A baseline for the multivariate comparison of resting-state networks
Elena A Allen, Erik B Erhardt, Eswar Damaraju, William Gruner, Judith M Segall, Rogers F Silva, Martin Havlicek, Srinivas Rachakonda, Jill Fries, Ravi Kalyanam, Andrew M Michael, Arvind Caprihan, Jessica A Turner, Tom Eichele, Steven Adelsheim, Angela D Bryan, Juan Bustillo, Vincent P Clark, Sarah W Feldstein Ewing, Francesca Filbey, Corey C Ford, Kent Hutchison, Rex E Jung, Kent A Kiehl, Piyadasa Kodituwakku, Yuko M Komesu, Andrew R Mayer, Godfrey D Pearlson, John P Phillips, Joseph R Sadek, Michael Stevens, Ursina Teuscher, Robert J Thoma, Vince D Calhoun, Elena A Allen, Erik B Erhardt, Eswar Damaraju, William Gruner, Judith M Segall, Rogers F Silva, Martin Havlicek, Srinivas Rachakonda, Jill Fries, Ravi Kalyanam, Andrew M Michael, Arvind Caprihan, Jessica A Turner, Tom Eichele, Steven Adelsheim, Angela D Bryan, Juan Bustillo, Vincent P Clark, Sarah W Feldstein Ewing, Francesca Filbey, Corey C Ford, Kent Hutchison, Rex E Jung, Kent A Kiehl, Piyadasa Kodituwakku, Yuko M Komesu, Andrew R Mayer, Godfrey D Pearlson, John P Phillips, Joseph R Sadek, Michael Stevens, Ursina Teuscher, Robert J Thoma, Vince D Calhoun
Abstract
As the size of functional and structural MRI datasets expands, it becomes increasingly important to establish a baseline from which diagnostic relevance may be determined, a processing strategy that efficiently prepares data for analysis, and a statistical approach that identifies important effects in a manner that is both robust and reproducible. In this paper, we introduce a multivariate analytic approach that optimizes sensitivity and reduces unnecessary testing. We demonstrate the utility of this mega-analytic approach by identifying the effects of age and gender on the resting-state networks (RSNs) of 603 healthy adolescents and adults (mean age: 23.4 years, range: 12-71 years). Data were collected on the same scanner, preprocessed using an automated analysis pipeline based in SPM, and studied using group independent component analysis. RSNs were identified and evaluated in terms of three primary outcome measures: time course spectral power, spatial map intensity, and functional network connectivity. Results revealed robust effects of age on all three outcome measures, largely indicating decreases in network coherence and connectivity with increasing age. Gender effects were of smaller magnitude but suggested stronger intra-network connectivity in females and more inter-network connectivity in males, particularly with regard to sensorimotor networks. These findings, along with the analysis approach and statistical framework described here, provide a useful baseline for future investigations of brain networks in health and disease.
Keywords: connectome; fMRI; functional connectivity; independent component analysis; resting-state.
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References
- Abbott C., Kim D., Sponheim S. R., Bustillo J., Calhoun V. D. (2010). Decreased default mode neural modulation with age in schizophrenia. Am. J. Geriatr. Psychiatry 18, 897–907
- Abou-Elseoud A., Starck T., Remes J., Nikkinen J., Tervonen O., Kiviniemi V. (2010). The effect of model order selection in group PICA. Hum. Brain Mapp. 31, 1207–1216
- Albert N., Robertson E., Miall R. (2009). The resting human brain and motor learning. Curr. Biol. 19, 1023–1027
- Allen E., Erhardt E., Eichele T., Mayer A. R., Calhoun V. D. (2010). “Comparison of pre-normalization methods on the accuracy of group ICA results”, in 16th Annual Meeting of the Organization for Human Brain Mapping, 6–10 June, Barcelona, Spain
- Ances B., Liang C., Leontiev O., Perthen J., Fleisher A., Lansing A., Buxton R. (2009). Effects of aging on cerebral blood flow, oxygen metabolism, and blood oxygenation level dependent responses to visual stimulation. Hum. Brain Mapp. 30, 1120–113210.1002/hbm.20574
- Andrews-Hanna J., Snyder A., Vincent J., Lustig C., Head D., Raichle M., Buckner R. (2007). Disruption of large-scale brain systems in advanced aging. Neuron 56, 924–93510.1016/j.neuron.2007.10.038
- Ashburner J., Friston K. J. (2005). Unified segmentation. Neuroimage 26, 839–85110.1016/j.neuroimage.2005.02.018
- Barron S., Jacobs L., Kinkel W. (1976). Changes in size of normal lateral ventricles during aging determined by computerized tomography. Neurology 26, 1011–1013
- Beall E., Lowe M. (2010). The non-separability of physiologic noise in functional connectivity MRI with spatial ICA at 3T. J. Neurosci. Methods 191, 263–276
- Beckmann C. F., DeLuca M., Devlin J. T., Smith S. M. (2005). Investigations into resting-state connectivity using independent component analysis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360, 1001–1013
- Bell A. J., Sejnowski T. (1995). An information-maximization approach to blind separation and blind deconvolution. Neural. Comput. 7, 1129–1159
- Birn R., Diamond J., Smith M., Bandettini P. (2006). Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI. Neuroimage 31, 1536–154810.1016/j.neuroimage.2006.02.048
- Birn R., Murphy K., Bandettini P. (2008). The effect of respiration variations on independent component analysis results of resting state functional connectivity. Hum. Brain Mapp. 29, 740–75010.1002/hbm.20577
- Biswal B. B., Mennes M., Zuo X. N., Gohel S., Kelly C., Smith S. M., Beckmann C. F., Adelstein J. S., Buckner R. L., Colcombe S., Dogonowski A. M., Ernst M., Fair D., Hampson M., Hoptman M. J., Hyde J. S., Kiviniemi V. J., Kötter R., Li S. J., Lin C. P., Lowe M. J., Mackay C., Madden D. J., Madsen K. H., Margulies D. S., Mayberg H. S., McMahon K., Monk C. S., Mostofsky S. H., Nagel B. J., Pekar J. J., Peltier S. J., Petersen S. E., Riedl V., Rombouts S. A., Rypma B., Schlaggar B. L., Schmidt S., Seidler R. D., Siegle G. J., Sorg C., Teng G. J., Veijola J., Villringer A., Walter M., Wang L., Weng X.C., Whitfield-Gabrieli S., Williamson P., Windischberger C., Zang Y. F., Zhang H. Y., Castellanos F. X., Milham M. P. (2010). Toward discovery science of human brain function. Proc. Natl. Acad. Sci. U.S.A. 107, 4734–4739
- Biswal B., Yetkin F., Haughton V., Hyde J. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 34, 537–541
- Bluhm R. L., Osuch E. A., Lanius R. A., Boksman K., Neufeld R. W. J., Théberge J., Williamson P. (2008). Default mode network connectivity: effects of age, sex, and analytic approach. Neuroreport 19, 887–89110.1097/WNR.0b013e328300ebbf
- Bockholt H. J., Scully M., Courtney W., Rachakonda S., Scott A., Caprihan A., Fries J., Kalyanam R., Segall J., dela Garza R., Lane S., Calhoun V. D. (2009). Mining the mind research network: a novel framework for exploring large scale, heterogeneous translational neuroscience research data sources. Front. Neuroinformatics 3:36.10.3389/neuro.11.036.2009
- Bookheimer S. (2002). Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. Annu. Rev. Neurosci. 25, 151–188
- Broyd S., Demanuele C., Debener S., Helps S. K., James C. J., Sonuga-Barke E. J. S. (2009). Default-mode brain dysfunction in mental disorders: a systematic review. Neurosci. Biobehav. Rev. 33, 279–296
- Buckner R., Andrews-Hanna J., Schacter D. (2008). The brain's default network. Ann. N. Y. Acad. Sci. 1124, 1–38
- Bullmore E., Sporns O. (2009). Complex brain networks: graph theoretical analysis of structural and functional systems. Nat. Rev. Neurosci. 10, 186–198
- Calhoun V. D., Adali T., Pearlson G. D., Pekar J. J. (2001). A method for making group inferences from functional MRI data using independent component analysis. Hum. Brain Mapp. 14, 140–15110.1002/hbm.1048
- Calhoun V. D., Adali T., Pearlson G. D., Pekar J. J. (2002a). Erratum: a method for making group inferences from functional MRI data using independent component analysis. Hum. Brain Mapp. 16, 131.10.1002/hbm.10044
- Calhoun V., Pekar J., McGinty V., Adali T., Watson T., Pearlson G. (2002b). Different activation dynamics in multiple neural systems during simulated driving. Hum. Brain Mapp. 16, 158–16710.1002/hbm.10032
- Calhoun V. D., Eichele T., Pearlson G. (2009). Functional brain networks in schizophrenia: a review. Front. Hum. Neurosci. 3:17.10.3389/neuro.09.017.2009
- Calhoun V. D., Kiehl K. A., Pearlson G. D. (2008a). Modulation of temporally coherent brain networks estimated using ICA at rest and during cognitive tasks. Hum. Brain Mapp. 29, 828–83810.1002/hbm.20581
- Calhoun V. D., Maciejewski P. K., Pearlson G. D., Kiehl K. A. (2008b). Temporal lobe and “default” hemodynamic brain modes discriminate between schizophrenia and bipolar disorder. Hum. Brain Mapp. 29, 1265–127510.1002/hbm.20463
- Caprihan A., Pearlson G., Calhoun V. (2008). Application of principal component analysis to distinguish patients with schizophrenia from healthy controls based on fractional anisotropy measurements. Neuroimage 42, 675–68210.1016/j.neuroimage.2008.04.255
- Cavanna A., Trimble M. (2006). The precuneus: a review of its functional anatomy and behavioural correlates. Brain 1293, 564–58310.1093/brain/awl004
- Christensen R. (1996). Analysis of Variance, Design and Regression: Applied Statistical Methods. New York: Chapman and Hall/CRC
- Christensen R. (2001). Advanced Linear Modeling: Multivariate, Time Series, and Spatial Data; Nonparametric Regression and Response Surface Maximization. New York: Springer Verlag
- Corbetta M., Shulman G. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201–215
- Cordes D., Haughton V. M., Arfanakis K., Wendt G. J., Turski P. A., Moritz C. H., Quigley M. A., Meyerand M. E. (2000). Mapping functionally related regions of brain with functional connectivity MR imaging. Am. J. Neuroradiol. 21, 1636–1644
- Costafreda S. G. (2010). Pooling fMRI data: meta-analysis, mega-analysis and multi-center studies. Front. Neuroinformatics 3:33.10.3389/neuro.11.033.2009
- Damoiseaux J. S., Beckmann C. F., Arigita E. J., Barkhof F., Scheltens P., Stam C. J., Smith S. M., Rombouts S. (2008). Reduced resting-state brain activity in the “default network” in normal aging. Cereb. Cortex 18, 1856–1864
- Damoiseaux J. S., Rombouts S., Barkhof F., Scheltens P., Stam C. J., Smith S. M., Beckmann C. F. (2006). Consistent resting-state networks across healthy subjects. Proc. Natl. Acad. Sci. U.S.A. 103, 13848–13853
- Derksen S., Keselman H. J. (1992). Backward, forward and stepwise automated subset selection algorithms: frequency of obtaining authentic and noise variables. Br. J. Math. Stat. Psychol. 45, 265–282
- Deshpande G., LaConte S., James G., Peltier S., Hu X. (2009). Multivariate granger causality analysis of fMRI data. Hum. Brain Mapp. 30, 1361–137310.1002/hbm.20606
- D'Esposito M., Deouell L. Y., Gazzaley A. (2003). Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging. Nat. Rev. Neurosci. 4, 863–872
- Eichele T., Debener S., Calhoun V. D., Specht K., Engel A. K., Hugdahl K., VonCramon D. Y., Ullsperger M. (2008). Prediction of human errors by maladaptive changes in event-related brain networks. Proc. Natl. Acad. Sci. U.S.A. 105, 6173–6178
- Erhardt E. B., Rachakonda S., Bedrick E. J., Allen E. A., Adali T., Calhoun V. D. (2010). Comparison of multi-subject ICA methods for analysis of fMRI data. Hum. Brain Mapp.[Epub ahead of print].10.1002/hbm.21170
- Esposito F., Aragri A., Pesaresi I., Cirillo S., Tedeschi G., Marciano E., Goebel R., DiSalle F. (2008). Independent component model of the default-mode brain function: combining individual-level and population-level analyses in resting-state fMRI. Magn. Reson. Imaging 26, 905–913
- Fair D. A., Bathula D., Mills K. L., Dias T. G. C., Blythe M. S., Zhang D., Snyder A. Z., Raichle M. E., Stevens A. A., Nigg J. T., Nagel B. J. (2010). Maturing thalamocortical functional connectivity across development. Front. Syst. Neurosci. 4:10.10.3389/fnsys.2010.00010
- Fair D. A., Cohen A. L., Dosenbach N. U., Church J. A., Miezin F. M., Barch D. M., Raichle M. E., Petersen S. E., Schlaggar B. L. (2008). The maturing architecture of the brain's default network. Proc. Natl. Acad. Sci. U.S.A. 105, 4028–4032
- Fan J., McCandliss B. D., Fossella J., Flombaum J. I., Posner M. I. (2005). The activation of attentional networks. Neuroimage 26, 471–47910.1016/j.neuroimage.2005.02.004
- Filippini N., MacIntosh B. J., Hough M. G., Goodwin G. M., Frisoni G. B., Smith S. M., Matthews P. M., Beckmann C. F., Mackay C. E. (2009). Distinct patterns of brain activity in young carriers of the APOE-4 allele. Proc. Natl. Acad. Sci. U.S.A. 106, 7209–7214
- Fox M. D., Raichle M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 8, 700–711
- Fox M., Snyder A., Vincent J., Corbetta M., Van Essen D., Raichle M. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U.S.A. 102, 9673.
- Fox M., Zhang D., Snyder A., Raichle M. (2009). The global signal and observed anticorrelated resting state brain networks. J. Neurophysiology 101, 3270
- Franco A. R., Pritchard A., Calhoun V. D., Mayer A. R. (2009). Interrater and intermethod reliability of default mode network selection. Hum. Brain Mapp. 30, 2293–230310.1002/hbm.20668
- Friston K. J., Holmes A. P., Worsley K. J., Poline J. B., Frith C. D., Frackowiak R. S. J. (1995). Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp. 2, 189–21010.1002/hbm.460020402
- Garrity A. G., Pearlson G. D., McKiernan K., Lloyd D., Kiehl K. A., Calhoun V. D. (2007). Aberrant “default mode” functional connectivity in schizophrenia. Am. J. Psychiatry 164, 450–457
- Genovese C. R., Lazar N. A., Nichols T. (2002). Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15, 870–87810.1006/nimg.2001.1037
- Glahn D., Winkler A., Kochunov P., Almasy L., Duggirala R., Carless M., Curran J., Olvera R., Laird A., Smith S., Beckmann C. F., Fox P. T., Blangerod J. (2010). Genetic control over the resting brain. Proc. Natl. Acad. Sci. U.S.A. 107, 1223–1228
- Gong G., Rosa-Neto P., Carbonell F., Chen Z. J., He Y., Evans A. C. (2009). Age- and gender-related differences in the cortical anatomical network. J. Neurosci. 29, 15684–15693
- Good C., Johnsrude I., Ashburner J., Henson R., Friston K., Frackowiak R. (2001). Cerebral asymmetry and the effects of sex and handedness on brain structure: a voxel-based morphometric analysis of 465 normal adult human brains. Neuroimage 14, 685–70010.1006/nimg.2001.0857
- Greicius M. (2008). Resting-state functional connectivity in neuropsychiatric disorders. Curr. Opin. Neurol. 21, 424–430
- Grill-Spector K., Malach R. (2004). The human visual cortex. Annu. Rev. Neurosci. 27, 649–677
- Hagmann P., Cammoun L., Gigandet X., Meuli R., Honey C. J., Wedeen V. J., Sporns O. (2008). Mapping the structural core of human cerebral cortex. PLoS Biol. 6, e159.10.1371/journal.pbio.0060159
- Haier R., Jung R., Yeo R., Head K., Alkire M. (2005). The neuroanatomy of general intelligence: sex matters. Neuroimage 25, 320–32710.1016/j.neuroimage.2004.11.019
- Hamilton C. (2008). Cognition and Sex Differences. New York: Palgrave Macmillan
- Hampson M., Peterson B., Skudlarski P., Gatenby J., Gore J. (2002). Detection of functional connectivity using temporal correlations in MR images. Hum. Brain Mapp. 15, 247–26210.1002/hbm.10022
- Hampson M., Tokoglu F., Sun Z., Schafer R., Skudlarski P., Gore J., Constable R. (2006). Connectivity-behavior analysis reveals that functional connectivity between left BA39 and Broca's area varies with reading ability. Neuroimage 31, 513–51910.1016/j.neuroimage.2005.12.040
- Harrison B. J., Pujol J., López-Solà M., Hernández-Ribas R., Deus J., Ortiz H., Soriano-Mas C., Yücel M., Pantelis C., Cardoner N. (2008). Consistency and functional specialization in the default mode brain network. Proc. Natl. Acad. Sci. U.S.A. 105, 9781–9786
- He B. J., Snyder A. Z., Vincent J. L., Epstein A., Shulman G. L., Corbetta M. (2007). Breakdown of functional connectivity in frontoparietal networks underlies behavioral deficits in spatial neglect. Neuron 53, 905–91810.1016/j.neuron.2007.02.013
- Henderson H. V., Velleman P. F. (1981). Building multiple regression models interactively. Biometrics 37, 391–41110.2307/2530428
- Himberg J., Hyvärinen A., Esposito F. (2004). Validating the independent components of neuroimaging time series via clustering and visualization. Neuroimage 22, 1214–1222
- Huppert T., Hoge R., Diamond S., Franceschini M., Boas D. (2006). A temporal comparison of BOLD, ASL, and NIRS hemodynamic responses to motor stimuli in adult humans. Neuroimage 29, 368–38210.1016/j.neuroimage.2005.08.065
- Hyvärinen A., Karhunen J., Oja E. (2001). Independent Component Analysis, Adaptive and Learning Systems for Signal Processing, Communications, and Control. New York: John Wiley and Sons
- Iidaka T., Matsumoto A., Nogawa J., Yamamoto Y., Sadato N. (2006). Frontoparietal network involved in successful retrieval from episodic memory: spatial and temporal analyses using fMRI and ERP. Cereb. Cortex 16, 1349–1360
- Jafri M. J., Pearlson G. D., Stevens M., Calhoun V. D. (2008). A method for functional network connectivity among spatially independent resting-state components in schizophrenia. Neuroimage 39, 1666–168110.1016/j.neuroimage.2007.11.001
- Judd C. M., McClelland G. H., Ryan C. S. (1989). Data Analysis: A Model-Comparison Approach. San Diego: Harcourt Brace Jovanovich
- Karunanayaka P., Holland S., Schmithorst V., Solodkin A., Chen E., Szaflarski J., Plante E. (2007). Age-related connectivity changes in fMRI data from children listening to stories. Neuroimage 34, 349–36010.1016/j.neuroimage.2006.08.028
- Kelly A. M., Di Martino A., Uddin L. Q., Shehzad Z., Gee D. G., Reiss P. T., Margulies D. S., Castellanos F. X., Milham M. P. (2009). Development of anterior cingulate functional connectivity from late childhood to early adulthood. Cereb. Cortex 19, 640–65710.1093/cercor/bhn117
- Kennedy D. P., Courchesne E. (2008). The intrinsic functional organization of the brain is altered in autism. Neuroimage 39, 1877–188510.1016/j.neuroimage.2007.10.052
- Kiviniemi V., Starck T., Remes J., Long X., Nikkinen J., Haapea M., Veijola J., Moilanen I., Isohanni M., Zang Y. F., Tervonen O. (2009). Functional segmentation of the brain cortex using high model order group PICA. Hum. Brain Mapp. 30, 3865–388610.1002/hbm.20813
- Klein T. A., Endrass T., Kathmann N., Neumann J., Von Cramon D. Y., Ullsperger M. (2007). Neural correlates of error awareness. Neuroimage 34, 1774–178110.1016/j.neuroimage.2006.11.014
- Koch W., Teipel S., Mueller S., Buerger K., Bokde A. L. W., Hampel H., Coates U., Reiser M., Meindl T. (2009). Effects of aging on default mode network activity in resting state fMRI: does the method of analysis matter? Neuroimage 51, 280–287
- Kochiyama T., Morita T., Okada T., Yonekura Y., Matsumura M., Sadato N. (2005). Removing the effects of task-related motion using independent-component analysis. Neuroimage 25, 802–81410.1016/j.neuroimage.2004.12.027
- Koechlin E., Ody C., Kouneiher F. (2003). The architecture of cognitive control in the human prefrontal cortex. Science 302, 1181–118510.1126/science.1088545
- Koechlin E., Summerfield C. (2007). An information theoretical approach to prefrontal executive function. Trends Cogn. Sci. 11, 229–235
- Kraemer H., Yesavage J., Taylor J., Kupfer D. (2000). How can we learn about developmental processes from cross-sectional studies, or can we? Am. J. Psychiatry 157, 163–171
- Krienen F., Buckner R. (2009). Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb. Cortex 19, 2485–249710.1093/cercor/bhp135
- Laird A. R., Eickhoff S. B., Li K., Robin D. A., Glahn D. C., Fox P. T. (2009). Investigating the functional heterogeneity of the default mode network using coordinate-based meta-analytic modeling. J. Neurosci. 29, 14496–1450510.1523/JNEUROSCI.4004-09.2009
- Luders E., Gaser C., Narr K. L., Toga A. W. (2009). Why sex matters: brain size independent differences in gray matter distributions between men and women. J. Neurosci. 29, 14265–1427010.1523/JNEUROSCI.2261-09.2009
- Luders E., Narr K., Thompson P., Woods R., Rex D., Jancke L., Steinmetz H., Toga A. (2005). Mapping cortical gray matter in the young adult brain: effects of gender. Neuroimage 26, 493–50110.1016/j.neuroimage.2005.02.010
- Mantel N. (1970). Why stepdown procedures in variable selection. Technometrics 12, 621–62510.2307/1267207
- Margulies D. S., Vincent J. L., Kelly C., Lohmann G., Uddin L. Q., Biswal B. B., Villringer A., Castellanos F. X., Milham M. P., Petrides M. (2009). Precuneus shares intrinsic functional architecture in humans and monkeys. Proc. Natl. Acad. Sci. U.S.A. 106, 20069–20074
- McKeown M. J., Hansen L. K., Sejnowsk T. J. (2003). Independent component analysis of functional MRI: what is signal and what is noise? Curr. Opin. Neurobiol. 13, 620–629
- Meda S., Giuliani N., Calhoun V., Jagannathan K., Schretlen D., Pulver A., Cascella N., Keshavan M., Kates W., Buchanan R., Sharma T., Pearlson G. D. (2008). A large scale (n= 400) investigation of gray matter differences in schizophrenia using optimized voxel-based morphometry. Schizophrenia Research 101, 95–10510.1016/j.schres.2008.02.007
- Mitra P., Bokil H. (2008). Observed Brain Dynamics. New York: Oxford University Press
- Murphy K., Birn R., Handwerker D., Jones T., Bandettini P. (2009). The impact of global signal regression on resting state correlations: are anti-correlated networks introduced? NeuroImage 44, 893–90510.1016/j.neuroimage.2008.09.036
- Murphy K., Birn R., Handwerker D., Jones T., Bandettini P. 2009. The impact of global signal regression on resting state correlations: Are anti-correlated networks introduced? NeuroImage 1041 44 (3), 893–90510.1016/j.neuroimage.2008.09.036
- Østby Y., Tamnes C., Fjell A., Westlye L., Due-Tønnessen P., Walhovd K. (2009). Heterogeneity in subcortical brain development: a structural magnetic resonance imaging study of brain maturation from 8 to 30 years. J. Neurosci. 29, 11772–1178210.1523/JNEUROSCI.1242-09.2009
- Raichle M. E., MacLeod A. M., Snyder A. Z., Powers W. J., Gusnard D. A., Shulman G. L. (2001). A default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98, 676–682
- Ridderinkhof K. R., Ullsperger M., Crone E. A., Nieuwenhuis S. (2004). The role of the medial frontal cortex in cognitive control. Science 306, 443–44710.1126/science.1100301
- Robinson S., Basso G., Soldati N., Sailer U., Jovicich J., Bruzzone L., Kryspin-Exner I., Bauer H., Moser E. (2009). A resting state network in the motor control circuit of the basal ganglia. BMC Neurosci. 10, 137.10.1186/1471-2202-10-137
- Roweis S. (1998). EM algorithms for PCA and SPCA. Adv. Neural Inf. Process Syst. 626–632
- Schmithorst V., Holland S. (2006). Functional MRI evidence for disparate developmental processes underlying intelligence in boys and girls. Neuroimage 31, 1366–137910.1016/j.neuroimage.2006.01.010
- Schmithorst V., Holland S. (2007). Sex differences in the development of neuroanatomical functional connectivity underlying intelligence found using Bayesian connectivity analysis. Neuroimage 35, 406–41910.1016/j.neuroimage.2006.11.046
- Schölvinck M., Maier A., Ye F., Duyn J., Leopold D. (2010). Neural basis of global resting-state fMRI activity. Proc. Natl. Acad. Sci. U.S.A. 107, 10238–10243
- Seifritz E., Esposito F., Hennel F., Mustovic H., Neuhoff J., Bilecen D., Tedeschi G., Scheffler K., Di Salle F. (2002). Spatiotemporal pattern of neural processing in the human auditory cortex. Science 297, 1706–170810.1126/science.1074355
- Shehzad Z., Kelly A., Reiss P., Gee D., Gotimer K., Uddin L., Lee S., Margulies D., Roy A., Biswal B., Petkova E., Castellanos F. X., Milham M. P. (2009). The resting brain: unconstrained yet reliable. Cereb. Cortex 19, 2209–222910.1093/cercor/bhn256
- Smith S. M., Fox P. T., Miller K. L., Glahn D. C., Fox P. M., Mackay C. E., Filippini N., Watkins K. E., Toro R., Laird A. R., Beckmann C. F. (2009). Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. U.S.A. 106, 13040–13045
- Sowell E., Peterson B., Kan E., Woods R., Yoshii J., Bansal R., Xu D., Zhu H., Thompson P., Toga A. (2007). Sex differences in cortical thickness mapped in 176 healthy individuals between 7 and 87 years of age. Cereb. Cortex 17, 1550–1560
- Sowell E., Peterson B., Thompson P., Welcome S., Henkenius A., Toga A. (2003). Mapping cortical change across the human life span. Nat. Neurosci. 6, 309–315
- Specht K., Reul J. (2003). Functional segregation of the temporal lobes into highly differentiated subsystems for auditory perception: an auditory rapid event-related fMRI-task. Neuroimage 20, 1944–195410.1016/j.neuroimage.2003.07.034
- Starck T., Remes J., Nikkinen J., Tervonen O., Kiviniemi V. (2010). Correction of low-frequency physiological noise from the resting state BOLD fMRI–effect on ICA default mode analysis at 1.5 T. J. Neurosci. Methods 186, 179–185
- Stevens M. C., Pearlson G. D., Calhoun V. D. (2009). Changes in the interaction of resting-state neural networks from adolescence to adulthood. Hum. Brain Mapp. 30, 2356–236610.1002/hbm.20673
- Sui J., Adali T., Pearlson G. D., Calhoun V. D. (2009). An ICA-based method for the identification of optimal fMRI features and components using combined group-discriminative techniques. Neuroimage 46, 73–8610.1016/j.neuroimage.2009.01.026
- Sullivan E. V., Pfefferbaum A. (2006). Diffusion tensor imaging and aging. Neurosci. Biobehav. Rev. 30, 749–761
- Sun F., Miller L., D'Esposito M. (2004). Measuring interregional functional connectivity using coherence and partial coherence analyses of fMRI data. Neuroimage 21, 647–65810.1016/j.neuroimage.2003.09.056
- Szaflarski J., Holland S., Schmithorst V., Byars A. (2006). fMRI study of language lateralization in children and adults. Hum. Brain Mapp. 27, 202–21210.1002/hbm.20177
- Tamnes C. K., Ostby Y., Fjell A. M., Westlye L. T., Due-Tønnessen P., Walhovd K. B. (2010). Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb. Cortex 20, 534–54810.1093/cercor/bhp118
- Van Dijk K. R. A., Hedden T., Venkataraman A., Evans K. C., Lazar S. W., Buckner R. L. (2010). Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. J. Neurophysiol. 103, 297–32110.1152/jn.00783.2009
- Vincent J., Kahn I., Snyder A., Raichle M., Buckner R. (2008). Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. J. Neurophysiol. 100, 3328–334210.1152/jn.90355.2008
- Wallentin M. (2009). Putative sex differences in verbal abilities and language cortex: a critical review. Brain Lang. 108, 175–18310.1016/j.bandl.2008.07.001
- Weiss E. M., Kemmler G., Deisenhammer E. A., Fleischhacker W. W., Delazer M. (2003). Sex differences in cognitive functions. Pers. Individ. Dif. 35, 863–875
- Whitfield-Gabrieli S., Thermenos H., Milanovic S., Tsuang M., Faraone S., McCarley R., Shenton M., Green A., Nieto-Castanon A., LaViolette P., Wojcik J., Gabrieli J. D. E., Seidman L. J. (2009). Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proc. Natl. Acad. Sci. U.S.A. 106, 1279–1284
- Whitford T., Rennie C., Grieve S., Clark C., Gordon E., Williams L. (2007). Brain maturation in adolescence: concurrent changes in neuroanatomy and neurophysiology. Hum. Brain Mapp. 28, 228–23710.1002/hbm.20273
- Xiong J., Ma L., Wang B., Narayana S., Duff E., Egan G., Fox P. (2009). Long-term motor training induced changes in regional cerebral blood flow in both task and resting states. Neuroimage 45, 75–8210.1016/j.neuroimage.2008.11.016
- Ystad M., Eichele T., Lundervold A. J., Lundervold A. (2010). Subcortical functional connectivity and verbal episodic memory in healthy elderly-a resting state fMRI study. Neuroimage 52, 379–38810.1016/j.neuroimage.2010.03.062
- Zuo X. N., Di Martino A., Kelly C., Shehzad Z. E., Gee D. G., Klein D. F., Castellanos F. X., Biswal B. B., Milham M. P. (2010). The oscillating brain: complex and reliable. Neuroimage 49, 1432–144510.1016/j.neuroimage.2009.09.037
Source: PubMed