Underconnected, But Not Broken? Dynamic Functional Connectivity MRI Shows Underconnectivity in Autism Is Linked to Increased Intra-Individual Variability Across Time

Brain Connectivity

Volumn 6, Issue 5, 2016, Pages 403-414

  Falahpour, Maryam ^a   Thompson, Wesley K ^b   Abbott, Angela E ^c   Jahedi, Afrooz ^c   Mulvey, Mark E ^c   Datko, Michael ^c,d   Liu, Thomas T ^a   Müller, Ralph Axel ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SAN DIEGO STATE UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

autism spectrum disorder; default mode network; fMRI; functional connectivity; intra individual variability; mediation analysis; resting state

Indexed keywords

ADULT; AMYGDALA; ANTERIOR CINGULATE; ANTERIOR INSULA; ARTICLE; AUTISM; BRAIN REGION; COMPARATIVE STUDY; CONNECTOME; CONTROLLED STUDY; DEFAULT MODE NETWORK; DORSAL ANTERIOR CINGULATE CORTEX; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HIPPOCAMPUS; HUMAN; INTRINSIC FUNCTIONAL CONNECTIVITY; MAJOR CLINICAL STUDY; MALE; MEDIAL PREFRONTAL CORTEX; PARIETAL CORTEX; POSTERIOR CINGULATE; PRIORITY JOURNAL; SALIENCE NETWORK; THALAMUS; ADOLESCENT; BRAIN; BRAIN CORTEX; BRAIN MAPPING; CHILD; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PROCEDURES; YOUNG ADULT;

ADOLESCENT; ADULT; AMYGDALA; AUTISM SPECTRUM DISORDER; AUTISTIC DISORDER; BRAIN; BRAIN MAPPING; CEREBRAL CORTEX; CHILD; CONNECTOME; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; THALAMUS; YOUNG ADULT;

EID: 85006206561     PISSN: 21580014     EISSN: 21580022     Source Type: Journal    
DOI: 10.1089/brain.2015.0389     Document Type: Article

References (82)

1. Abbott AE, Nair A, Keown CL, Datko MC, Jahedi A, Fishman I, et al. 2015. Patterns of atypical functional connectivity and behavioral links in autism differ between default, salience, and executive networks. Cerebral Cortex. DOI: 10.1093/cercor/bhv191.
2. Abrams DA, Lynch CJ, Cheng KM, Phillips J, Supekar K, Ryali S, et al. 2013. Underconnectivity between voice-selective cortex and reward circuitry in children with autism. Proc Natl Acad Sci U S A 110:12060-12065.
3. Allen EA, Damaraju E, Plis SM, Erhardt EB, Eichele T, Calhoun VD. 2014. Tracking whole-brain connectivity dynamics in the resting state. Cereb Cortex 24:663-676.
4. Anticevic A, Repovs G, Shulman GL, Barch DM. 2010. When less is more: TPJ and default network deactivation during encoding predicts working memory performance. Neuroimage 49:2638-2648.
5. Assaf M, Jagannathan K, Calhoun VD, Miller L, Stevens MC, Sahl R, et al. 2010. Abnormal functional connectivity of default mode sub-networks in autism spectrum disorder patients. Neuroimage 53:247-256.
6. Buckner RL, Krienen FM, Yeo BT. 2013. Opportunities and limitations of intrinsic functional connectivity MRI. Nat Neurosci 16:832-837.
7. Buzsáki G, Freeman W. 2015. Editorial overview: brain rhythms and dynamic coordination. Curr Opin Neurobiol 31:v-ix.
8. CDC. 2015. Estimated prevalence of autism and other developmental disabilities following questionnaire changes in the 2014 National Health Interview Survey. National Health Statistics Reports 87:1-20.
9. Cerliani L, Mennes M, Thomas RM, Di Martino A, Thioux M, Keysers C. 2015. Increased functional connectivity between subcortical and cortical resting-state networks in autism spectrum disorder. JAMA Psychiatry 72:767-777.
10. Chang C, Glover GH. 2010. Time-frequency dynamics of resting-state brain connectivity measured with fMRI. Neuroimage 50:81-98.
11. Chang C, Liu Z, Chen MC, Liu X, Duyn JH. 2013a. EEG correlates of time-varying BOLD functional connectivity. Neuroimage 72:227-236.
12. Chang C, Metzger CD, Glover GH, Duyn JH, Heinze HJ, Walter M. 2013b. Association between heart rate variability and fluctuations in resting-state functional connectivity. Neuroimage 68:93-104.
13. Cox RW. 1996. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed 29:162-173.
14. Di Martino A, Kelly C, Grzadzinski R, Zuo XN, Mennes M, Mairena MA, et al. 2011. Aberrant striatal functional connectivity in children with autism. Biol Psychiatry 69:847-856.
15. Di Martino A, Ross K, Uddin LQ, Sklar AB, Castellanos FX, Milham MP. 2009. Functional brain correlates of social and nonsocial processes in autism spectrum disorders: an activation likelihood estimation meta-analysis. Biol Psychiatry 65:63-74.
16. Di Martino A, Yan CG, Li Q, Denio E, Castellanos FX, Alaerts K, et al. 2014. The autism brain imaging data exchange: towards a large-scale evaluation of the intrinsic brain architecture in autism. Mol Psychiatry 19:659-667.
17. Dinstein I, Heeger DJ, Lorenzi L, Minshew NJ, Malach R, Behrmann M. 2012. Unreliable evoked responses in autism. Neuron 75:981-991.
18. Doyle-Thomas KA, Lee W, Foster NE, Tryfon A, Ouimet T, Hyde KL, et al. 2015. Atypical functional brain connectivity during rest in autism spectrum disorders. Ann Neurol 77:866-876.
19. Ebisch SJ, Gallese V, Willems RM, Mantini D, Groen WB, Romani GL, et al. 2011. Altered intrinsic functional connectivity of anterior and posterior insula regions in highfunctioning participants with autism spectrum disorder. Hum Brain Mapp 32:1013-1028.
20. Fishman I, Datko M, Cabrera Y, Carper RA, Müller R-A. 2015. Reduced integration and differentiation of the imitation network in autism: a combined functional connectivity magnetic resonance imaging and diffusion-weighted imaging study. Ann Neurol 78:958-969.
21. Fishman I, Keown CL, Lincoln AJ, Pineda JA, Müller R-A. 2014. Atypical cross talk between mentalizing and mirror neuron networks in autism spectrum disorder. JAMA Psychiatry 71:751-760.
22. Fox MD, Snyder AZ, Vincent JL, Raichle ME. 2007. Intrinsic fluctuations within cortical systems account for intertrial variability in human behavior. Neuron 56:171-184.
23. Fox MD, Snyder AZ, Zacks JM, Raichle ME. 2006. Coherent spontaneous activity accounts for trial-to-trial variability in human evoked brain responses. Nat Neurosci 9:23-25.
24. Geschwind DH, Levitt P. 2007. Autism spectrum disorders: developmental disconnection syndromes. Curr Opin Neurobiol 17:103-111.
25. Geurts HM, Grasman RP, Verte S, Oosterlaan J, Roeyers H, van Kammen SM, et al. 2008. Intra-individual variability in ADHD, autism spectrum disorders and Tourette's syndrome. Neuropsychologia 46:3030-3041.
26. Gotts SJ, Simmons WK, Milbury LA, Wallace GL, Cox RW, Martin A. 2012. Fractionation of social brain circuits in autism spectrum disorders. Brain 135(Pt 9):2711-2725.
27. Grelotti DJ, Klin AJ, Gauthier I, Skudlarski P, Cohen DJ, Gore JC, et al. 2005. fMRI activation of the fusiform gyrus and amygdala to cartoon characters but not to faces in a boy with autism. Neuropsychologia 43:373-385.
28. Haigh SM, Heeger DJ, Dinstein I, Minshew N, Behrmann M. 2014. Cortical variability in the sensory-evoked response in autism. J Autism Dev Disord 45:1176-1190.
29. Handwerker DA, Roopchansingh V, Gonzalez-Castillo J, Bandettini PA. 2012. "Periodic changes in fMRI connectivity. Neuroimage 63:1712-1719.
30. Hardan AY, Minshew NJ, Melhem NM, Srihari S, Jo B, Bansal R, et al. 2008. An MRI and proton spectroscopy study of the thalamus in children with autism. Psychiatry Res 163:97-105.
31. Hinds O, Thompson TW, Ghosh S, Yoo JJ, Whitfield-Gabrieli S, Triantafyllou C, et al. 2013. Roles of default-mode network and supplementary motor area in human vigilance performance: evidence from real-time fMRI. J Neurophysiol 109:1250-1258.
32. Honey CJ, Sporns O, Cammoun L, Gigandet X, Thiran JP, Meuli R, et al. 2009. Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci U S A 106:2035-2040.
33. Hughes JR. 2007. Autism: the first firm finding = underconnectivity? Epilepsy Behav 11:20-24.
34. Hutchison RM, Womelsdorf T, Allen EA, Bandettini PA, Calhoun VD, Corbetta M, et al. 2013. Dynamic functional connectivity: promise, issues, and interpretations. Neuroimage 80:360-378.
35. Jann K, Federspiel A, Giezendanner S, Andreotti J, Kottlow M, Dierks T, et al. 2012. Linking brain connectivity across different time scales with electroencephalogram, functional magnetic resonance imaging, and diffusion tensor imaging. Brain Connect 2:11-20.
36. Jo HJ, Saad ZS, Simmons WK, Milbury LA, Cox RW. 2010. Mapping sources of correlation in resting state FMRI, with artifact detection and removal. Neuroimage 52:571-582.
37. Jolles DD, van Buchem MA, Crone EA, Rombouts SA. 2013. Functional brain connectivity at rest changes after working memory training. Hum Brain Mapp 34:396-406.
38. Just MA, Cherkassky VL, Keller TA, Minshew NJ. 2004. Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain 127(Pt 8):1811-1821.
39. Just MA, Keller TA, Malave VL, Kana RK, Varma S. 2012. Autism as a neural systems disorder: a theory of frontalposterior underconnectivity. Neurosci Biobehav Rev 36: 1292-1313.
40. Kana RK, Keller TA, Minshew NJ, Just MA. 2007. Inhibitory control in high-functioning autism: decreased activation and underconnectivity in inhibition networks. Biol Psychiatry 62:198-206.
41. Kelly AM, Uddin LQ, Biswal BB, Castellanos FX, Milham MP. 2008. Competition between functional brain networks mediates behavioral variability. Neuroimage 39:527-537.
42. Kennedy DP, Courchesne E. 2008. The intrinsic functional organization of the brain is altered in autism. Neuroimage 39:1877-1885.
43. Khan AJ, Nair A, Keown CL, Datko MC, Lincoln AJ, Müller RA. 2015. Cerebro-cerebellar resting state functional connectivity in children and adolescents with autism spectrum disorder. Biol Psychiatry 78:625-634.
44. Kleinhans NM, Richards T, Johnson LC, Weaver KE, Greenson J, Dawson G, et al. 2011. fMRI evidence of neural abnormalities in the subcortical face processing system in ASD. Neuroimage 54:697-704.
45. Kleinhans NM, Richards T, Sterling L, Stegbauer KC, Mahurin R, Johnson LC, et al. 2008. Abnormal functional connectivity in autism spectrum disorders during face processing. Brain 131(Pt 4):1000-1012.
46. Laufs H, Krakow K, Sterzer P, Eger E, Beyerle A, Salek-Haddadi A, et al. 2003. Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest. Proc Natl Acad Sci U S A 100:11053-11058.
47. Lewis CM, Baldassarre A, Committeri G, Romani GL, Corbetta M. 2009. Learning sculpts the spontaneous activity of the resting human brain. Proc Natl Acad Sci U S A 106: 17558-17563.
48. Lynch CJ, Uddin LQ, Supekar K, Khouzam A, Phillips J, Menon V. 2013. Default mode network in childhood autism: posteromedial cortex heterogeneity and relationship with social deficits. Biol Psychiatry 74:212-219.
49. MacDonald SW, Nyberg L, Backman L. 2006. Intra-individual variability in behavior: links to brain structure, neurotransmission and neuronal activity. Trends Neurosci 29:474-480.
50. MacKinnon DP, Fairchild AJ, Fritz MS. 2007. Mediation analysis. Ann Rev Psychol 58:593-614.
51. Mason MF, Norton MI, Van Horn JD, Wegner DM, Grafton ST, Macrae CN. 2007. Wandering minds: the default network and stimulus-independent thought. Science 315:393-395.
52. Mennes M, Zuo XN, Kelly C, Di Martino A, Zang YF, Biswal B, et al. 2011. Linking inter-individual differences in neural activation and behavior to intrinsic brain dynamics. Neuroimage 54:2950-2959.
53. Milne E. 2011. Increased intra-participant variability in children with autistic spectrum disorders: evidence from single-trial analysis of evoked EEG. Front Psychol 2:51.
54. Monk CS, Peltier SJ, Wiggins JL, Weng SJ, Carrasco M, Risi S, et al. 2009. Abnormalities of intrinsic functional connectivity in autism spectrum disorders. Neuroimage 47:764-772.
55. Müller R-A, Shih P, Keehn B, Deyoe JR, Leyden KM, Shukla DK. 2011. Underconnected, but how? A survey of functional connectivity MRI studies in autism spectrum disorders. Cerebral Cortex 21:2233-2243.
56. Murphy ER, Foss-Feig J, Kenworthy L, Gaillard WD, Vaidya CJ. 2012. Atypical functional connectivity of the amygdala in childhood autism spectrum disorders during spontaneous attention to eye-gaze. Autism Res Treat 2012:652408.
57. Nair A, Carper RA, Abbott AE, Chen CP, Solders S, Nakutin S, et al. 2015. Regional specificity of aberrant thalamocortical connectivity in autism. Hum Brain Mapp 36:4497-4511.
58. Nair A, Keown CL, Datko M, Shih P, Keehn B, Müller RA. 2014. Impact of methodological variables on functional connectivity findings in autism spectrum disorders. Hum Brain Mapp 35:4035-4048.
59. Nair A, Treiber JM, Shukla DK, Shih P, Müller R-A. 2013. Thalamocortical connectivity in autism spectrum disorder: a study of functional and anatomical connectivity. Brain 136(Pt 6):1942-1955.
60. Olafsson V, Kundu P, Wong EC, Bandettini PA, Liu TT. 2015. Enhanced identification of BOLD-like components with multi-echo simultaneous multi-slice (MESMS) fMRI and multi-echo ICA. Neuroimage 112:43-51.
61. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE. 2012. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuro-Image 59:2142-2154.
62. Power JD, Mitra A, Laumann TO, Snyder AZ, Schlaggar BL, Petersen SE. 2014. Methods to detect, characterize, and remove motion artifact in resting state fMRI. NeuroImage 84:320-341.
63. Power JD, Schlaggar BL, Petersen SE. 2015. Recent progress and outstanding issues in motion correction in resting state fMRI. Neuroimage 105C:536-551.
64. Rack-Gomer AL, Liu TT. 2012. Caffeine increases the temporal variability of resting-state BOLD connectivity in the motor cortex. Neuroimage 59:2994-3002.
65. Sadaghiani S, Scheeringa R, Lehongre K, Morillon B, Giraud AL, Kleinschmidt A. 2010. Intrinsic connectivity networks, alpha oscillations, and tonic alertness: a simultaneous electroencephalography/functional magnetic resonance imaging study. J Neurosci 30:10243-10250.
66. Satterthwaite TD, Elliott MA, et al. 2013. An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. NeuroImage 64:240-256.
67. Schölvinck ML, Maier A, Ye FQ, Duyn JH, Leopold DA. 2010. Neural basis of global resting-state fMRI activity. Proc Natl Acad Sci U S A 107:10238-10243.
68. Sekhon JS. 2011. Multivariate and propensity score matching software with automated balance optimization: the matching package for R. J Stat Softw 42:1-52.
69. Shehzad Z, Kelly AM, Reiss PT, Gee DG, Gotimer K, Uddin LQ, et al. 2009. The resting brain: unconstrained yet reliable. Cereb Cortex 19:2209-2229.
70. Shih P, Keehn B, Oram JK, Leyden KM, Keown CL, Müller R-A. 2011. Functional differentiation of posterior superior temporal sulcus in autism: a functional connectivity magnetic resonance imaging study. Biol Psychiatry 70:270-277.
71. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, et al. 2004. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23(Suppl. 1):S208-S219.
72. Stevens WD, Buckner RL, Schacter DL. 2010. Correlated lowfrequency BOLD fluctuations in the resting human brain are modulated by recent experience in category-preferential visual regions. Cereb Cortex 20:1997-2006.
73. Supekar K, Uddin LQ, Khouzam A, Phillips J, Gaillard WD, Kenworthy LE, et al. 2013. Brain hyperconnectivity in children with autism and its links with social deficits. Cell Rep 5:738-747.
74. Tagliazucchi E, von Wegner F, Morzelewski A, Brodbeck V, Laufs H. 2012. Dynamic BOLD functional connectivity in humans and its electrophysiological correlates. Front Hum Neurosci 6:339.
75. Tyszka JM, Kennedy DP, Paul LK, Adolphs R. 2014. Largely typical patterns of resting-state functional connectivity in highfunctioning adults with autism. Cereb Cortex 24:1894-1905.
76. Uddin LQ, Supekar K, Lynch CJ, Khouzam A, Phillips J, Feinstein C, et al. 2013a. Salience network-based classification and prediction of symptom severity in children with autism. JAMA Psychiatry 70:869-879.
77. Uddin LQ, Supekar K, Menon V. 2013b. Reconceptualizing functional brain connectivity in autism from a developmental perspective. Front Hum Neurosci 7:458.
78. Van Dijk KR, Hedden T, Venkataraman A, Evans KC, Lazar SW, Buckner RL. 2010. Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. J Neurophysiol 103:297-321.
79. von dem Hagen EA, Stoyanova RS, Baron-Cohen S, Calder AJ. 2012. Reduced functional connectivity within and between 'social' resting state networks in autism spectrum conditions. Soc Cogn Affect Neurosci 8:694-701.
80. Wang L, Saalmann YB, Pinsk MA, Arcaro MJ, Kastner S. 2012. Electrophysiological low-frequency coherence and crossfrequency coupling contribute to BOLD connectivity. Neuron 76:1010-1020.
81. Washington SD, Gordon EM, Brar J, Warburton S, Sawyer AT, Wolfe A, et al. 2013. Dysmaturation of the default mode network in autism. Hum Brain Mapp 35:1284-1296.
82. Wass S. 2011. Distortions and disconnections: disrupted brain connectivity in autism. Brain Cogn 75:18-28.