EEG-BOLD correlations during (post-)adolescent brain maturation

NeuroImage

Volumn 56, Issue 3, 2011, Pages 1493-1505

  Lüchinger, Rafael ^a   Michels, Lars ^b   Martin, Ernst ^a,b   Brandeis, Daniel ^a,c  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^c CENTRAL INSTITUTE OF MENTAL HEALTH   (Germany)

Author keywords

Adolescence; EEG BOLD coupling; Eyes open eyes closed; Global spectral power; Late brain maturation; Resting state; Simultaneous EEG fRMI

Indexed keywords

OXYGEN;

ADOLESCENT; ADULT; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN MATURATION; CELL MATURATION; CONTROLLED STUDY; CORRELATIONAL STUDY; DEVELOPMENTAL STAGE; ELECTROENCEPHALOGRAM; EYELID CLOSURE; FEMALE; FREQUENCY MODULATION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; MALE; NERVE CELL; NEUROPHYSIOLOGY; NORMAL HUMAN; OXYGEN BLOOD LEVEL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ADOLESCENT; ADULT; AGING; ALPHA RHYTHM; BRAIN; DATA INTERPRETATION, STATISTICAL; DELTA RHYTHM; ELECTROENCEPHALOGRAPHY; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MODELS, NEUROLOGICAL; NERVE NET; OXYGEN; PHOTIC STIMULATION; REGRESSION ANALYSIS; REST; THETA RHYTHM; YOUNG ADULT;

EID: 79955466089     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.02.050     Document Type: Article

References (73)

1. Allen P.J., Josephs O., Turner R. A method for removing imaging artifact from continuous EEG recorded during functional MRI. Neuroimage 2000, 12:230-239.
2. Allen P.J., Polizzi G., Krakow K., Fish D.R., Lemieux L. Identification of EEG events in the MR scanner: the problem of pulse artifact and a method for its subtraction. Neuroimage 1998, 8:229-239.
3. Barry R.J., Clarke A.R., Johnstone S.J., Magee C.A., Rushby J.A. EEG differences between eyes-closed and eyes-open resting conditions. Clin. Neurophysiol. 2007, 118:2765-2773.
4. Beckmann C.F., DeLuca M., Devlin J.T., Smith S.M. Investigations into resting-state connectivity using independent component analysis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005, 360:1001-1013.
5. Ben-Simon E., Podlipsky I., Arieli A., Zhdanov A., Hendler T. Never resting brain: simultaneous representation of two alpha related processes in humans. PLoS ONE 2008, 3:e3984.
6. Berger H. Über das Elektrenkephalogramm des Menschen. Eur. Arch. Psychiatry Clin. Neurosci. 1929, 87:527-570.
7. Bianciardi M., Fukunaga M., van Gelderen P., Horovitz S.G., de Zwart J.A., Duyn J.H. Modulation of spontaneous fMRI activity in human visual cortex by behavioral state. Neuroimage 2009, 45:160-168.
8. Blakemore S.J., Choudhury S. Brain development during puberty: state of the science. Dev. Sci. 2006, 9:11-14.
9. Boord P.R., Rennie C.J., Williams L.M. Integrating "brain" and "body" measures: correlations between EEG and metabolic changes over the human lifespan. J. Integr. Neurosci. 2007, 6:205-218.
10. Brem S., Bach S., Kucian K., Guttorm T.K., Martin E., Lyytinen H., Brandeis D., Richardson U. Brain sensitivity to print emerges when children learn letter-speech sound correspondences. Proc. Natl Acad. Sci. USA 2010, 107:7939-7944.
11. Campbell I.G., Feinberg I. Longitudinal trajectories of non-rapid eye movement delta and theta EEG as indicators of adolescent brain maturation. Proc. Natl Acad. Sci. USA 2009, 106:5177-5180.
12. Case R. The role of the frontal lobes in the regulation of cognitive development. Brain Cogn. 1992, 20:51-73.
13. Clarke A.R., Barry R.J., McCarthy R., Selikowitz M. Age and sex effects in the EEG: development of the normal child. Clin. Neurophysiol. 2001, 112:806-814.
14. Damoiseaux J.S., Rombouts S.A., Barkhof F., Scheltens P., Stam C.J., Smith S.M., Beckmann C.F. Consistent resting-state networks across healthy subjects. Proc. Natl Acad. Sci. USA 2006, 103:13848-13853.
15. de Munck J.C., Goncalves S.I., Huijboom L., Kuijer J.P., Pouwels P.J., Heethaar R.M., Lopes da Silva F.H. The hemodynamic response of the alpha rhythm: an EEG/fMRI study. Neuroimage 2007, 35:1142-1151.
16. de Munck J.C., Goncalves S.I., Mammoliti R., Heethaar R.M., Lopes da Silva F.H. Interactions between different EEG frequency bands and their effect on alpha-fMRI correlations. Neuroimage 2009, 47:69-76.
17. Delorme A., Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Meth. 2004, 134:9-21.
18. Difrancesco M.W., Holland S.K., Szaflarski J.P. Simultaneous EEG/functional magnetic resonance imaging at 4 Tesla: correlates of brain activity to spontaneous alpha rhythm during relaxation. J. Clin. Neurophysiol. 2008, 25:255-264.
19. Dustman R.E., Shearer D.E., Emmerson R.Y. Life-span changes in EEG spectral amplitude, amplitude variability and mean frequency. Clin. Neurophysiol. 1999, 110:1399-1409.
20. Fair D.A., Dosenbach N.U., Church J.A., Cohen A.L., Brahmbhatt S., Miezin F.M., Barch D.M., Raichle M.E., Petersen S.E., Schlaggar B.L. Development of distinct control networks through segregation and integration. Proc. Natl Acad. Sci. USA 2007, 104:13507-13512.
21. Feige B., Scheffler K., Esposito F., Di Salle F., Hennig J., Seifritz E. Cortical and subcortical correlates of electroencephalographic alpha rhythm modulation. J. Neurophysiol. 2005, 93:2864-2872.
22. Feinberg I., Campbell I.G. Sleep EEG changes during adolescence: an index of a fundamental brain reorganization. Brain Cogn. 2010, 72:56-65.
23. Forman S.D., Cohen J.D., Fitzgerald M., Eddy W.F., Mintun M.A., Noll D.C. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn. Reson. Med. 1995, 33:636-647.
24. Fox M.D., Snyder A.Z., Vincent J.L., Corbetta M., Van Essen D.C., Raichle M.E. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl Acad. Sci. USA 2005, 102:9673-9678.
25. Gasser T., Verleger R., Bacher P., Sroka L. Development of the EEG of school-age children and adolescents. I. Analysis of band power. Electroencephalogr. Clin. Neurophysiol. 1988, 69:91-99.
26. Gastaut H. Electrocorticographic study of the reactivity of rolandic rhythm. Rev. Neurol. (Paris) 1952, 87:176-182.
27. Gibbs F.A., Knott J.R. Growth of the electrical activity of the cortex. Electroencephalogr. Clin. Neurophysiol. 1949, 1:223-229.
28. Giedd J.N., Blumenthal J., Jeffries N.O., Castellanos F.X., Liu H., Zijdenbos A., Paus T., Evans A.C., Rapoport J.L. Brain development during childhood and adolescence: a longitudinal MRI study. Nat. Neurosci. 1999, 2:861-863.
29. Gogtay N., Giedd J.N., Lusk L., Hayashi K.M., Greenstein D., Vaituzis A.C., Nugent T.F., Herman D.H., Clasen L.S., Toga A.W., Rapoport J.L., Thompson P.M. Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl Acad. Sci. USA 2004, 101:8174-8179.
30. Goldman R.I., Stern J.M., Engel J., Cohen M.S. Simultaneous EEG and fMRI of the alpha rhythm. NeuroReport 2002, 13:2487-2492.
31. Goncalves S.I., de Munck J.C., Pouwels P.J., Schoonhoven R., Kuijer J.P., Maurits N.M., Hoogduin J.M., Van Someren E.J., Heethaar R.M., Lopes da Silva F.H. Correlating the alpha rhythm to BOLD using simultaneous EEG/fMRI: inter-subject variability. Neuroimage 2006, 30:203-213.
32. Henning S., Merboldt K.D., Frahm J. Task- and EEG-correlated analyses of BOLD MRI responses to eyes opening and closing. Brain Res. 2006, 1073-1074:359-364.
33. Jann K., Dierks T., Boesch C., Kottlow M., Strik W., Koenig T. BOLD correlates of EEG alpha phase-locking and the fMRI default mode network. Neuroimage 2009, 45:903-916.
34. John E.R., Ahn H., Prichep L., Trepetin M., Brown D., Kaye H. Developmental equations for the electroencephalogram. Science 1980, 210:1255-1258.
35. Jung T.P., Makeig S., Westerfield M., Townsend J., Courchesne E., Sejnowski T.J. Removal of eye activity artifacts from visual event-related potentials in normal and clinical subjects. Clin. Neurophysiol. 2000, 111:1745-1758.
36. Laufs H. Endogenous brain oscillations and related networks detected by surface EEG-combined fMRI. Hum. Brain Mapp. 2008, 29:762-769.
37. Laufs H., Holt J.L., Elfont R., Krams M., Paul J.S., Krakow K., Kleinschmidt A. Where the BOLD signal goes when alpha EEG leaves. Neuroimage 2006, 31:1408-1418.
38. Laufs H., Kleinschmidt A., Beyerle A., Eger E., Salek-Haddadi A., Preibisch C., Krakow K. EEG-correlated fMRI of human alpha activity. Neuroimage 2003, 19:1463-1476.
39. Laufs H., Krakow K., Sterzer P., Eger E., Beyerle A., Salek-Haddadi A., Kleinschmidt A. Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest. Proc. Natl Acad. Sci. USA 2003, 100:11053-11058.
40. Lehmann D., Skrandies W. Reference-free identification of components of checkerboard-evoked multichannel potential fields. Electroencephalogr. Clin. Neurophysiol. 1980, 48:609-621.
41. Logothetis N.K., Pauls J., Augath M., Trinath T., Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 2001, 412:150-157.
42. Luna B., Padmanabhan A., O'Hearn K. What has fMRI told us about the development of cognitive control through adolescence?. Brain Cogn. 2010, 72:101-113.
43. Mantini D., Perrucci M.G., Del Gratta C., Romani G.L., Corbetta M. Electrophysiological signatures of resting state networks in the human brain. Proc. Natl Acad. Sci. USA 2007, 104:13170-13175.
44. Marx E., Deutschlander A., Stephan T., Dieterich M., Wiesmann M., Brandt T. Eyes open and eyes closed as rest conditions: impact on brain activation patterns. Neuroimage 2004, 21:1818-1824.
45. Marx E., Stephan T., Nolte A., Deutschlander A., Seelos K.C., Dieterich M., Brandt T. Eye closure in darkness animates sensory systems. Neuroimage 2003, 19:924-934.
46. Matousek M., Petersen I. Automatic evaluation of EEG background activity by means of age-dependent EEG quotients. Electroencephalogr. Clin. Neurophysiol. 1973, 35:603-612.
47. Maurer U., Brem S., Bucher K., Kranz F., Benz R., Steinhausen H.C., Brandeis D. Impaired tuning of a fast occipito-temporal response for print in dyslexic children learning to read. Brain 2007, 130:3200-3210.
48. Michels L., Bucher K., Luchinger R., Klaver P., Martin E., Jeanmonod D., Brandeis D. Simultaneous EEG-fMRI during a working memory task: modulations in low and high frequency bands. PLoS ONE 2010, 5:e10298.
49. Moosmann M., Ritter P., Krastel I., Brink A., Thees S., Blankenburg F., Taskin B., Obrig H., Villringer A. Correlates of alpha rhythm in functional magnetic resonance imaging and near infrared spectroscopy. Neuroimage 2003, 20:145-158.
50. Nir Y., Fisch L., Mukamel R., Gelbard-Sagiv H., Arieli A., Fried I., Malach R. Coupling between neuronal firing rate, gamma LFP, and BOLD fMRI is related to interneuronal correlations. Curr. Biol. 2007, 17:1275-1285.
51. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
52. Paus T. Mapping brain maturation and cognitive development during adolescence. Trends Cogn. Sci. 2005, 9:60-68.
53. Paus T., Keshavan M., Giedd J.N. Why do many psychiatric disorders emerge during adolescence?. Nat. Rev. Neurosci. 2008, 9:947-957.
54. Pfurtscheller G. Central beta rhythm during sensorimotor activities in man. Electroencephalogr. Clin. Neurophysiol. 1981, 51:253-264.
55. Pfurtscheller G. Functional brain imaging based on ERD/ERS. Vis. Res. 2001, 41:1257-1260.
56. Puligheddu M., de Munck J.C., Stam C.J., Verbunt J., de Jongh A., van Dijk B.W., Marrosu F. Age distribution of MEG spontaneous theta activity in healthy subjects. Brain Topogr. 2005, 17:165-175.
57. Raichle M.E., MacLeod A.M., Snyder A.Z., Powers W.J., Gusnard D.A., Shulman G.L. A default mode of brain function. Proc. Natl Acad. Sci. USA 2001, 98:676-682.
58. Raichle M.E., Snyder A.Z. A default mode of brain function: a brief history of an evolving idea. Neuroimage 2007, 37:1083-1090. discussion 1097-1089.
59. Ritter P., Moosmann M., Villringer A. Rolandic alpha and beta EEG rhythms' strengths are inversely related to fMRI-BOLD signal in primary somatosensory and motor cortex. Hum. Brain Mapp. 2009, 30:1168-1187.
60. Salmelin R., Hari R. Characterization of spontaneous MEG rhythms in healthy adults. Electroencephalogr. Clin. Neurophysiol. 1994, 91:237-248.
61. Scheeringa R., Bastiaansen M.C., Petersson K.M., Oostenveld R., Norris D.G., Hagoort P. Frontal theta EEG activity correlates negatively with the default mode network in resting state. Int. J. Psychophysiol. 2008, 67:242-251.
62. Sisk C.L., Foster D.L. The neural basis of puberty and adolescence. Nat. Neurosci. 2004, 7:1040-1047.
63. Slotnick S.D., Moo L.R., Segal J.B., Hart J. Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. Brain Res. Cogn. Brain Res. 2003, 17:75-82.
64. Sowell E.R., Thompson P.M., Tessner K.D., Toga A.W. Mapping continued brain growth and gray matter density reduction in dorsal frontal cortex: inverse relationships during postadolescent brain maturation. J. Neurosci. 2001, 21:8819-8829.
65. Stevens M.C. The developmental cognitive neuroscience of functional connectivity. Brain Cogn. 2009, 70:1-12.
66. Takeshita K., Nagamine T., Thuy D.H., Satow T., Matsuhashi M., Yamamoto J., Takayama M., Fujiwara N., Shibasaki H. Maturational change of parallel auditory processing in school-aged children revealed by simultaneous recording of magnetic and electric cortical responses. Clin. Neurophysiol. 2002, 113:1470-1484.
67. Thatcher R.W. Cyclic cortical reorganization: origins of human cognitive development. Human behavior and the developing brain 1994, 232-266. Guilford Press, New York. G.D.K.W. Fischer (Ed.).
68. Tyvaert L., Hawco C., Kobayashi E., LeVan P., Dubeau F., Gotman J. Different structures involved during ictal and interictal epileptic activity in malformations of cortical development: an EEG-fMRI study. Brain 2008, 131:2042-2060.
69. van den Heuvel M.P., Hulshoff Pol H.E. Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur. Neuropsychopharmacol. 2010, 20:519-534.
70. Viswanathan A., Freeman R.D. Neurometabolic coupling in cerebral cortex reflects synaptic more than spiking activity. Nat. Neurosci. 2007, 10:1308-1312.
71. Wackermann J., Matousek M. From the "EEG age" to a rational scale of brain electric maturation. Electroencephalogr. Clin. Neurophysiol. 1998, 107:415-421.
72. Whitford T.J., Rennie C.J., Grieve S.M., Clark C.R., Gordon E., Williams L.M. Brain maturation in adolescence: concurrent changes in neuroanatomy and neurophysiology. Hum. Brain Mapp. 2007, 28:228-237.
73. Yang L., Liu Z., Rios C., Yuan H., He B. Electrophysiological neuroimaging: cortical correlates of alpha rhythm modulation. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 2009:1934-1936.