disorders. Arch Gen Psychiatry. 2011;68(3):306-13.
86. Pierce K, Muller RA, Ambrose J, Allen G, Courchesne E. Face processing occurs outside the fusiform 'face area' in autism: evidence from functional MRI. Brain. 2001;124(Pt 10):2059-73.
87. Riedl V, Bienkowska K, Strobel C, Tahmasian M, Grimmer T, Forster S, et al. Local activity determines functional connectivity in the resting human brain: a simultaneous FDG-PET/fMRI study. J Neurosci. 2014;34(18):6260-6.
88. Beucke JC, Sepulcre J, Talukdar T, Linnman C, Zschenderlein K, Endrass T, et al. Abnormally high degree connectivity of the orbitofrontal cortex in obsessive-compulsive disorder. JAMA Psychiatry. 2013;70(6):619-29.
89. 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(11):1885-93.
90. McAlonan GM, Suckling J, Wong N, Cheung V, Lienenkaemper N, Cheung C, et al. Distinct patterns of grey matter abnormality in high-functioning autism and Asperger's syndrome. J Child Psychol Psychiatry. 2008;49(12):1287-95.
91. Via E, Radua J, Cardoner N, Happe F, Mataix-Cols D. Meta-analysis of gray matter abnormalities in autism spectrum disorder: should Asperger disorder be subsumed under a broader umbrella of autistic spectrum disorder? Arch Gen Psychiatry. 2011;68(4):409-18.