Tourette; basal ganglia; cortico-striato-thalamo-cortical circuit; resting state networks; tics
Abstract :
[en] INTRODUCTION: Tourette syndrome (TS) is a neuropsychiatric disorder with the core phenomenon of tics, whose origin and temporal pattern are unclear. We investigated the When and Where of tic generation and resting state networks (RSNs) via functional magnetic resonance imaging (fMRI). METHODS: Tic-related activity and the underlying RSNs in adult TS were studied within one fMRI session. Participants were instructed to lie in the scanner and to let tics occur freely. Tic onset times, as determined by video-observance were used as regressors and added to preceding time-bins of 1 s duration each to detect prior activation. RSN were identified by independent component analysis (ICA) and correlated to disease severity by the means of dual regression. RESULTS: Two seconds before a tic, the supplementary motor area (SMA), ventral primary motor cortex, primary sensorimotor cortex and parietal operculum exhibited activation; 1 s before a tic, the anterior cingulate, putamen, insula, amygdala, cerebellum and the extrastriatal-visual cortex exhibited activation; with tic-onset, the thalamus, central operculum, primary motor and somatosensory cortices exhibited activation. Analysis of resting state data resulted in 21 components including the so-called default-mode network. Network strength in those regions in SMA of two premotor ICA maps that were also active prior to tic occurrence, correlated significantly with disease severity according to the Yale Global Tic Severity Scale (YGTTS) scores. DISCUSSION: We demonstrate that the temporal pattern of tic generation follows the cortico-striato-thalamo-cortical circuit, and that cortical structures precede subcortical activation. The analysis of spontaneous fluctuations highlights the role of cortical premotor structures. Our study corroborates the notion of TS as a network disorder in which abnormal RSN activity might contribute to the generation of tics in SMA.
Ackermans, L., Duits, A., van der Linden, C., Tijssen, M., Schruers, K., Temel, Y., et al. (2011). Double-blind clinical trial of thalamic stimulation in patients with Tourette syndrome. Brain 134, 832-844. doi: 10.1093/brain/awq380
Ackermans, L., Kuhn, J., Neuner, I., Temel, Y., and Visser-Vandewalle, V. (2013a). Surgery for Tourette Syndrome. World Neurosurg. 80, S29. e15-S29. e22. doi: 10.1016/j.wneu.2012.06.017
Ackermans, L., Neuner, I., Temel, Y., Duits, A., Kuhn, J., and Visser-Vandewalle, V. (2013b). Thalamic deep brain stimulation for Tourette syndrome. Behav. Neurol. 27, 133-138. doi: 10.3233/BEN-120301
Beckmann, C. F., and Smith, S. M. (2004). Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans. Med. Imaging 23, 137-152. doi: 10.1109/TMI.2003.822821
Benjamini, Y., and Yekutieli, D. (2001). The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29, 1165-1188. doi: 10.1214/aos/1013699998
Biswal, B., Yetkin, F. Z., Haughton, V. M., and Hyde, J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 34, 537-541. doi: 10.1002/mrm.1910340409
Bluhm, R. L., Miller, J., Lanius, R. A., Osuch, E. A., Boksman, K., Neufeld, R. W. J., et al. (2007). Spontaneous low-frequency fluctuations in the BOLD signal in schizophrenic patients: anomalies in the default network. Schizophr. Bull. 33, 1004-1012. doi: 10.1093/schbul/sbm052
Bohlhalter, S., Goldfine, A., Matteson, S., Garraux, G., Hanakawa, T., Kansaku, K., et al. (2006). Neural correlates of tic generation in Tourette syndrome: an event-related functional MRI study. Brain 129, 2029-2037. doi: 10.1093/brain/awl050
Boly, M., Tshibanda, L., Vanhaudenhuyse, A., Noirhomme, Q., Schnakers, C., Ledoux, D., et al. (2009). Functional connectivity in the default network during resting state is preserved in a vegetative but not in a brain dead patient. Hum. Brain Mapp. 30, 2393-2400. doi: 10.1002/hbm.20672
Bonavita, S., Gallo, A., Sacco, R., Corte, M. D., Bisecco, A., Docimo, R., et al. (2011). Distributed changes in default-mode resting-state connectivity in multiple sclerosis. Mult. Scler. 17, 411-422. doi: 10.1177/1352458510394609
Braun, A. R., Stoetter, B., Randolph, C., Hsiao, J. K., Vladar, K., Gernert, J., et al. (1993). The functional neuroanatomy of Tourette's syndrome: an FDG-PET study. I. Regional changes in cerebral glucose metabolism differentiating patients and controls. Neuropsychopharmacology 9, 277-291. doi: 10.1038/npp.1993.64
Buckner, R. L., Andrews-Hanna, J. R., and Schacter, D. L. (2008). The brain's default network: anatomy, function, and relevance to disease. Ann. N.Y. Acad. Sci. 1124, 1-38. doi: 10.1196/annals.1440.011
Cannon, E., Silburn, P., Coyne, T., O'Maley, K., Crawford, J. D., and Sachdev, P. S. (2012). Deep brain stimulation of anteromedial globus pallidus interna for severe Tourette's syndrome. Am. J. Psychiatry 169, 860-866. doi: 10.1176/appi.ajp.2012.11101583
Cavanna, A. E., and Termine, C. (2012). Tourette syndrome. Adv. Exp. Med. Biol. 724, 375-383. doi: 10.1007/978-1-4614-0653-2_28
Church, J. A., Fair, D. A., Dosenbach, N. U. F., Cohen, A. L., Miezin, F. M., Petersen, S. E., et al. (2009). Control networks in paediatric Tourette syndrome show immature and anomalous patterns of functional connectivity. Brain 132, 225-238. doi: 10.1093/brain/awn223
Cohen, D. J., and Leckman, J. F. (1991). Tourette's syndrome. JAMA 265, 1738.
Craig, A. D. (2002). How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 3, 655-666. doi: 10.1038/nrn894
Craig, A. D. B. (2009). Emotional moments across time: a possible neural basis for time perception in the anterior insula. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 1933-1942. doi: 10.1098/rstb.2009.0008
Cunnington, R., Windischberger, C., Deecke, L., and Moser, E. (2003). The preparation and readiness for voluntary movement: a high-field event-related fMRI study of the Bereitschafts-BOLD response. Neuroimage 20, 404-412. doi: 10.1016/S1053-8119(03)00291-X
Damoiseaux, J. S., and Greicius, M. D. (2009). Greater than the sum of its parts: a review of studies combining structural connectivity and resting-state functional connectivity. Brain Struct. Funct. 213, 525-533. doi: 10.1007/s00429-009-0208-6
Damoiseaux, J. S., Rombouts, S. A. R. B., Barkhof, F., Scheltens, P., Stam, C. J., Smith, S. M., et al. (2006). Consistent resting-state networks across healthy subjects. Proc. Natl. Acad. Sci. U.S.A. 103, 13848-13853. doi: 10.1073/pnas.0601417103
Delaveau, P., Salgado-Pineda, P., Fossati, P., Witjas, T., Azulay, J.-P., and Blin, O. (2010). Dopaminergic modulation of the default mode network in Parkinson's disease. Eur. Neuropsychopharmacol. 20, 784-792. doi: 10.1016/j.euroneuro.2010.07.001
Derbyshire, S. W. G., Whalley, M. G., Stenger, V. A., and Oakley, D. A. (2004). Cerebral activation during hypnotically induced and imagined pain. Neuroimage 23, 392-401. doi: 10.1016/j.neuroimage.2004.04.033
Devinsky, O., Morrell, M. J., and Vogt, B. A. (1995a). REVIEW: Contributions of anterior cingulate cortex to behaviour. Brain 118, 279-306.
Devinsky, O., Morrell, M. J., and Vogt, B. A. (1995b). Contributions of anterior cingulate cortex to behaviour. Brain118(Pt 1), 279-306.
Disbrow, E., Litinas, E., Recanzone, G. H., Padberg, J., and Krubitzer, L. (2003). Cortical connections of the second somatosensory area and the parietal ventral area in macaque monkeys. J. Comp. Neurol. 462, 382-399. doi: 10.1002/cne.10731
Draganski, B., Martino, D., Cavanna, A. E., Hutton, C., Orth, M., Robertson, M. M., et al. (2010). Multispectral brain morphometry in Tourette syndrome persisting into adulthood. Brain 133, 3661-3675. doi: 10.1093/brain/awq300
Eccles, J. C. (1982). The initiation of voluntary movements by the supplementary motor area. Arch. Psychiatr. Nervenkr. 231, 423-441. doi: 10.1007/BF00342722
Eickhoff, S. B., Jbabdi, S., Caspers, S., Laird, A. R., Fox, P. T., Zilles, K., et al. (2010). Anatomical and functional connectivity of cytoarchitectonic areas within the human parietal operculum. J. Neurosci. 30, 6409-6421. doi: 10.1523/JNEUROSCI.5664-09.2010
Esposito, F., Tessitore, A., Giordano, A., De Micco, R., Paccone, A., Conforti, R., et al. (2013). Rhythm-specific modulation of the sensorimotor network in drug-naive patients with Parkinson's disease by levodopa. Brain 136, 710-725. doi: 10.1093/brain/awt007
Felling, R. J., and Singer, H. S. (2011). Neurobiology of tourette syndrome: current status and need for further investigation. J. Neurosci. 31, 12387-12395. doi: 10.1523/JNEUROSCI.0150-11.2011
Filippini, N., MacIntosh, B. J., Hough, M. G., Goodwin, G. M., Frisoni, G. B., Smith, S. M., et al. (2009). Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele. Proc. Natl. Acad. Sci. U.S.A. 106, 7209-7214. doi: 10.1073/pnas.0811879106
Franzkowiak, S., Pollok, B., Biermann-Ruben, K., Südmeyer, M., Paszek, J., Thomalla, G., et al. (2012). Motor-cortical interaction in Gilles de la Tourette syndrome. PLoS ONE 7:e27850. doi: 10.1371/journal.pone.0027850
Fried, I., Katz, A., McCarthy, G., Sass, K. J., Williamson, P., Spencer, S. S., et al. (1991). Functional organization of human supplementary motor cortex studied by electrical stimulation. J. Neurosci. 11, 3656-3666.
Greicius, M. D., Krasnow, B., Reiss, A. L., and Menon, V. (2003). Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. U.S.A. 100, 253-258. doi: 10.1073/pnas.0135058100
Greicius, M. D., Srivastava, G., Reiss, A. L., and Menon, V. (2004). Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc. Natl. Acad. Sci. U.S.A. 101, 4637-4642. doi: 10.1073/pnas.0308627101
Hampson, M., Tokoglu, F., King, R. A., Constable, R. T., and Leckman, J. F. (2009). Brain areas coactivating with motor cortex during chronic motor tics and intentional movements. Biol. Psychiatry 65, 594-599. doi: 10.1016/j.biopsych.2008.11.012
Heise, K.-F., Steven, B., Liuzzi, G., Thomalla, G., Jonas, M., Müller-Vahl, K., et al. (2010). Altered modulation of intracortical excitability during movement preparation in Gilles de la Tourette syndrome. Brain 133, 580-590. doi: 10.1093/brain/awp299
Hsieh, J. C., Hägermark, O., Ståhle-Bäckdahl, M., Ericson, K., Eriksson, L., Stone-Elander, S., et al. (1994). Urge to scratch represented in the human cerebral cortex during itch. J. Neurophysiol. 72, 3004-3008.
Isnard, J., Guénot, M., Sindou, M., and Mauguière, F. (2004). Clinical manifestations of insular lobe seizures: a stereo-electroencephalographic study. Epilepsia 45, 1079-1090. doi: 10.1111/j.0013-9580.2004.68903.x
Kawohl, W., Brühl, A., Krowatschek, G., Ketteler, D., and Herwig, U. (2009a). Functional magnetic resonance imaging of tics and tic suppression in Gilles de la Tourette syndrome. World J. Biol. Psychiatry 10, 567-570. doi: 10.1080/15622970802118356
Kawohl, W., Schneider, F., Vernaleken, I., and Neuner, I. (2009b). Aripiprazole in the pharmacotherapy of Gilles de la Tourette syndrome in adult patients. World J. Biol. Psychiatry 10, 827-831. doi: 10.1080/15622970701762544
Kawohl, W., Schneider, F., Vernaleken, I., and Neuner, I. (2009c). Chronic motor tic disorder and aripiprazole. J. Neuropsychiatry Clin. Neurosci. 21, 224. doi: 10.1176/appi.neuropsych.21.2.224
Khalifa, N., and von Knorring, A.-L. (2003). Prevalence of tic disorders and Tourette syndrome in a Swedish school population. Dev. Med. Child Neurol. 45, 315-319. doi: 10.1111/j.1469-8749.2003.tb00402.x
Kwan, C. L., Crawley, A. P., Mikulis, D. J., and Davis, K. D. (2000). An fMRI study of the anterior cingulate cortex and surrounding medial wall activations evoked by noxious cutaneous heat and cold stimuli. Pain 85, 359-374. doi: 10.1016/S0304-3959(99)00287-0
Leckman, J. F. (2002). Tourette's syndrome. Lancet 360, 1577-1586. doi: 10.1016/S0140-6736(02)11526-1
Leckman, J. F., Riddle, M. A., Hardin, M. T., Ort, S. I., Swartz, K. L., Stevenson, J., et al. (1989). The Yale Global Tic Severity Scale: initial testing of a clinician-rated scale of tic severity. J. Am. Acad. Child Adolesc. Psychiatry 28, 566-573. doi: 10.1097/00004583-198907000-00015
Lerner, A., Bagic, A., Boudreau, E. A., Hanakawa, T., Pagan, F., Mari, Z., et al. (2007). Neuroimaging of neuronal circuits involved in tic generation in patients with Tourette syndrome. Neurology 68, 1979-1987. doi: 10.1212/01.wnl.0000264417.18604.12
Lerner, A., Bagic, A., Simmons, J. M., Mari, Z., Bonne, O., Xu, B., et al. (2012). Widespread abnormality of the γ-aminobutyric acid-ergic system in Tourette syndrome. Brain 135, 1926-1936. doi: 10.1093/brain/aws104
Li, S.-J., Li, Z., Wu, G., Zhang, M.-J., Franczak, M., and Antuono, P. G. (2002). Alzheimer disease: evaluation of a functional MR imaging index as a marker. Radiology 225, 253-259. doi: 10.1148/radiol.2251011301
Luppino, G., Matelli, M., Camarda, R. M., Gallese, V., and Rizzolatti, G. (1991). Multiple representations of body movements in mesial area 6 and the adjacent cingulate cortex: an intracortical microstimulation study in the macaque monkey. J. Comp. Neurol. 311, 463-482. doi: 10.1002/cne.903110403
Mesulam, M. M., and Mufson, E. J. (1982a). Insula of the old world monkey. I. Architectonics in the insulo-orbito-temporal component of the paralimbic brain. J. Comp. Neurol. 212, 1-22.
Mesulam, M. M., and Mufson, E. J. (1982b). Insula of the old world monkey. III: Efferent cortical output and comments on function. J. Comp. Neurol. 212, 38-52.
Mufson, E. J., and Mesulam, M. M. (1982). Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum. J. Comp. Neurol. 212, 23-37. doi: 10.1002/cne.902120103
Müller-Vahl, K. R., Cath, D. C., Cavanna, A. E., Dehning, S., Porta, M., Robertson, M. M., et al. (2011). European clinical guidelines for Tourette syndrome and other tic disorders. Part IV: deep brain stimulation. Eur. Child Adolesc. Psychiatry 20, 209-217. doi: 10.1007/s00787-011-0166-4
Neuner, I., Kellermann, T., Stöcker, T., Kircher, T., Habel, U., Shah, J. N., et al. (2010a). Amygdala hypersensitivity in response to emotional faces in Tourette's patients. World J. Biol. Psychiatry 11, 858-872. doi: 10.3109/15622975.2010.480984
Neuner, I., Kupriyanova, Y., Stöcker, T., Huang, R., Posnansky, O., Schneider, F., et al. (2010b). White-matter abnormalities in Tourette syndrome extend beyond motor pathways. Neuroimage 51, 1184-1193. doi: 10.1016/j.neuroimage.2010.02.049
Neuner, I., and Ludolph, A. G. (2011). [Neurobiology, clinical characteristics and therapy in Tourette's syndrome]. Fortschr. Neurol. Psychiatr. 79, 724-732. doi: 10.1055/s-0031-1281853
Neuner, I., Nordt, C., Schneider, F., and Kawohl, W. (2012). Effectiveness of aripiprazole in the treatment of adult Tourette patients up to 56 months. Hum. Psychopharmacol. 27, 364-369. doi: 10.1002/hup.2235
Neuner, I., Podoll, K., Janouschek, H., Michel, T. M., Sheldrick, A. J., and Schneider, F. (2009). From psychosurgery to neuromodulation: deep brain stimulation for intractable Tourette syndrome. World J. Biol. Psychiatry 10, 366-376. doi: 10.1080/15622970802513317
Neuner, I., Wegener, P., Stoecker, T., Kircher, T., Schneider, F., and Shah, N. J. (2007). Development and implementation of an MR-compatible whole body video system. Neurosci. Lett. 420, 122-127. doi: 10.1016/j.neulet.2007.03.063
Nichols, T. E., and Holmes, A. P. (2002). Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 15, 1-25. doi: 10.1002/hbm.1058
Oakes, T. R., Fox, A. S., Johnstone, T., Chung, M. K., Kalin, N., and Davidson, R. J. (2007). Integrating VBM into the General Linear Model with voxelwise anatomical covariates. Neuroimage 34, 500-508. doi: 10.1016/j.neuroimage.2006.10.007
Pearlson, G. D., and Calhoun, V. D. (2009). Convergent approaches for defining functional imaging endophenotypes in schizophrenia. Front. Hum. Neurosci. 3:37. doi: 10.3389/neuro.09.037.2009
Peterson, B. S., Skudlarski, P., Anderson, A. W., Zhang, H., Gatenby, J. C., Lacadie, C. M., et al. (1998). A functional magnetic resonance imaging study of tic suppression in Tourette syndrome. Arch. Gen. Psychiatry 55, 326-333. doi: 10.1001/archpsyc.55.4.326
Peterson, B. S., Thomas, P., Kane, M. J., Scahill, L., Zhang, H., Bronen, R., et al. (2003). Basal Ganglia volumes in patients with Gilles de la Tourette syndrome. Arch. Gen. Psychiatry 60, 415-424. doi: 10.1001/archpsyc.60.4.415
Plessen, K. J., Bansal, R., and Peterson, B. S. (2009). Imaging evidence for anatomical disturbances and neuroplastic compensation in persons with Tourette syndrome. J. Psychosom. Res. 67, 559-573. doi: 10.1016/j.jpsychores.2009.07.005
Qi, H.-X., Lyon, D. C., and Kaas, J. H. (2002). Cortical and thalamic connections of the parietal ventral somatosensory area in marmoset monkeys (Callithrix jacchus). J. Comp. Neurol. 443, 168-182. doi: 10.1002/cne.10113
Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., and Shulman, G. L. (2001). A default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98, 676-682. doi: 10.1073/pnas.98.2.676
Robertson, M. M. (2012). The Gilles de la Tourette syndrome: the current status. Arch. Dis. Child. Educ. Pract. Ed. 97, 166-175. doi: 10.1136/archdischild-2011-300585
Roessner, V., Rothenberger, A., Rickards, H., and Hoekstra, P. J. (2011). European clinical guidelines for Tourette syndrome and other tic disorders. Eur. Child Adolesc. Psychiatry 20, 153-154. doi: 10.1007/s00787-011-0165-5
Roland, P. E., Larsen, B., Lassen, N. A., and Skinhøj, E. (1980). Supplementary motor area and other cortical areas in organization of voluntary movements in man. J. Neurophysiol. 43, 118-136.
Rosazza, C., and Minati, L. (2011). Resting-state brain networks: literature review and clinical applications. Neurol. Sci. 32, 773-785. doi: 10.1007/s10072-011-0636-y
Sadaghiani, S., Hesselmann, G., Friston, K. J., and Kleinschmidt, A. (2010). The relation of ongoing brain activity, evoked neural responses, and cognition. Front. Syst. Neurosci. 4:20. doi: 10.3389/fnsys.2010.00020
Singer, H. S. (2005). Tourette's syndrome: from behaviour to biology. Lancet Neurol. 4, 149-159. doi: 10.1016/S1474-4422(05)01012-4
Smith, S. M., Fox, P. T., Miller, K. L., Glahn, D. C., Fox, P. M., Mackay, C. E., et al. (2009). Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. U.S.A. 106, 13040-13045. doi: 10.1073/pnas.0905267106
Stern, E., Silbersweig, D. A., Chee, K. Y., Holmes, A., Robertson, M. M., Trimble, M., et al. (2000). A functional neuroanatomy of tics in Tourette syndrome. Arch. Gen. Psychiatry 57, 741-748. doi: 10.1001/archpsyc.57.8.741
Tessitore, A., Esposito, F., Vitale, C., Santangelo, G., Amboni, M., Russo, A., et al. (2012). Default-mode network connectivity in cognitively unimpaired patients with Parkinson disease. Neurology 79, 2226-2232. doi: 10.1212/WNL.0b013e31827689d6
Thomalla, G., Siebner, H. R., Jonas, M., Bäumer, T., Biermann-Ruben, K., Hummel, F., et al. (2009). Structural changes in the somatosensory system correlate with tic severity in Gilles de la Tourette syndrome. Brain 132, 765-777. doi: 10.1093/brain/awn339
Van Eimeren, T., Monchi, O., Ballanger, B., and Strafella, A. P. (2009). Dysfunction of the default mode network in Parkinson disease: a functional magnetic resonance imaging study. Arch. Neurol. 66, 877-883.
Vandewalle, V., van der Linden, C., Groenewegen, H. J., and Caemaert, J. (1999). Stereotactic treatment of Gilles de la Tourette syndrome by high frequency stimulation of thalamus. Lancet 353, 724. doi: 10.1016/S0140-6736(98)05964-9
Wang, Z., Maia, T. V., Marsh, R., Colibazzi, T., Gerber, A., and Peterson, B. S. (2011). The neural circuits that generate tics in Tourette's syndrome. Am. J. Psychiatry 168, 1326-1337. doi: 10.1176/appi.ajp.2011.09111692
Werner, C. J., Dogan, I., Saß, C., Mirzazade, S., Schiefer, J., Shah, N. J., et al. (2014). Altered resting-state connectivity in Huntington's Disease. Hum. Brain Mapp. 35, 2582-2593. doi: 10.1002/hbm.22351
Werner, C. J., Stöcker, T., Kellermann, T., Wegener, H. P., Schneider, F., Shah, N. J., et al. (2010). Altered amygdala functional connectivity in adult Tourette's syndrome. Eur. Arch. Psychiatry Clin. Neurosci. 260(Suppl.), S95-S99. doi: 10.1007/s00406-010-0161-7
Wolf, R. C., Sambataro, F., Vasic, N., Wolf, N. D., Thomann, P. A., Saft, C., et al. (2012). Default-mode network changes in preclinical Huntington's disease. Exp. Neurol. 237, 191-198. doi: 10.1016/j.expneurol.2012.06.014
Worbe, Y., Gerardin, E., Hartmann, A., Valabrégue, R., Chupin, M., Tremblay, L., et al. (2010). Distinct structural changes underpin clinical phenotypes in patients with Gilles de la Tourette syndrome. Brain 133, 3649-3660. doi: 10.1093/brain/awq293
Ziemann, U., Paulus, W., and Rothenberger, A. (1997). Decreased motor inhibition in Tourette's disorder: evidence from transcranial magnetic stimulation. Am. J. Psychiatry 154, 1277-1284.
Zuo, X.-N., Kelly, C., Adelstein, J. S., Klein, D. F., Castellanos, F. X., and Milham, M. P. (2010). Reliable intrinsic connectivity networks: test-retest evaluation using ICA and dual regression approach. Neuroimage 49, 2163-2177. doi: 10.1016/j.neuroimage.2009.10.080