The perils of global signal regression for group comparisons: A case study of Autism Spectrum Disorders

Frontiers in Human Neuroscience

Volumn , Issue JUL, 2013, Pages

  Gotts, Stephen J ^a   Saad, Ziad S ^a   Jo, Hang Joon ^a   Wallace, Gregory L ^a   Cox, Robert W ^a   Martin, Alex ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

Artifact; Functional connectivity; GCOR; Global correlation; Resting state fMRI; Typically developing

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; AUTISM; BEHAVIOR DISORDER; BRAIN VENTRICLE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CRANIAL SINUS; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; GLOBAL SIGNAL REGRESSION; HUMAN; MALE; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE SCANNER; PREDICTION; REGRESSION ANALYSIS; SCHOOL CHILD; SIGNAL PROCESSING; WHITE MATTER;

EID: 84887546061     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2013.00356     Document Type: Article

References (68)

1. Anderson, J. S., Druzgal, T. J., Lopez-Larson, M., Jeong, E.-K., Desai, K., and Yurgelun-Todd, D. (2011a). Network anticorrelations, global regression, and phase-shifted soft tissue correction. Hum. Brain Mapp. 32, 919-934. doi: 10.1002/hbm.21079
2. Anderson, J. S., Nielsen, J. A., Froehlich, A. L., DuBray, M. B., Druzgal, T. J., Cariello, A. N., et al. (2011b). Functional connectivity magnetic resonance imaging classification of autism. Brain 134, 3742-3754. doi: 10.1093/brain/awr263
3. Assaf, M., Jagannathan, K., Calhoun, V. D., Miller, L., Stevens, M. C., Sahl, R., et al. (2010). Abnormal functional connectivity of default mode sub-networks in autism spectrum disorder patients. Neuroimage 53, 247-256. doi: 10.1016/j.neuroimage.2010.05.067
4. Belmonte, M. K., Allen, G., Beckel-Mitchener, A., Boulanger, L. M., Carper, R. A., and Webb, S. J. (2004). Autism and abnormal development of brain connectivity. J. Neurosci. 24, 9228-9231. doi: 10.1523/JNEUROSCI.3340-04.2004
5. Birn, R. M., Diamond, J. B., Smith, M. A., and Bandettini, P. A. (2006). Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI. Neuroimage 31, 1536-1548. doi: 10.1016/j.neuroimage.2006.02.048
6. Birn, R. M., Smith, M. A., Jones, T. B., and Bandettini, P. A. (2008). The respiration response function: the temporal dynamics of fMRI signal fluctuations related to changes in respiration. Neuroimage 40, 644-654. doi: 10.1016/j.neuroimage.2007.11.059
7. Buckner, R. L., Sepulcre, J., Talukdar, T., Krienen, F. M., Liu, H., Hedden, T., et al. (2009). Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. J. Neurosci. 29, 1860-1873. doi: 10.1523/JNEUROSCI.5062-08.2009
8. Castelli, F., Frith, C., Happe, F., and Frith, U. (2002). Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. Brain 125, 1839-1849. doi: 10.1093/brain/awf189
9. Chang, C., Cunningham, J. P., and Glover, G. H. (2009). Influence of heart rate on the BOLD signal: The cardiac response function. Neuroimage 44, 857-869. doi: 10.1016/j.neuroimage.2008.09.029
10. Chang, C., and Glover, G. H. (2009). Relationship between respiration, end-tidal CO2, and BOLD signals in resting-state fMRI. Neuroimage 47, 1381-1393. doi: 10.1016/j.neuroimage.2009.04.048
11. Cole, M. W., Pathak, S., and Schneider, W. (2010). Identifying the brain's most globally connected regions. Neuroimage 49, 3132-3148. doi: 10.1016/j.neuroimage.2009.11.001
12. Constantino, J. N. (2002). The Social Responsiveness Scale. Los Angeles, CA: Western Psychological Services.
13. Cordes, D., Haughton, V., Carew, J. D., Arfanakis, K., and Maravilla, K. (2002). Hierarchical clustering to measure connectivity in fMRI resting-state data. Magn. Reson. Imaging 20, 305-317. doi: 10.1016/S0730-725X(02)00503-9
14. Cox, R. W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Comp. Biomed. Res. 29, 162-173. doi: 10.1006/cbmr.1996.0014
15. Deen, B., and Pelphrey, K. (2012). Perspective: Brain scans need a rethink. Nature491, S20. doi: 10.1038/491S20a
16. Di Martino, A., Ross, K., Uddin, L. Q., Sklar, A. B., Castellanos, F. X., and Milham, M. P. (2009). Functional brain correlates of social and nonsocial processes in autism spectrum disorders: an activation likelihood estimation meta-analysis. Biol. Psychiatry 65, 63-74. doi: 10.1016/j.biopsych.2008.09.022
17. Di Martino, A., Zuo, X. N., Kelly, C., Grzadzinski, R., Mennes, M., Schvarcz, A., et al. (2013). Shared and distinct intrinsic functional network centrality in autism and attention-deficit/hyperactivity disorder. Biol. Psychiatry. doi: 10.1016/j.biopsych.2013.02.011. [Epub ahead of print].
18. Dinstein, I., Pierce, K., Eyler, L., Solso, S., Malach, R., Behrmann, M., et al. (2011). Disrupted neural synchronization in toddlers with autism. Neuron 70, 1218-1225. doi: 10.1016/j.neuron.2011.04.018
19. Ebisch, S. J., Gallese, V., Willems, R. M., Mantini, D., Groen, W. B., Romani, G. L., et al. (2011). Altered intrinsic functional connectivity of anterior and posterior insula regions in high-functioning participants with autism spectrum disorder. Hum. Brain Mapp. 32, 1013-1028. doi: 10.1002/hbm.21085
20. Fischl, B., Salat, D. H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., et al. (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341-355. doi: 10.1016/S0896-6273(02)00569-X
21. Fox, M. D., and Greicius, M. (2010). Clinical applications of resting state functional connectivity. Front. Syst. Neurosci. 4:19. doi: 10.3389/fnsys.2010.00019
22. Fox, M. D., and Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 8, 700-711. doi: 10.1038/nrn2201
23. Fox, M. D., Zhang, D., Snyder, A. Z., and Raichle, M. E. (2009). The global signal and observed anticorrelated resting state brain networks. J. Neurophysiol. 101, 3270-3283. doi: 10.1152/jn.90777.2008
24. Fransson, P., Skiold, B., Horsch, S., Nordell, A., Blennow, M., Lagercrantz, H., et al. (2007). Resting-state networks in the infant brain. Proc. Natl. Acad. Sci. U.S.A. 104, 15531-15536. doi: 10.1073/pnas.0704380104
25. Glover, G. H., Li, T. Q., and Ress, D. (2000). Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn. Reson. Med. 44, 162-167.
26. Gotts, S. J., Simmons, W. K., Milbury, L. A., Wallace, G. L., Cox, R. W., and Martin, A. (2012). Fractionation of social brain circuits in autism spectrum disorders. Brain 135, 2711-2725. doi: 10.1093/brain/aws160
27. Jiang, X., Bollich, A., Cox, P., Hyder, E., James, J., Gowani, S. A., et al. (2013). A quantitative link between face discrimination deficits and neuronal selectivity for faces in autism. Neuroimage Clin. 2, 320-331. doi: 10.1016/j.nicl.2013.02.002
28. Jo, H. J., Gotts, S. J., Reynolds, R. C., Bandettini, P. A., Martin, A., and Cox, R. W. (2013). Effective preprocessing procedures virtually eliminate distance-dependent motion artifacts in resting state FMRI. J. Appl. Math. 2013, 9. doi: 10.1155/2013/935154
29. Jo, H. J., Saad, Z. S., Simmons, W. K., Milbury, L. A., and Cox, R. W. (2010). Mapping sources of correlation in resting state FMRI, with artifact detection and removal. Neuroimage 52, 571-582. doi: 10.1016/j.neuroimage.2010.04.246
30. Jones, T. B., Bandettini, P. A., Kenworthy, L., Case, L. K., Milleville, S. C., Martin, A., et al. (2010). Sources of group differences in functional connectivity: an investigation applied to autism spectrum disorder. Neuroimage 49, 401-414. doi: 10.1016/j.neuroimage.2009.07.051
31. Just, M. A., Cherkassky, V. L., Keller, T. A., and Minshew, N. J. (2004). Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain 127, 1811-1821. doi: 10.1093/brain/awh199
32. Kaiser, M. D., Hudac, C. M., Shultz, S., Lee, S. M., Cheung, C., Berken, A. M., et al. (2010). Neural signatures of autism. Proc. Natl. Acad. Sci. U.S.A. 107, 21223-21228. doi: 10.1073/pnas.1010412107
33. Keller, C. J., Bickel, S., Honey, C. J., Groppe, D. M., Entz, L., Craddock, R. C., et al. (2013). Neurophysiological investigation of spontaneous correlated and anticorrelated fluctuations of the BOLD signal. J. Neurosci. 33, 6333-6342. doi: 10.1523/JNEUROSCI.4837-12.2013
34. Kennedy, D. P., and Courchesne, E. (2008). Functional abnormalities of the default network during self-and other-reflection in autism. Soc. Cogn. Affect. Neurosci. 3, 177-190. doi: 10.1093/scan/nsn011
35. Khan, S., Gramfort, A., Shetty, N. R., Kitzbichler, M. G., Ganesan, S., Moran, J. M., et al. (2013). Local and long-range functional connectivity is reduced in concert in autism spectrum disorders. Proc. Natl. Acad. Sci. U.S.A. 110, 3107-3112. doi: 10.1073/pnas.1214533110
36. Kundu, P., Inati, S. J., Evans, J. W., Luh, W. M., and Bandettini, P. A. (2012). Differentiating BOLD and non-BOLD signals in fMRI time series using multi-echo EPI. Neuroimage 60, 1759-1770. doi: 10.1016/j.neuroimage.2011.12.028
37. Lainhart, J. E., Bigler, E. D., Bocian, M., Coon, H., Dinh, E., Dawson, G., et al. (2006). Head circumference and height in autism: a study by the Collaborative Program of Excellence in Autism. Am. J. Med. Genet. A 140, 2257-2274. doi: 10.1002/ajmg.a.31465
38. Le Couteur, A., Rutter, M., Lord, C., Rios, P., Robertson, S., Holdgrafer, M., et al. (1989). Autism diagnostic interview: a standardized investigator-based instrument. J. Autism Dev. Disord. 19, 363-387. doi: 10.1007/BF02212936
39. Lombardo, M. V., Chakrabarti, B., Bullmore, E. T., Sadek, S. A., Pasco, G., Wheelwright, S. J., et al. (2010). Atypical neural self-representation in autism. Brain 133, 611-624. doi: 10.1093/brain/awp306
40. Lord, C., Risi, S., Lambrecht, L., Cook, E. H. Jr., Leventhal, B. L., Dilavore, P. C., et al. (2000). The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J. Autism Dev. Disord. 30, 205-223. doi: 10.1023/A:1005592401947
41. Lord, C., Rutter, M., and Le Couteur, A. (1994). Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J. Autism Dev. Disord. 24, 659-685. doi: 10.1007/BF02172145
42. Margulies, D. S., Vincent, J. L., Kelly, C., Lohmann, G., Uddin, L. Q., Biswal, B. B., et al. (2009). Precuneus shares intrinsic functional architecture in humans and monkeys. Proc. Natl. Acad. Sci. U.S.A. 106, 20069-20074.
43. Maris, E., and Oostenveld, R. (2007). Nonparametric statistical testing of EEG-and MEG-data. J. Neurosci. Methods 25, 2862-2874.
44. Monk, C. S., Peltier, S. J., Wiggins, J. L., Weng, S. J., Carrasco, M., Risi, S., et al. (2009). Abnormalities of intrinsic functional connectivity in autism spectrum disorders. Neuroimage 47, 764-772. doi: 10.1016/j.neuroimage.2009.04.069
45. Müller, R. A., Shih, P., Keehn, B., Deyoe, J. R., Leyden, K. M., and Shukla, D. K. (2011). Underconnected, but how? A survey of functional connectivity MRI studies in autism spectrum disorders. Cereb. Cortex 21, 2233-2243. doi: 10.1093/cercor/bhq296
46. Murphy, K., Birn, R. M., Handwerker, D. A., Jones, T. B., and Bandettini, P. A. (2009). The impact of global signal regression on resting state correlations: are anti-correlated networks introduced? Neuroimage 44, 893-905. doi: 10.1016/j.neuroimage.2008.09.036
47. Paakki, J. J., Rahko, J., Long, X., Moilanen, I., Tervonen, O., Nikkinen, J., et al. (2010). Alteration in regional homogeneity of resting-state brain activity in autism spectrum disorders. Brain Res. 1321, 169-179. doi: 10.1016/j.brainres.2009.12.081
48. Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., and Petersen, S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59, 2142-2154. doi: 10.1016/j.neuroimage.2011.10.018
49. Rudie, J. D., Brown, J. A., Beck-Pancer, D., Hernandez, L. M., Dennis, E. L., Thompson, P. M., et al. (2013). Altered functional and structural brain network organization in autism. Neuroimage Clin. 2, 79-94. doi: 10.1016/j.nicl.2012.11.006
50. Saad, Z. S., Gotts, S. J., Murphy, K., Chen, G., Jo, H. J., Martin, A., et al. (2012). Trouble at rest: how correlation patterns and group differences become distorted after global signal regression. Brain Connect. 2, 25-32. doi: 10.1089/brain.2012.0080
51. Saad, Z. S., Reynolds, R. C., Jo, H. J., Gotts, S. J., Chen, G., Martin, A., et al. (2013). Correcting brain-wide correlation differences in resting-state FMRI. Brain Connect. doi: 10.1089/brain.2013.0156. [Epub ahead of print].
52. Salomon, R., Bleich-Cohen, M., Hahamy-Dubossarsky, A., Dinstien, I., Weizman, R., Poyurovsky, M., et al. (2011). Global functional connectivity deficits in schizophrenia depend on behavioral state. J. Neurosci. 31, 12972-12981. doi: 10.1523/JNEUROSCI.2987-11.2011
53. Satterthwaite, T. D., Elliott, M. A., Gerraty, R. T., Ruparel, K., Loughead, J., Calkins, M. E., 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. doi: 10.1016/j.neuroimage.2012.08.052
54. Satterthwaite, T. D., Wolf, D. H., Loughead, J., Ruparel, K., Elliott, M. A., Hakonarson, H., et al. (2012). Impact of in-scanner head motion on multiple measures of functional connectivity: relevance for studies of neurodevelopment in youth. Neuroimage 60, 623-632. doi: 10.1016/j.neuroimage.2011.12.063
55. Schölvinck, M. L., Maier, A., Ye, F. Q., Duyn, J. H., and Leopold, D. A. (2010). Neural basis of global resting-state fMRI activity. Proc. Natl. Acad. Sci. U.S.A. 107, 10238-10243. doi: 10.1073/pnas.0913110107
56. Shmueli, K., Van Gelderen, P., De Zwart, J. A., Horovitz, S. G., Fukunaga, M., Jansma, J. M., et al. (2007). Low-frequency fluctuations in the cardiac rate as a source of variance in the resting-state fMRI BOLD signal. Neuroimage 38, 306-320. doi: 10.1016/j.neuroimage.2007.07.037
57. Shukla, D. K., Keehn, B., and Müller, R. A. (2010). Regional homogeneity of fMRI time series in autism spectrum disorders. Neurosci. Lett. 26, 46-51. doi: 10.1016/j.neulet.2010.03.080
58. Snyder, A. Z., and Raichle, M. E. (2012). A brief history of the resting state: the Washington University perspective. Neuroimage 62, 902-910. doi: 10.1016/j.neuroimage.2012.01.044
59. Talairach, J., and Tournoux, P. (1988). Co-planar Stereotaxic Atlas of the Human Brain. New York, NY: Thieme Medical Publishers.
60. Tyszka, J. M., Kennedy, D. P., Paul, L. K., and Adolphs, R. (2013). Largely typical patterns of resting-state functional connectivity in high-functioning adults with autism. Cereb. Cortex. doi: 10.1093/cercor/bht040. [Epub ahead of print].
61. Van Dijk, K. R., Sabuncu, M. R., and Buckner, R. L. (2012). The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 59, 431-438. doi: 10.1016/j.neuroimage.2011.07.044
62. Vincent, J. L., Patel, G. H., Fox, M. D., Snyder, A. Z., Baker, J. T., Van Essen, D. C., et al. (2007). Intrinsic functional architecture in the anaesthetized monkey brain. Nature447, 83-86. doi: 10.1038/nature05758
63. von dem Hagen, E. A., Stoyanova, R. S., Baron-Cohen, S., and Calder, A. J. (2012). Reduced functional connectivity within and between 'social' resting state networks in autism spectrum conditions. Soc. Cogn. Affect. Neurosci. doi: 10.1093/scan/nss053. [Epub ahead of print].
64. Weisberg, J., Milleville, S. C., Kenworthy, L., Wallace, G. L., Gotts, S. J., Beauchamp, M. S., et al. (2012). Social Perception in Autism Spectrum Disorders: impaired category selectivity for dynamic but not static images in ventral temporal cortex. Cereb. Cortex. doi: 10.1093/cercor/bhs276. [Epub ahead of print].
65. Weng, S. J., Wiggins, J. L., Peltier, S. J., Carrasco, M., Risi, S., Lord, C., et al. (2010). Alterations of resting state functional connectivity in the default network in adolescents with autism spectrum disorders. Brain Res. 1313, 202-214. doi: 10.1016/j.brainres.2009.11.057
66. Yan, C.-G., Cheung, B., Kelly, C., Colcombe, S., Craddock, R. C., Di Martino, A., et al. (2013). A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. Neuroimage 76C, 183-201. doi: 10.1016/j.neuroimage.2013.03.004
67. Yan, C.-G., Craddock, R. C., Zuo, X.-N., Zang, Y.-F., and Milham, M. P. (2013). Standardizing the intrinsic brain: Towards robust measurement of inter-individual variation in 1000 functional connectomes. Neuroimage doi: 10.1016/j.neuroimage.2013.04.081. [Epub ahead of print].
68. Zang, Y., Jiang, T., Lu, Y., He, Y., and Tian, L. (2004). Regional homogeneity approach to fMRI data analysis. Neuroimage 22, 394-400. doi: 10.1016/j.neuroimage.2003.12.030