[en] Objectives:Recent fMRI studies have shown that it is possible to reliably identify the default-mode network (DMN) in the absence of any task, by resting-state connectivity analyses in healthy volunteers. We here aimed to identify the DMN in the challenging patient population of disorders of consciousness encountered following coma. Experimental design: A spatial independent component analysis-based methodology permitted DMN assessment, decomposing connectivity in all its different sources either neuronal or artifactual. Three different selection criteria were introduced assessing anticorrelation-corrected connectivity with or without an automatic masking procedure and calculating connectivity scores encompassing both spatial and temporal properties. These three methods were validated on 10 healthy controls and applied to an independent group of 8 healthy controls and 11 severely brain-damaged patients [locked-in syndrome (n = 2), minimally conscious (n = 1), and vegetative state (n = 8)]. Principal observations: All vegetative patients showed fewer connections in the default-mode areas, when compared with controls, contrary to locked-in patients who showed near-normal connectivity. In the minimally conscious-state patient, only the two selection criteria considering both spatial and temporal properties were able to identify an intact right lateralized BOLD connectivity pattern, and metabolic PET data suggested its neuronal origin. Conclusions: When assessing resting-state connectivity in patients with disorders of consciousness, it is important to use a methodology excluding non-neuronal contributions caused by head motion, respiration, and heart rate artifacts encountered in all studied patients. Hum Brain Mapp, 2011. (c) 2011 Wiley-Liss, Inc.
Research Center/Unit :
GIGA CRC (Cyclotron Research Center) In vivo Imaging-Aging & Memory - ULiège
Disciplines :
Physics
Author, co-author :
Soddu, Andrea ; Université de Liège - ULiège > Centre de recherches du cyclotron - Comascience group
Vanhaudenhuyse, Audrey ; Université de Liège - ULiège > Centre de recherches du cyclotron - Coma science group
Bahri, Mohamed Ali ; Université de Liège - ULiège > Centre de recherches du cyclotron
Bruno, Marie-Aurélie ; Université de Liège - ULiège > Centre de recherches du cyclotron
Boly, Mélanie ; Université de Liège - ULiège > Centre de Recherches du Cyclotron - Comascience group > Neurologie
Demertzi, Athina ; Université de Liège - ULiège > Centre de recherches du cyclotron - Comascience group
Tshibanda, J. F.
Phillips, Christophe ; Université de Liège - ULiège > Centre de recherches du cyclotron
Stanziano, M.
Ovadia-Caro, S.
Nir, Y.
Maquet, Pierre ; Université de Liège - ULiège > Centre de recherches du cyclotron
Papa, M.
Malach, R.; Université de Liège - ULiège > Centre de recherches du cyclotron
Laureys, Steven ; Université de Liège - ULiège > Centre de recherches du cyclotron - Comascience group
Noirhomme, Quentin ; Université de Liège - ULiège > Centre de recherches du cyclotron - comascience group
Identifying the default-mode component in spatial IC analyses of patients with disorders of consciousness.
Publication date :
2012
Journal title :
Human Brain Mapping
ISSN :
1065-9471
eISSN :
1097-0193
Publisher :
Wiley Liss, Inc., New York, United States - New York
Volume :
36
Pages :
37-43
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
Progetto FIRB Internazionalizzazione
Funders :
ISF - Israel Science Foundation [IL] MIUR - Ministero dell'Istruzione, dell'Università e della Ricerca [IT] EC - European Commission [BE] JSMF - James S McDonnell Foundation [US-MO] [US-MO] MSF - Mind Science Foundation [US-TX] [US-TX] FMRE - Fondation Médicale Reine Elisabeth [BE]
Funding number :
Contract grant number: 160/07
Funding text :
Contract grant number: RBIN04KW43; Contract grant sponsors: Italian Minerva Grants; European Commission (DISCOS-Marie Curie RTN, Mindbridge, DECODER
Alkire MT, Miller J (2005): General anesthesia and the neural correlates of consciousness. Prog Brain Res 150: 229-244.
American Congress of Rehabilitation Medicine (1995): Recommendations for use of uniform nomenclature pertinent to patients with severe alterations in consciousness. Arch Phys Med Rehabil 76: 205-209.
Anand A, Li Y, Wang Y, Wu J, Gao S, Bukhari L, Mathews VP, Kalnin A, Lowe MJ (2005): Activity and connectivity of brain mood regulating circuit in depression: A functional magnetic resonance study. Biol Psychiatry 57: 1079-1088.
Baars BJ, Ramsoy TZ, Laureys S (2003): Brain, conscious experience and the observing self. Trends Neurosci 26: 671-675.
Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005): Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 360: 1001-1013.
Birn RM, Murphy K, Bandettini PA (2008): The effect of respiration variations on independent component analysis results of resting state functional connectivity. Hum Brain Mapp 29: 740-750.
Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995): Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34: 537-541.
Boly M, Phillips C, Balteau E, Schnakers C, Degueldre C, Moonen G, Luxen A, Peigneux P, Faymonville ME, Maquet P, Laureys S (2008): Consciousness and cerebral baseline activity fluctuations. Hum Brain Mapp 29: 868-874.
Boly M, Tshibanda L, Vanhaudenhuyse A, Noirhomme Q, Schnakers C, Ledoux D, Boveroux P, Garweg C, Lambermont B, Phillips C, Luxen A, Moonen G, Bassetti C, Maquet P, Laureys S (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.
Born JD, Albert A, Hans P, Bonnal J (1985): Relative prognostic value of best motor response and brain stem reflexes in patients with severe head injury. Neurosurgery 16: 595-601.
Boveroux P, Vanhaudenhuyse A, Bruno MA, Noirhomme Q, Lauwick S, Luxen A, Degueldre C, Plenevaux A, Schnakers C, Phillips C, Brichant JF, Bonhomme V, Maquet P, Greicius MD, Laureys S, Boly M (2010): Breakdown of within- and between-network resting state functional magnetic resonance imaging connectivity during propofol-induced loss of consciousness. Anesthesiology 113: 1038-1053.
Calhoun VD, Eichele T, Pearlson G (2009): Functional brain networks in schizophrenia: A review. Front Hum Neurosci 3: 17.
Cole DM, Smith SM, Beckmann CF (2010): Advances and pitfalls in the analysis and interpretation of resting-state FMRI data. Front Syst Neurosci 4: 8.
Cordes D, Haughton VM, Arfanakis K, Wendt GJ, Turski PA, Moritz CH, et al. (2000): Mapping functionally related regions of brain with functional connectivity MR imaging. AJNR Am J Neuroradiol 21: 1636-1644.
Dai W, Carmichael OT, Lopez OL, Becker JT, Kuller LH, Gach HM (2008): Effects of image normalization on the statistical analysis of perfusion MRI in elderly brains. J Magn Reson Imaging 28: 1351-1360.
Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006): Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103: 13848-13853.
De Luca M, Beckmann CF, De Stefano N, Matthews PM, Smith SM (2006): fMRI resting state networks define distinct modes of long-distance interactions in the human brain. Neuroimage 29: 1359-1367.
De Martino F, Gentile F, Esposito F, Balsi M, Di Salle F, Goebel R, Formisano E (2007): Classification of fMRI independent components using IC-fingerprints and support vector machine classifiers. Neuroimage 34: 177-194.
Esposito F, Scarabino T, Hyvarinen A, Himberg J, Formisano E, Comani S, Tedeschi G, Goebel R, Seifritz E, Di Salle F (2005): Independent component analysis of fMRI group studies by self-organizing clustering. Neuroimage 25: 193-205.
Esposito F, Aragri A, Pesaresi I, Cirillo S, Tedeschi G, Marciano E, Goebel R, Di Salle 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 DA, Cohen AL, Dosenbach NU, Church JA, Miezin FM, Barch DM, Raichle ME, Petersen SE, Schlaggar BL (2008): The maturing architecture of the brain's default network. Proc Natl Acad Sci USA 105: 4028-4032.
Formisano E, Esposito F, Di Salle F, Goebel R (2004): Cortex-based independent component analysis of fMRI time series. Magn Reson Imaging 22: 1493-1504.
Fox MD, Raichle ME (2007): Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8: 700-711.
Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005): The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102: 9673-9678.
Fox MD, Zhang D, Snyder AZ, Raichle ME (2009): The global signal and observed anticorrelated resting state brain networks. J Neurophysiol 101: 3270-3283.
Giacino JT, Kalmar K, Whyte J (2004): The JFK Coma Recovery Scale-Revised: Measurement characteristics and diagnostic utility. Arch Phys Med Rehabil 85: 2020-2029.
Golland Y, Bentin S, Gelbard H, Benjamini Y, Heller R, Nir Y, Hasson U, Malach R (2007): Extrinsic and intrinsic systems in the posterior cortex of the human brain revealed during natural sensory stimulation. Cereb Cortex 17: 766-777.
Golland Y, Golland P, Bentin S, Malach R (2008): Data-driven clustering reveals a fundamental subdivision of the human cortex into two global systems. Neuropsychologia 46: 540-553.
Gray MA, Minati L, Harrison NA, Gianaros PJ, Napadow V, Critchley HD (2009): Physiological recordings: Basic concepts and implementation during functional magnetic resonance imaging. Neuroimage 47: 1105-1115.
Greicius MD, Menon V (2004): Default-mode activity during a passive sensory task: Uncoupled from deactivation but impacting activation. J Cogn Neurosci 16: 1484-1492.
Greicius MD, Krasnow B, Reiss AL, Menon V (2003): Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proc Natl Acad Sci USA 100: 253-258.
Greicius MD, Srivastava G, Reiss AL, Menon V (2004): Default-mode network activity distinguishes Alzheimer's disease from healthy aging: Evidence from functional MRI. Proc Natl Acad Sci USA 101: 4637-4642.
Gusnard DA, Akbudak E, Shulman GL, Raichle ME (2001): Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function. Proc Natl Acad Sci USA 98: 4259-4264.
Hagmann P, Cammoun L, Gigandet X, Gerhard S, Ellen Grant P, Wedeen V, Meuli R, Thiran JP, Honey CJ, Sporns O (2008): Mapping the structural core of human cerebral cortex. PLoS Biol 6: e159.
Hyvarinen A, Karhunen J, Oja E (2001): Independent Component Analysis. John Wiley & Sons.
Jafri MJ, Pearlson GD, Stevens M, Calhoun VD (2008): A method for functional network connectivity among spatially independent resting-state components in schizophrenia. Neuroimage 39: 1666-1681.
Kennedy DP, Redcay E, Courchesne E (2006): Failing to deactivate: Resting functional abnormalities in autism. Proc Natl Acad Sci USA 103: 8275-8280.
Kiviniemi V, Kantola JH, Jauhiainen J, Hyvärinen A, Tervonen O (2003): Independent component analysis of nondeterministic fMRI signal sources. Neuroimage 19: 253-260.
Kiviniemi V, Starck T, Remes J, Long X, Nikkinen J, Haapea M, Veijola J, Moilanen I, Isohanni M, Zang YF, Tervonen O (2009): Functional segmentation of the brain cortex using high model order group PICA. Hum Brain Mapp 30: 3865-3886.
Koch W, Teipel S, Mueller S, Buerger K, Bokde ALW, Hampel H, Coates U, Reiser M (2010): Effects of aging on default mode network activity in resting state fMRI: Does the method of analysis matter? Neuroimage 15: 280-287.
Laureys S, Owen AM, Schiff ND (2004): Brain function in coma, vegetative state, and related disorders. Lancet Neurol 3: 537-546.
Laureys S, Perrin F, Bredart S (2007): Self-consciousness in non-communicative patients. Conscious Cogn 16: 722-741; discussion 742-725.
Lowe MJ, Mock BJ, Sorenson JA (1998): Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage 7: 119-132.
Maquet P (1997): Positron emission tomography studies of sleep and sleep disorders. J Neurol 244: S23-S28.
McKeown MJ, Makeig S, Brown GG, Jung TP, Kindermann SS, Bell AJ, Sejnowski T (1998): Analysis of fMRI data by blind separation into independent spatial components. Hum Brain Mapp 6: 160-188.
Meindl T, Teipel S, Elmouden R, Mueller S, Koch W, Dietrich O, Coates U, Reiser M, Glaser C (2010): Test-retest reproducibility of the default-mode network in healthy individuals. Hum Brain Mapp 31: 237-246.
Minoshima S, Giordani B, Berent S, Frey KA, Foster NL, Kuhl DE (1997): Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease. Ann Neurol 42: 85-94.
Mitra PP, Ogawa S, Hu X, Ugurbil K (1997): The nature of spatiotemporal changes in cerebral hemodynamics as manifested in functional magnetic resonance imaging. Magn Reson Med 37: 511-518.
Murphy K, Birn RM, Handwerker DA, Jones TB, Bandettini PA (2009): The impact of global signal regression on resting state correlations: Are anti-correlated networks introduced? Neuroimage 44: 893-905.
Nir Y, Hasson U, Levy I, Yeshurun Y, Malach R (2006): Widespread functional connectivity and fMRI fluctuations in human visual cortex in the absence of visual stimulation. Neuroimage 30: 1313-1324.
Nir Y, Mukamel R, Dinstein I, Privman E, Harel M, Fisch L, Gelbard-Sagiv H, Kipervasser S, Andelman F, Neufeld MY, Kramer U, Arieli A, Fried I, Malach R (2008): Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex. Nat Neurosci 11: 1100-1108.
Perlbarg V, Marrelec G (2008): Contribution of exploratory methods to the investigation of extended large-scale brain networks in functional MRI: Methodologies, results, and challenges. Int J Biomed Imaging 2008: 218519.
Perlbarg V, Bellec P, Anton JL, Pelegrini-Issac M, Doyon J, Benali H (2007): CORSICA: Correction of structured noise in fMRI by automatic identification of ICA components. Magn Reson Imaging 25: 35-46.
Rainville P, Hofbauer RK, Bushnell MC, Duncan GH, Price DD (2002): Hypnosis modulates activity in brain structures involved in the regulation of consciousness. J Cogn Neurosci 14: 887-901.
Rombouts SA, Damoiseaux JS, Goekoop R, Barkhof F, Scheltens P, Smith SM, Beckmann CF (2009): Model-free group analysis shows altered BOLD FMRI networks in dementia. Hum Brain Mapp 30: 256-266.
Schilbach L, Eickhoff SB, Rotarska-Jagiela A, Fink GR, Vogeley K (2008): Minds at rest? Social cognition as the default mode of cognizing and its putative relationship to the "default system" of the brain. Conscious Cogn 17: 457-467.
Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF (2009): Correspondence of the brain's functional architecture during activation and rest. Proc Natl Acad Sci USA 106: 13040-13045.
Soddu A, Vanhaudenhuyse A, Demertzi A, Bruno MA, Tshibanda L, Di H, Boly M, Papa M, Laureys S, Noirhomme Q: Resting state activity in patients with disorders of consciousness. Funct Neurol 2011 (in press).
The Multi-Society Task Force on PVS (1994): Medical aspects of the persistent vegetative state (1). N Engl J Med 330: 1499-1508.
Vanhaudenhuyse A, Noirhomme Q, Tshibanda LJ, Bruno MA, Boveroux P, Schnakers C, Soddu A, Perlbarg V, Ledoux D, Brichant JF, Moonen G, Maquet P, Greicius MD, Laureys S, Boly M (2010): Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. Brain 133: 161-171.
Vanhaudenhuyse A, Demertzi A, Schabus M, Noirhomme Q, Bredart S, Boly M, Phillips C, Soddu A, Luxen A, Moonen G, Laureys S (2011): Two distinct neuronal networks mediate the awareness of environment and of self. J Cogn Neurosci 23(3):570-578.
Vincent JL, Patel GH, Fox MD, Snyder AZ, Baker JT, Van Essen DC, Zempel JM, Snyder LH, Corbetta M, Raichle ME (2007): Intrinsic functional architecture in the anaesthetized monkey brain. Nature 447: 83-86.
Weissman-Fogel I, Moayedi M, Taylor KS, Pope G, Davis KD (2010): Cognitive and default-mode resting state networks: Do male and female brains "rest" differently? Hum Brain Mapp 31: 1713-1726.
Xiong J, Parsons LM, Gao JH, Fox PT (1999): Interregional connectivity to primary motor cortex revealed using MRI resting state images. Hum Brain Mapp 8: 151-156.
Yang H, Long XY, Yang Y, Yan H, Zhu CZ, Zhou XP, Zang YF, Gong QY (2007): Amplitude of low frequency fluctuation within visual areas revealed by resting-state functional MRI. Neuroimage 36: 144-152.
Ylipaavalniemi J, Vigario R (2008): Analyzing consistency of independent components: An fMRI illustration. Neuroimage 39: 169-180.
