The correlation between white-matter microstructure and the complexity of spontaneous brain activity: A difussion tensor imaging-MEG study

NeuroImage

Volumn 57, Issue 4, 2011, Pages 1300-1307

  Fernández, Alberto ^a,b   Ríos Lago, Marcos ^c,d   Abásolo, Daniel ^e   Hornero, Roberto ^e   Álvarez Linera, Juan ^d,f   Paul, Nuria ^a   Maestú, Fernando ^b   Ortiz, Tomás ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b TECHNICAL UNIVERSITY OF MADRID   (Spain)

^c UNIVERSIDAD NACIONAL DE EDUCACIÓN A DISTANCIA   (Spain)

^d Instituto de Salud Carlos III   (Spain)

^e UNIVERSITY OF VALLADOLID   (Spain)

^f HOSPITAL RUBER INTERNACIONAL   (Spain)

Author keywords

Brain oscillations; Complexity; Difussion tensor imaging; Fractional anisotropy; Magentoencephalography

Indexed keywords

ADULT; AGED; ARTICLE; BRAIN FUNCTION; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; ELECTROENCEPHALOGRAM; FEMALE; FRACTIONAL ANISOTROPY; HUMAN; LEMPEL ZIV COMPLEXITY; MAGNETOENCEPHALOGRAPHY; NERVE FIBER; NEUROANATOMY; PARAHIPPOCAMPAL GYRUS; PRIORITY JOURNAL; SCORING SYSTEM; STRUCTURE ACTIVITY RELATION; WHITE MATTER;

AGED; ANISOTROPY; BRAIN; BRAIN MAPPING; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; HUMANS; MAGNETOENCEPHALOGRAPHY; NEURAL PATHWAYS;

EID: 79960262497     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.05.079     Document Type: Article

References (83)

1. Abásolo D., Hornero R., Gómez C., Garcia M., Lopez M. Analysis of EEG background activity in Alzheimer's disease patients with Lempel-Ziv complexity and central tendency measure. Med. Eng. Phys. 2006, 28(4):315-322.
2. Aboitiz F., Montiel J. One hundred million years of interhemispheric communication: the history of the corpus callosum. Braz. J. Med. Biol. Res. 2003, 36(4):409-420.
3. Aboy M., Hornero R., Abásolo D., Alvarez D. Interpretation of the Lempel-Ziv complexity measure in the context of biomedical signal analysis. IEEE Trans. Biomed. Eng. 2006, 53(11):2282-2288.
4. Anokhin A.P., Birbaumer N., Lutzenberger W., Nikolaev A., Vogel F. Age increases brain complexity. Electroencephalogr. Clin. Neurophysiol. 1996, 99(1):63-68.
5. Ashburner J., Friston K.J. Voxel-based morphometry-the methods. NeuroImage 2000, 11:805-821.
6. Babloyantz A. Estimation of correlation dimension from single and multichannel recordings: a critical review. Brain Dynamics 1983, 122-131. Springer, Berlin. E.B.T.H. Basar (Ed.).
7. Babloyantz A. Evidence of chaotic dynamics of brain activity during the sleep cycle. Phys. Lett. (A) 1985, 111:152-156.
8. Barnett L., Buckley C.L., Bullock S. Neural complexity and structural connectivity. Phys. Rev. E Stat. Nonlin. Soft. Matter. Phys. 2009, 79(5 Pt 1):051914.
9. Basser P.J., Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J. Magn. Reson. B 1996, 111(3):209-219.
10. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed. 2002, 15(7-8):435-455.
11. Ben Bashat D., Ben Sira L., Graif M., Pianka P., Hendler T., Cohen Y., Assaf Y. Normal white matter development from infancy to adulthood: comparing diffusion tensor and high b value diffusion weighted MR images. J. Magn. Reson. Imaging 2005, 21(5):503-511.
12. Bhardwaj R.D., Mahmoodabadi S.Z., Otsubo H., Snead O.C., Rutka J.T., Widjaja E. Diffusion tensor tractography detection of functional pathway for the spread of epileptiform activity between temporal lobe and Rolandic region. Childs Nerv. Syst. 2010, 26(2):185-190.
13. Bonifazi P., Goldin M., Picardo M.A., Jorquera I., Cattani A., Bianconi G., Represa A., Ben-Ari Y., Cossart R. GABAergic hub neurons orchestrate synchrony in developing hippocampal networks. Science 2009, 326(5958):1419-1424.
14. Bozzali M., Cercignani M., Sormani M.P., Comi G., Filippi M. Quantification of brain gray matter damage in different MS phenotypes by use of diffusion tensor MR imaging. AJNR Am. J. Neuroradiol. 2002, 23:985-988.
15. Camara E., Bodammer N., Rodriguez-Fornells A., Tempelmann C. Age-related water diffusion changes in human brain: a voxel-based approach. NeuroImage 2007, 34(4):1588-1599.
16. Cantero J.L., Atienza M., Cruz-Vadell A., Suarez-Gonzalez A., Gil-Neciga E. Increased synchronization and decreased neural complexity underlie thalamocortical oscillatory dynamics in mild cognitive impairment. NeuroImage 2009, 46(4):938-948.
17. Cheng Y., Chou K.H., Chen I.Y., Fan Y.T., Decety J., Lin C.P. Atypical development of white matter microstructure in adolescents with autism spectrum disorders. NeuroImage 2010, 50(3):873-882.
18. Chepuri N.B., Yen Y.F., Burdette J.H., Li H., Moody D.M., Maldjian J.A. Diffusion anisotropy in the corpus callosum. AJNR Am. J. Neuroradiol. 2002, 23(5):803-808.
19. Di Virgilio G., Clarke S. Direct interhemispheric visual input to human speech áreas. Hum. Brain Mapp. 1997, 5(5):347-354.
20. Dougherty R.F., Ben-Shachar M., Deutsch G.K., Hernandez A., Fox G.R., Wandell B.A. Temporal-callosal pathway diffusivity predicts phonological skills in children. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(20):8556-8561.
21. Ferenets R., Vanluchene A., Lipping T., Heyse B., Struys M.M. Behavior of entropy/complexity measures of the electroencephalogram during propofol-induced sedation: dose-dependent effects of remifentanil. Anesthesiology 2007, 106(4):696-706.
22. Fernández A., Hornero R., Mayo A., Poza J., Gil-Gregorio P., Ortiz T. MEG spectral profile in Alzheimer's disease and mild cognitive impairment. Clin. Neurophysiol. 2006, 117(2):306-314.
23. Fernández A., Quintero J., Hornero R., Zuluaga P., Navas M., Gómez C., Escudero J., Garcia-Campos N., Biederman J., Ortiz T. Complexity analysis of spontaneous brain activity in attention-deficit/hyperactivity disorder: diagnostic implications. Biol. Psychiatry 2009, 65(7):571-577.
24. Fernández A., Hornero R., Gómez C., Turrero A., Gil-Gregorio P., Matias-Santos J., Ortiz T. Complexity analysis of spontaneous brain activity in Alzheimer disease and mild cognitive impairment: an MEG study. Alzheimer Dis. Assoc. Disord. 2010, 24(2):182-189.
25. Fox M.D., Raichle M.E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 2007, 8:700-711.
26. Friston K.J. Theoretical neurobiology and schizophrenia. Br. Med. Bull. 1996, 52(3):644-655.
27. Friston K.J., Ashburner J., Frith C., Poline J.B., Heather J.D., Frackowiak R.S.J. Spatial registration and normalization of images. Hum. Brain Mapp. 1995, 2:165-189.
28. Gao W., Lin W., Chen Y., Gerig G., Smith J.K., Jewells V., Gilmore J.H. Temporal and spatial development of axonal maturation and myelination of white matter in the developing brain. AJNR Am. J. Neuroradiol. 2009, 30(2):290-296.
29. Genovese C.R., Lazar N.A., Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage 2002, 15:870-878.
30. 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(10):861-863.
31. Gómez C., Hornero R., Abásolo D., Fernández A., López M. Complexity analysis of the magnetoencephalogram background activity in Alzheimer's disease patients. Med. Eng. Phys. 2006, 28(9):851-859.
32. Good C.D., Johnsrude I.S., Ashburner J., Henson R.N., Friston K.J., Frackowiak R.S. Avoxel-based morphometric study of ageing in 465 normal adult human brains. NeuroImage 2001, 14:21-36.
33. Hagmann P., Cammoun L., Gigandet X., Meuli R., Honey C.J., Wedeen V.J., Sporns O. Mapping the structural core of human cerebral cortex. PLoS Biol. 2008, 6(7):e159.
34. Hasan K.M., Sankar A., Halphen C., Kramer L.A., Brandt M.E., Juranek J., Cirino P.T., Fletcher J.M., Papanicolaou A.C., Ewing-Cobbs L. Development and organization of the human brain tissue compartments across the lifespan using diffusion tensor imaging. Neuroreport 2007, 18(16):1735-1739.
35. Hasan K.M., Kamali A., Iftikhar A., Kramer L.A., Papanicolaou A.C., Fletcher J.M., Ewing-Cobbs L. Diffusion tensor tractography quantification of the human corpus callosum fiber pathways across the lifespan. Brain Res. 2009, 1249:91-100.
36. Heylighen F. The Growth of Structural and Functional Complexity during Evolution 1999, 17-44. Kluwer Academic, Dordrecht.
37. Hirono N., Kitagaki H., Kazui H., Hashimoto M., Mori E. Impact of white matter changes on clinical manifestation of Alzheimer's disease: a quantitative study. Stroke 2000, 31:2182-2188.
38. Ho B.C., Andreasen N.C., Nopoulos P., Arndt S., Magnotta V., Flaum M. Progressive structural brain abnormalities and their relationship to clinical outcome: a longitudinal magnetic resonance imaging study early in schizophrenia. Arch. Gen. Psychiatry 2003, 60:585-594.
39. Huang H., Zhang J., Jiang H., Wakana S., Poetscher L., Miller M.I., van Zijl C.M., Hillis A.E., Wytik R., Mori S. DTI tractography based parcellation of white matter: application of the mid-sagittal morphology of corpus callosum. NeuroImage 2005, 26(1):295-305.
40. Huang M., Theilmann R.J., Robb A., Angeles A., Nichols S., Drake A., Dandrea J., Levy M., Holland M., Song T. Integrated imaging approach with MEG and DTI to Detect mild traumatic brain injury in military and civilian patients. J. Neurotrauma 2009, 26(8):1213-1226.
41. Jones D.K., Symms M.R., Cercignani M., Howard R.J. The effect of filter size on VBM analyses of DT-MRI data. NeuroImage 2005, 26(2):546-554.
42. Jones D.K., Catani M., Pierpaoli C., Reeves S.J., Shergill S.S., O'Sullivan M., Golesworthy P., McGuire P., Horsfield M.A., Simmons A., Williams S.C., Howard R.J. Age effects on diffusion tensor magnetic resonance imaging tractography measures of frontal cortex connections in schizophrenia. Hum. Brain Mapp. 2006, 27(3):230-238.
43. Kamada K., Todo T., Masutani Y., Aoki S., Ino K., Morita A., Saito N. Visualization of the frontotemporal language fibers by tractography combined with functional magnetic resonance imaging and magnetoencephalography. J. Neurosurg. 2007, 106(1):90-98.
44. Kolmogorov A.N. Three approaches to the quantitative definition of information. Inf. Trans. 1965, 1:3-11.
45. Koukkou M., Lehmann D., Wackermann J., Dvorak I., Henggeler B. Dimensional complexity of EEG brain mechanisms in untreated schizophrenia. Biol. Psychiatry 1993, 33(6):397-407.
46. Kraus M.F., Susmaras T., Caughlin B.P., Walker C.J., Sweeney J.A., Little D.M. White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain 2007, 130(Pt 10):2508-2519.
47. Le Bihan D., van Zijl P. From the diffusion coefficient to the diffusion tensor. NMR Biomed. 2002, 15:431-434.
48. Lempel A., Ziv J. On the complexity of finite sequences. IEEE Trans. Inf. Theory 1976, 22:75-81.
49. Li Y., Tong S., Liu D., Gai Y., Wang X., Wang J., Qiu Y., Zhu Y. Abnormal EEG complexity in patients with schizophrenia and depression. Clin. Neurophysiol. 2008, 119(6):1232-1241.
50. Lopes da Silva F. Neural mechanisms underlying brain waves: from neural membranes to networks. Electroencephalogr. Clin. Neurophysiol. 1991, 79(2):81-93.
51. Lutzenberger W., Preissl H., Pulvermuller F. Fractal dimension of electroencephalographic time series and underlying brain processes. Biol. Cybern. 1995, 73(5):477-482.
52. Markowithsch H.J. Which brain regions are critically involved in the retrieval of old episodic memory?. Brain Res. Brain Res. Rev. 1995, 21(2):117-127.
53. McLaughlin N.C., Paul R.H., Grieve S.M., Williams L.M., Laidlaw D., DiCarlo M., Clark C.R., Whelihan W., Cohen R.A., Whitford T.J., Gordon E. Diffusion tensor imaging of the corpus callosum: a cross-sectional study across the lifespan. Int. J. Dev. Neurosci. 2007, 25(4):215-221.
54. Meyer-Lindenberg A. The evolution of complexity in human brain development: an EEG study. Electroencephalogr. Clin. Neurophysiol. 1996, 99(5):405-411.
55. Mori S., Wakana S., Nagae-Poetscher L.M., Van Zijl P.C. MRI Atlas of Human White Matter 2005, Elsevier, Amsterdam.
56. Nagarajan R. Quantifying physiological data with Lempel-Ziv complexity-certain issues. IEEE Trans. Biomed. Eng. 2002, 49(11):1371-1373.
57. Oouchi H., Yamada K., Sakai K., Kizu O., Kubota T., Ito H., Nishimura T. Diffusion anisotropy measurement of brain white matter is affected by voxel size: understimation occurs in areas with crossing fibers. AJNR Am. J. Neuroradiol. 2007, 28:1102-1106.
58. Pereda E., Quiroga R.Q., Bhattacharya J. Nonlinear multivariate analysis of neurophysiological signals. Prog. Neurobiol. 2005, 77(1-2):1-37.
59. Pfurtscheller G., Lopes da Silva F.H. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin. Neurophysiol. 1999, 110(11):1842-1857.
60. Radhakrishnan N., Gangadhar B.N. Estimating regularity in epileptic seizure time-series data. A complexity-measure approach. IEEE Eng. Med. Biol. Mag. 1998, 17(3):89-94.
61. Raichle M.E., MacLeod A.M., Snyder A., Powers W.J., Gusnard D.A., Shulman G.L. A default mode of brain function. Proc. Natl. Acad. Sci. 2001, 98:676-682.
62. Roberts T.P., Khan S.Y., Blaskey L., Dell J., Levy S.E., Zarnow D.M., Edgar J.C. Developmental correlation of diffusion anisotropy with auditory-evoked response. Neuroreport 2009, 20(18):1586-1591.
63. Robinson P.A., Rennie C.J., Wright J.J., Bahramali H., Gordon E., Rowe D.L. Prediction of electroencephalographic spectra from neurophysiology. Phys. Rev. E Stat. Nonlin. Soft. Matter. Phys. 2001, 63(2 Pt 1):021903.
64. Salat D.H., Tuch D.S., Greve D.N., van der Kouwe A.J., Hevelone N.D., Zaleta A.K., Rosen B.R., Fischl B., Corkin S., Rosas H.D., Dale A.M. Age-related alterations in white matter microstructure measured by diffusion tensor imaging. Neurobiol. Aging 2005, 26:1215-1227.
65. Schmahmann J., Pandya D. Fiber Pathways of the Brain 2006, Oxford University Press, Oxford.
66. Segalowitz S.J., Santesso D.L., Jetha M.K. Electrophysiological changes during adolescence: a review. Brain Cogn. 2010, 72(1):86-100.
67. Shaw P., Eckstrand K., Sharp W., Blumenthal J., Lerch J.P., Greenstein D., Clasen L., Evans A., Giedd J., Rapoport J.L. Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation. Proc. Natl. Acad. Sci. 2007, 104(49):19649-19654.
68. Shimony J.S., McKinstry R.C., Akbudak E., Aronovitz J.A., Snyder A.Z., Lori N.F., Cull T.S., Conturo T.E. Quantitative diffusion-tensor anisotropy brain MR imaging: normative human data and anatomic analysis. Radiology 1999, 212(3):770-784.
69. Sowell E.R., Thompson P.M., Holmes C.J., Batth R., Jernigan T.L., Toga A.W. Localizing age-related changes in brain structure between childhood and adolescence using statistical parametric mapping. NeuroImage 1999, 9(6 Pt 1):587-597.
70. Sporns O., Tononi G., Edelman G.M. Connectivity and complexity: the relationship between neuroanatomy and brain dynamics. Neural Netw. 2000, 13(8-9):909-922.
71. Stam C.J. Nonlinear dynamical analysis of EEG and MEG: review of an emerging field. Clin. Neurophysiol. 2005, 116(10):2266-2301.
72. Stam C.J., Jones B.F., Nolte G., Breakspear M., Scheltens P. Small-world networks and functional connectivity in Alzheimer's disease. Cereb. Cortex 2007, 17:92-99.
73. Steen R.G., Ogg R.J., Reddick W.E., Kingsley P.B. Age-related changes in the pediatric brain: quantitative MR evidence of maturational changes during adolescence. AJNR Am. J. Neuroradiol. 1997, 18(5):819-828.
74. Stufflebeam S.M., Witzel T., Mikulski S., Hamalainen M.S., Temereanca S., Barton J.J., Tuch D.S., Manoach D.S. A non-invasive method to relate the timing of neural activity to white matter microstructural integrity. NeuroImage 2008, 42(2):710-716.
75. Tononi G., Sporns O., Edelman G.M. A measure for brain complexity: relating functional segregation and integration in the nervous system. Proc. Natl. Acad. Sci. U. S. A. 1994, 91(11):5033-5037.
76. Tononi G., Edelman G.M., Sporns O. Complexity and coherency: integrating information in the brain. Trends Cogn. Sci. 1998, 2(12):474-484.
77. Wakana S., Jiang H., Nagae-Poetscher L.M., van Zijl P.C., Mori S. Fiber tract-based atlas of human white matter anatomy. Radiology 2004, 230(1):77-87.
78. 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(3):228-237.
79. Widjaja E., Zarei Mahmoodabadi S., Otsubo H., Snead O.C., Holowka S., Bells S., Raybaud C. Subcortical alterations in tissue microstructure adjacent to focal cortical dysplasia: detection at diffusion-tensor MR imaging by using magnetoencephalographic dipole cluster localization. Radiology 2009, 251(1):206-215.
80. Widjaja E., Simao G., Mahmoodabadi S.Z., Ochi A., Snead O.C., Rutka J., Otsubo H. Diffusion tensor imaging identifies changes in normal-appearing white matter within the epileptogenic zone in tuberous sclerosis complex. Epilepsy Res. 2010, 89(2-3):246-253.
81. Yan R., Gao R.X. Complexity as a measure for machine health evaluation. IEEE Trans. Instrum. Meas. 2004, 53(4):1327-1334.
82. Zarei M., Johansen-Berg H., Smith S., Ciccarelli O., Thompson A.J., Matthews P.M. Functional anatomy of interhemispheric cortical connections in the human brain. J. Anat. 2006, 209(3):311-320.
83. Zhang X.S., Roy R.J., Jensen E.W. EEG complexity as a measure of depth of anesthesia for patients. IEEE Trans. Biomed. Eng. 2001, 48(12):1424-1433.