Shifted Coupling of EEG Driving Frequencies and fMRI Resting State Networks in Schizophrenia Spectrum Disorders

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Razavi, Nadja ^a   Jann, Kay ^a,b   Koenig, Thomas ^a   Kottlow, Mara ^a   Hauf, Martinus ^a   Strik, Werner ^a   Dierks, Thomas ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIDEPRESSANT AGENT; ATYPICAL ANTIPSYCHOTIC AGENT; CHLORPROMAZINE; DIAZEPAM; MOOD STABILIZER; NEUROLEPTIC AGENT; TRANQUILIZER;

ADULT; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; DEFAULT MODE NETWORK; DISEASE ASSOCIATION; ELECTROENCEPHALOGRAPHY; FEMALE; FREQUENCY ANALYSIS; FUNCTIONAL ASSESSMENT; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; PATHOPHYSIOLOGY; PSYCHOSIS; RESTING STATE NETWORK; SCHIZOPHRENIA; WORKING MEMORY;

ADULT; BRAIN; BRAIN MAPPING; CASE-CONTROL STUDIES; ELECTROENCEPHALOGRAPHY; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; SCHIZOPHRENIA; YOUNG ADULT;

EID: 84885084794     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076604     Document Type: Article

References (109)

1. American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders: DSM-IV. Washington (DC): American Psychiatric Association.
2. Saha S, Chant D, Welham J, McGrath J, (2005) A systematic review of the prevalence of schizophrenia. PLoS Med 2: 413-433.
3. Andreasen NC, (1997) Linking mind and brain in the study of mental illnesses: a project for a scientific psychopathology. Science 275: 1586-1593.
4. Friston KJ, (1998) The disconnection hypothesis. Schizophr Res 30: 115-125.
5. McGuire PK, Frith CD, (1996) Disordered functional connectivity in schizophrenia. Psychol Med 26: 663-667.
6. Friston KJ (1999) Schizophrenia and the disconnection hypothesis. Acta Psychiatr Scand Suppl 395: 68-79.
7. 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.
8. Lowe MJ, Mock BJ, Sorenson JA, (1998) Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage 7: 119-132.
9. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, et al. (2001) A default mode of brain function. Proc Natl Acad Sci U S A 98: 676-682.
10. Zhang D, Raichle ME, (2010) Disease and the brain's dark energy. Nature Rev Neurosci 6: 15-28.
11. Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, et al. (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci U S A 103: 13848-13853.
12. 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.
13. 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 U S A 98: 4259-4264.
14. Greicius M, (2008) Resting-state functional connectivity in neuropsychiatric disorders. Curr Opin Neurol 21: 424-430.
15. Luchinger R, Michels L, Martin E, Brandeis D, (2011) EEG-BOLD correlations during (post-) adolescent brain maturation. Neuroimage 56: 1493-1505.
16. Olbrich S, Mulert C, Karch S, Trenner M, Leicht G, et al. (2009) EEG-vigilance and BOLD effect during simultaneous EEG/fMRI measurement. Neuroimage 45: 319-332.
17. Sala-Llonch R, Pena-Gomez C, Arenaza-Urquijo EM, Vidal-Pineiro D, Bargallo N, et al. (2012) Brain connectivity during resting state and subsequent working memory task predicts behavioural performance. Cortex 48: 1187-1196.
18. Liu X, Zhu XH, Chen W, (2011) Baseline BOLD correlation predicts individuals' stimulus-evoked BOLD responses. Neuroimage 54: 2278-2286.
19. Calhoun VD, Eichele T, Pearlson G, (2009) Functional brain networks in schizophrenia: a review. Front Hum Neurosci 3: 17.
20. Whitfield-Gabrieli S, Thermenos HW, Milanovic S, Tsuang MT, Faraone SV, et al. (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.
21. Whitfield-Gabrieli S, Ford JM, (2012) Default mode network activity and connectivity in psychopathology. Annu Rev Clin Psychol 8: 49-76.
22. Northoff G, Qin P, (2011) How can the brain's resting state activity generate hallucinations? A 'resting state hypothesis' of auditory verbal hallucinations. Schizophr Res 127: 202-214.
23. Karbasforoushan H, Woodward ND, (2012) Resting-state networks in schizophrenia. Curr Top Med Chem 12: 2404-2414.
24. Broyd SJ, Demanuele C, Debener S, Helps SK, James CJ, et al. (2009) Default-mode brain dysfunction in mental disorders: A systematic review. Neurosci Biobehav Rev 33: 279-296.
25. 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.
26. Carter CS, MacDonald AW, (2001) Anterior cingulate cortex activity and impaired self-monitoring of performance in patients with schizophrenia: an event-related fMRI study. Am J Psychiatry 158: 1423-1428.
27. MacDonald AW, (2003) Event-related FMRI study of context processing in dorsolateral prefrontal cortex of patients with schizophrenia. J Abnorm Psychol 112: 689-697.
28. Minzenberg MJ, Laird AR, Thelen S, Carter CS, Glahn DC, (2009) Meta-analysis of 41 functional neuroimaging studies of executive function in schizophrenia. Arch Gen Psychiatry 66: 811-822.
29. Assaf M, Jagannathan K, Calhoun V, Kraut M, Hart J Jr, et al. (2009) Temporal sequence of hemispheric network activation during semantic processing: a functional network connectivity analysis. Brain Cogn 70: 238-246.
30. Jann K, Kottlow M, Dierks T, Boesch C, Koenig T, (2010) Topographic electrophysiological signatures of FMRI Resting State Networks. PLoS One 5: e12945.
31. Wu X, Lu J, Chen K, Long Z, Wang X, et al. (2009) Multiple neural networks supporting a semantic task: an fMRI study using independent component analysis. Neuroimage 45: 1347-1358.
32. Horn H, Jann K, Federspiel A, Walther S, Wiest R, et al. (2012) Semantic network disconnection in formal thought disorder. Neuropsychobiology 66: 14-23.
33. Ellison-Wright I, Bullmore E, (2009) Meta-analysis of diffusion tensor imaging studies in schizophrenia. Schizophr Res 108: 3-10.
34. Gur RE, Keshavan MS, Lawrie SM, (2007) Deconstructing psychosis with human brain imaging. Schizophr Bull 33: 921-931.
35. Camchong J, Macdonald AW III, Bell C, Mueller BA, Lim KO, (2009) Altered Functional and Anatomical Connectivity in Schizophrenia. Schizophr Bull 37: 640-650.
36. Federspiel A, Begre S, Kiefer C, Schroth G, Strik WK, et al. (2006) Alterations of white matter connectivity in first episode schizophrenia. Neurobiol Dis 22: 702-709.
37. Rotarska-Jagiela A, Oertel-Knoechel V, Demartino F, van dV, V, Formisano E, et al. (2009) Anatomical brain connectivity and positive symptoms of schizophrenia: A diffusion tensor imaging study. Psychiatry Res 174: 9-16.
38. Koch K, Schultz CC, Wagner G, Schachtzabel C, Reichenbach JR, et al. (2012) Disrupted white matter connectivity is associated with reduced cortical thickness in the cingulate cortex in schizophrenia. Cortex: In press.
39. Repovs G, Csernansky JG, Barch DM, (2010) Brain Network Connectivity in Individuals with Schizophrenia and Their Siblings. Biol Psychiatry 69: 967-973.
40. Salomon R, Bleich-Cohen M, Hahamy-Dubossarsky A, Dinstien I, Weizman R, et al. (2011) Global Functional Connectivity Deficits in Schizophrenia Depend on Behavioral State. J Neurosci 31: 12972-12981.
41. Skudlarski P, Jagannathan K, Anderson K, Stevens MC, Calhoun VD, et al. (2010) Brain connectivity is not only lower but different in schizophrenia: a combined anatomical and functional approach. Biol Psychiatry 68: 61-69.
42. Wolf ND, Sambataro F, Vasic N, Frasch K, Schmid M, et al. (2011) Dysconnectivity of multiple resting-state networks in patients with schizophrenia who have persistent auditory verbal hallucinations. J Psychiatry Neurosci 36: 110008.
43. Woodward ND, Rogers B, Heckers S, (2011) Functional resting-state networks are differentially affected in schizophrenia. Schizophr Res 130: 86-93.
44. Pettersson-Yeo W, Allen P, Benetti S, McGuire P, Mechelli A, (2010) Dysconnectivity in schizophrenia: Where are we now? Neurosci Biobehav Rev 35: 1110-1124.
45. Singer W, (2001) Consciousness and the binding problem. Ann NY Acad Sci 929: 123-146.
46. Varela F, Lachaux JP, Rodriguez E, Martinerie J, (2001) The brainweb: phase synchronization and large-scale integration. Nature Rev Neurosci 2: 229-239.
47. Jann K, Dierks T, Boesch C, Kottlow M, Strik W, et al. (2009) BOLD correlates of EEG alpha phase-locking and the fMRI default mode network. Neuroimage 45: 903-916.
48. Buxton RB, Wong EC, Frank LR, (1998) Dynamics of blood flow and oxygenation changes during brain activation: The balloon model. Magn Res Med 39: 855-864.
49. Obata T, Liu TT, Miller KL, Luh WM, Wong EC, et al. (2004) Discrepancies between BOLD and flow dynamics in primary and supplementary motor areas: application of the balloon model to the interpretation of BOLD transients. Neuroimage 21: 144-153.
50. Buxton RB, Uludag K, Dubowitz DJ, Liu TT, (2004) Modeling the hemodynamic response to brain activation. Neuroimage 23Suppl 1: S220-S233.
51. Low MD (1987) Psychology, Psychophysiology, and the EEG. In: Niedermeyer E, Lopes da Silva FH, Electroencephalography: basic principles, clinical applications, and related fields. 2nd ed. Baltimore-Munich: Urban & Schwarzenberg. 541-548.
52. Niedermeyer E (1987) Sleep and EEG. In: Niedermeyer E, Lopes da Silva FH, Electroencephalography: basic principles, clinical applications and related fields. 2nd ed. Baltimore-Munich: Urban & Schwarzenberg. 119-132.
53. Niedermeyer E (1987) The normal EEG of the waking adult. In: Niedermeyer E, Lopes da Silva FH,Electroencephalography: basic principles, clinical applications and related fields. 2nd ed. Baltimore-Munich: Urban & Schwarzenberg. 97-117.
54. Boutros NN, Arfken C, Galderisi S, Warrick J, Pratt G, et al. (2008) The status of spectral EEG abnormality as a diagnostic test for schizophrenia. Schizophr Res 99: 225-237.
55. Galderisi S, Mucci A, Mignone ML, Maj M, Kemali D, (1991) CEEG mapping in drug-free schizophrenics. Differences from healthy subjects and changes induced by haloperidol treatment. Schizophr Res 6: 15-23.
56. Dierks T, Mueller T, (2009) EEG and EP in Psychiatrc Disorders. Epileptologie 26: 21-27.
57. Galderisi S, Mucci A, Volpe U, Boutros N, (2009) Evidence-based medicine and electrophysiology in schizophrenia. Clin EEG Neurosci 40: 62-77.
58. Mientus S, Gallinat J, Wuebben Y, Pascual-Marqui RD, Mulert C, et al. (2002) Cortical hypoactivation during resting EEG in schizophrenics but not in depressives and schizotypal subjects as revealed by low resolution electromagnetic tomography (LORETA). Psychiatry Res 116: 95-111.
59. Sponheim SR, Clementz BA, Iacono WG, Beiser M, (2000) Clinical and biological concomitants of resting state EEG power abnormalities in schizophrenia. Biol Psychiatry 48: 1088-1097.
60. Venables NC, Bernat EM, Sponheim SR, (2009) Genetic and disorder-specific aspects of resting state EEG abnormalities in schizophrenia. Schizophr Bull 35: 826-839.
61. Laufs H, Holt JL, Elfont R, Krams M, Paul JS, et al. (2006) Where the BOLD signal goes when alpha EEG leaves. Neuroimage 31: 1408-1418.
62. Mantini D, Perrucci MG, Del Gratta C, Romani GL, Corbetta M, (2007) Electrophysiological signatures of resting state networks in the human brain. Proc Natl Acad Sci U S A 104: 13170-13175.
63. Hughes JR, John ER, (1999) Conventional and quantitative electroencephalography in psychiatry. J Neuropsychiatry Clin Neurosci 11: 190-208.
64. World Health Organization (1993) The ICD-10 Classification of Mental and Behavioral Disorders: Diagnostic Criteria for Research. Geneva: World Health Organization.
65. Deichmann R, Schwarzbauer C, Turner R, (2004) Optimisation of the 3D MDEFT sequence for anatomical brain imaging: technical implications at 1.5 and 3 T. Neuroimage 21: 757-767.
66. Ferree TC, Luu P, Russell GS, Tucker DM, (2001) Scalp electrode impedance, infection risk, and EEG data quality. Clin Neurophysiol 112: 536-544.
67. Kappenman ES, Luck SJ, (2010) The effects of electrode impedance on data quality and statistical significance in ERP recordings. Psychophysiology 47: 888-904.
68. Mandelkow H, Halder P, Boesiger P, Brandeis D, (2006) Synchronization facilitates removal of MRI artefacts from concurrent EEG recordings and increases usable bandwidth. Neuroimage 32: 1120-1126.
69. Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. New York: Thieme.
70. Esposito F, Scarabino T, Hyvarinen A, Himberg J, Formisano E, et al. (2005) Independent component analysis of fMRI group studies by self-organizing clustering. Neuroimage 25: 193-205.
71. Gallo A, Esposito F, Sacco R, Docimo R, Bisecco A, et al. (2012) Visual resting-state network in relapsing-remitting MS with and without previous optic neuritis. Neurology 79: 1458-1465.
72. Esposito F, Goebel R, (2011) Extracting functional networks with spatial independent component analysis: the role of dimensionality, reliability and aggregation scheme. Curr Opin Neurol 24: 378-385.
73. 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.
74. De Martino F, Gentile F, Esposito F, Balsi M, Di Salle F, et al. (2007) Classification of fMRI independent components using IC-fingerprints and support vector machine classifiers. Neuroimage 34: 177-194.
75. Franco AR, Pritchard A, Calhoun VD, Mayer AR, (2009) Interrater and intermethod reliability of default mode network selection. Hum Brain Mapp 30: 2293-2303.
76. Allen PJ, Josephs O, Turner R, (2000) A method for removing imaging artifact from continuous EEG recorded during functional MRI. Neuroimage 12: 230-239.
77. Kottlow M, Jann K, Dierks T, Koenig T, (2012) Increased phase synchronization during continuous face integration measured simultaneously with EEG and fMRI. Clin Neurophysiol 123: 1536-1548.
78. Aguirre GK, Zarahn E, D'esposito M, (1998) The variability of human, BOLD hemodynamic responses. Neuroimage 8: 360-369.
79. Koenig T, Melie-Garcia L, Stein M, Strik W, Lehmann C, (2008) Establishing correlations of scalp field maps with other experimental variables using covariance analysis and resampling methods. Clin Neurophysiol 119: 1262-1270.
80. Koenig T, Melie-Garcia L, (2010) A method to determine the presence of averaged event-related fields using randomization tests. Brain Topogr 23: 233-242.
81. Koenig T, Kottlow M, Stein M, Melie-Garcia L, (2011) Ragu: a free tool for the analysis of EEG and MEG event-related scalp field data using global randomization statistics. Comput Intell Neurosci 2011: 938925.
82. Strik WK, Fallgatter AJ, Brandeis D, Pascual-Marqui RD, (1998) Three-dimensional tomography of event-related potentials during response inhibition: evidence for phasic frontal lobe activation. Electroencephalogr Clin Neurophysiol 108: 406-413.
83. Rotarska-Jagiela A, van dV, V, Oertel-Knochel V, Uhlhaas PJ, Vogeley K, et al. (2010) Resting-state functional network correlates of psychotic symptoms in schizophrenia. Schizophr Res 117: 21-30.
84. Diederen KM, De Weijer AD, Daalman K, Blom JD, Neggers SF, et al. (2010) Decreased language lateralization is characteristic of psychosis, not auditory hallucinations. Brain 133: 3734-3744.
85. Crow TJ, (1997) Is schizophrenia the price that Homo sapiens pays for language? Schizophr Res 28: 127-141.
86. Sommer IE, Ramsey NF, Kahn RS, (2001) Language lateralization in schizophrenia, an fMRI study. Schizophr Res 52: 57-67.
87. Miyauchi T, Endo S, Kajiwara S, Ishii M, Okajima J, (1996) Computerized electroencephalogram in untreated schizophrenics: a comparison between disorganized and paranoid types. Psychiatry Clin Neurosci 50: 71-78.
88. Pascual-Marqui RD, Sekihara K, Brandeis D, Michel CM (2009) Imaging the electric neuronal generators of EEG/MEG. In: Michel CM, Koenig T, Brandeis D, Gianotti LR, Wackermann J, Cambridge: Cambridge University Press. 49-77.
89. Gordon E, Palmer DM, Cooper N, (2010) EEG alpha asymmetry in schizophrenia, depression, PTSD, panic disorder, ADHD and conduct disorder. Clin EEG Neurosci 41: 178-183.
90. Ishii R, Shinosaki K, Ikejiri Y, Ukai S, Yamashita K, et al. (2000) Theta rhythm increases in left superior temporal cortex during auditory hallucinations in schizophrenia: a case report. Neuroreport 11: 3283-3287.
91. Kim DI, Manoach DS, Mathalon DH, Turner JA, Mannell M, et al. (2009) Dysregulation of working memory and default-mode networks in schizophrenia using independent component analysis, an fBIRN and MCIC study. Hum Brain Mapp 30: 3795-3811.
92. Meda SA, Stevens MC, Folley BS, Calhoun VD, Pearlson GD, (2009) Evidence for anomalous network connectivity during working memory encoding in schizophrenia: an ICA based analysis. PLoS One 4: e7911.
93. Nikulin VV, Brismar T, (2006) Phase synchronization between alpha and beta oscillations in the human electroencephalogram. Neuroscience 137: 647-657.
94. Garrity AG, Pearlson GD, McKiernan K, Lloyd D, Kiehl KA, et al. (2007) Aberrant "default mode" functional connectivity in schizophrenia. Am J Psychiatry 164: 450-457.
95. Kim DI, Mathalon DH, Ford JM, Mannell M, Turner JA, et al. (2009) Auditory oddball deficits in schizophrenia: an independent component analysis of the fMRI multisite function BIRN study. Schizophr Bull 35: 67-81.
96. McKiernan KA, Kaufman JN, Kucera-Thompson J, Binder JR, (2003) A parametric manipulation of factors affecting task-induced deactivation in functional neuroimaging. J Cogn Neurosci 15: 394-408.
97. Bates AT, Kiehl KA, Laurens KR, Liddle PF, (2009) Low-frequency EEG oscillations associated with information processing in schizophrenia. Schizophr Res 115: 222-230.
98. Klimesch W, (1999) EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Brain Res Rev 29: 169-195.
99. Scheeringa R, Bastiaansen MC, Petersson KM, Oostenveld R, Norris DG, et al. (2008) Frontal theta EEG activity correlates negatively with the default mode network in resting state. Int J Psychophysiol 67: 242-251.
100. Hanslmayr S, Backes H, Straub S, Popov T, Langguth B, et al. (2012) Enhanced resting-state oscillations in schizophrenia are associated with decreased synchronization during inattentional blindness. Hum Brain Mapp: In press.
101. Ogilvie RD, (2001) The process of falling asleep. Sleep Med Rev 5: 247-270.
102. Strijkstra AM, Beersma DG, Drayer B, Halbesma N, Daan S, (2003) Subjective sleepiness correlates negatively with global alpha (8-12 Hz) and positively with central frontal theta (4-8 Hz) frequencies in the human resting awake electroencephalogram. Neurosci Lett 340: 17-20.
103. Tanaka H, Hayashi M, Hori T, (1997) Topographical characteristics and principal component structure of the hypnagogic EEG. Sleep 20: 523-534.
104. Hayashi M, Katoh K, Hori T, (1999) Hypnagogic imagery and EEG activity. Percept Mot Skills 88: 676-678.
105. Yang CM, Han HY, Yang MH, Su WC, Lane T, (2010) What subjective experiences determine the perception of falling asleep during sleep onset period? Conscious Cogn 19: 1084-1092.
106. Sham PC, MacLean CJ, Kendler KS, (1994) A typological model of schizophrenia based on age at onset, sex and familial morbidity. Acta Psychiatr Scand 89: 135-141.
107. Segalowitz SJ, Santesso DL, Jetha MK, (2010) Electrophysiological changes during adolescence: a review. Brain Cogn 72: 86-100.
108. Douaud G, Mackay C, Andersson J, James S, Quested D, et al. (2009) Schizophrenia delays and alters maturation of the brain in adolescence. Brain 132: 2437-2448.
109. Paus T, Keshavan M, Giedd JN, (2008) Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 9: 947-957.