Sex differences in resting-state functional connectivity in multiple sclerosis

American Journal of Neuroradiology

Volumn 34, Issue 12, 2013, Pages 2304-2311

  Koenig, Katherine A ^a   Lowe, M J ^a   Lin, J ^a   Sakaie, K E ^a   Stone, L ^a   Bermel, R A ^a   Beall, E B ^a   Rao, S M ^a   Trapp, B D ^a   Phillips, M D ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANTERIOR CINGULATE; ARTICLE; BEHAVIOR; BOLD SIGNAL; CAUDATE NUCLEUS; CLINICAL ARTICLE; CONNECTOME; CONTROLLED STUDY; DEFAULT MODE NETWORK; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; MIDDLE FRONTAL GYRUS; MULTIPLE SCLEROSIS; NUCLEAR MAGNETIC RESONANCE SCANNER; POSTERIOR CINGULATE; PREFRONTAL CORTEX; PUTAMEN; RESTING STATE FUNCTIONAL CONNECTIVITY MAGNETIC RESONANCE IMAGING; SEX DIFFERENCE; TEMPORAL GYRUS; VOLUMETRY;

ADULT; BRAIN; BRAIN MAPPING; CONNECTOME; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MULTIPLE SCLEROSIS; NERVE NET; NEURAL PATHWAYS; REST; SEX FACTORS;

EID: 84890490869     PISSN: 01956108     EISSN: 1936959X     Source Type: Journal    
DOI: 10.3174/ajnr.A3630     Document Type: Article

References (66)

1. Debouverie M, Pittion-Vouyovitch S, Louis S, et al. Increasing incidence of multiple sclerosis among women in Lorraine, Eastern France. Mult Scler 2007;13:962-67
2. Celius E, Vandvik B. Multiple sclerosis in Oslo, Norway: prevalence on 1 January 1995 and incidence over a 25-year period. Eur J Neurol 2001;8:463-69
3. Orton S, Herrera B, Yee I, et al. Sex ratio of multiple sclerosis in Canada: a longitudinal study. Lancet Neurol 2006;5:932-36
4. Bove R, Healy B, Augustine A, et al. Effect of gender on late-onset multiple sclerosis. Mult Scler 2012;18:1472-79
5. Khaleeli Z, Ciccarelli O, Manfredonia F, et al. Predicting progression in primary progressive multiple sclerosis: a 10-year multicenter study. Ann Neurol 2008;63:790-93
6. Runmarker B, Andersen O. Prognostic factors in a multiple sclerosis incidence cohort with twenty-five years of follow-up. Brain 1993;116:117-34
7. Koutsis G, Evangelopoulos M, Andreadou E, et al. The onset of multiple sclerosis in Greece: a single-center study of 1,034 consecutive patients. Eur Neurol 2010;63:350-56
8. Menon R, Di Dario M, Cordiglieri C, et al. Gender-based blood transcriptomes and interactomes in multiple sclerosis: involvement of SP1 dependent gene transcription. J Autoimmun 2012;38:J144-55
9. Zoccolella S, Tortorella C, Iaffaldano P, et al. Low serum urate levels are associated to female gender in multiple sclerosis patients. PLoS One 2012;7:e40608
10. Greer JM, Csurhes PA, Pender MP, et al. Effect of gender on T-cell proliferative responses to myelin proteolipid protein antigens in patients with multiple sclerosis and controls. J Autoimmun 2004;22:345-52
11. D'hooghe MB, Haentjens P, Nagels G, et al. Menarche, oral contraceptives, pregnancy and progression of disability in relapsing onset and progressive onset multiple sclerosis. J Neurol 2012;259:855-61
12. Kipp M, Amor S, Krauth R, et al. Multiple sclerosis: neuroprotective alliance of estrogen-progesterone and gender. Front Neuroendocrinol 2012;33:1-16
13. Tomassinia V, Pozzilli C. Sex hormones, brain damage and clinical course of multiple sclerosis. J Neurol Sci 2009;286:35-39
14. Sicotte NL, Liva SM, Klutch R, et al. Treatment of multiple sclerosis with the pregnancy hormone estriol. Ann Neurol 2002;52:421-28
15. Ziehn M, Avedisian A, Dervin S, et al. Estriol preserves synaptic transmission in the hippocampus during autoimmune demyelinating disease. Lab Invest 2012;92:1234-45
16. Fazekas F, Enzinger C, Wallner-Blazek M, et al. Gender differences in MRI studies on multiple sclerosis. J Neurol Sci 2009;286:28-30
17. Antulov R, Weinstock-Guttman B, Cox J, et al. Gender-related differences in MS: a study of conventional and nonconventional MRI measures. Mult Scler 2009;15:345-54
18. Li D, Zhao G, Paty D, et al. Randomized controlled trial of interfer-on-beta-1a in secondary progressive MS: MRI results. Neurology 2001;56:1505-13
19. Riccitelli G, Rocca M, Pagani E, et al. Mapping regional grey and white matter atrophy in relapsing-remitting multiple sclerosis. Mult Scler 2012;18:1027-37
20. Massella A, D'Intino G, Fernández M, et al. Gender effect on neurodegeneration and myelin markers in an animal model for multiple sclerosis. BMC Neurosci 2012;13:1-14
21. Biswal B, Yetkin FZ, Haughton VM, et al. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 1995;34:537-41
22. Faivre A, Rico A, Zaaraoui W, et al. Assessing brain connectivity at rest is clinically relevant in early multiple sclerosis. Mult Scler 2012;18:1251-58
23. Bonavita S, Gallo A, Sacco R, et al. Distributed changes in default-mode resting-state connectivity in multiple sclerosis. Mult Scler 2011;17:411-22
24. Parisi L, Rocca M, Valsasina P, et al. Cognitive rehabilitation correlates with the functional connectivity of the anterior cingulate cortex in patients with multiple sclerosis. Brain Imaging Behav 2012 Apr 19 [Epub ahead of print]
25. Schoonheim M, Geurts J, Landi D, et al. Functional connectivity changes in multiple sclerosis patients: a graph analytical study of MEG resting state data. Hum Brain Mapp 2013;34:52-61
26. Rocca M, Valsasina P, Absinta M, et al. Default-mode network dysfunction and cognitive impairment in progressive MS. Neurology 2010;74:1252-59
27. Hawellek D, Hipp J, Lewis C, et al. Increased functional connectivity indicates the severity of cognitive impairment in multiple sclerosis. Proc Natl Acad Sci U S A 2011;108:19066-71
28. Segall J, Allen E, Jung R, et al. Correspondence between structure and function in the human brain at rest. Front Neuroinform 2012;6:1-17
29. Allen E, Erhardt E, Damaraju E, et al. A baseline for the multivariate comparison of resting-state networks. Front Syst Neurosci 2011;5:1-23
30. Filippi M, Valsasina P, Misci P, et al. The organization of intrinsic brain activity differs between genders: a resting-state fMRI study in a large cohort of young healthy subjects. Hum Brain Mapp 2013;34:1330-43
31. Tian L, Wang J, Yan C, et al. Hemisphere- and gender-related differences in small-world brain networks: a resting-state functional MRI study. Neuroimage 2011;54:191-202
32. Biswal B, Mennes M, Zuo X, et al. Toward discovery science of human brain function. Proc Natl Acad Sci U S A 2010;107:4734-39
33. Liu H, Stufflebeam S, Sepulcre J, et al. Evidence from intrinsic activity that asymmetry of the human brain is controlled by multiple factors. Proc Natl Acad Sci U S A 2009;106:20499-503
34. Schoonheim M, Hulst H, Landi D, et al. Gender-related differences in functional connectivity in multiple sclerosis. Mult Scler 2012;18:164-73
35. Raichle M, MacLeod A, Snyder A, et al. A default mode of brain function. Proc Natl Acad Sci U S A 2001;98:676-82
36. Anticevic A, Cole M, Murray J, et al. The role of default network deactivation in cognition and disease. Trends Cogn Sci 2012;16:584-92
37. Rocca M, Valsasina P, Martinelli V, et al. Large-scale neuronal network dysfunction in relapsing-remitting multiple sclerosis. Neurology 2012;79:1449-57
38. McDonald W, Compston A, Edan G, et al. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the Diagnosis of Multiple Sclerosis. Ann Neurol 2001;50:121-27
39. Glover G, Li T, Ress D. Image-Based Method for Retrospective Correction of Physiological Motion Effects in fMRI: RETROICOR. Magn Reson Med 2000;44:162-67
40. Cox R. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 1996;29:162-73
41. Smith SM, Zhang Y, Jenkinson M, et al. Accurate, robust and automated longitudinal and cross-sectional brain change analysis. NeuroImage 2002;17:479-89
42. Smith SM, Jenkinson M, Woolrich MW, et al. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 2004;23:208-19
43. Jenkinson M, Smith SM. A global optimisation method for robust affine registration of brain images. Med Image Anal 2001;5:143-56
44. Jenkinson M, Bannister PR, Brady JM, et al. Improved optimisation for the robust and accurate linear registration and motion correction of brain images. NeuroImage 2002;17:825-41
45. Zhang Y, Brady M, Smith M. Segmentation of brain MR images through a hidden Markov random field model and the expectation maximization algorithm. IEEE Trans Med Imaging 2001;20:45-57
46. MATLAB. Version 7.4.0 (R2007a). Natick, Massachusetts: The Math-Works Inc; 2007
47. Cox R, Saad Z. Surfing the connectome: InstaCorr in AFNI and SUMA. Second Biennial International Conference on Resting-State Functional Brain Connectivity. Milwaukee, Wisconsin; September 16-19, 2010
48. Saad Z, Glen D, Chen G, et al. A new method for improving functional-to-structural alignment using local Pearson correlation. NeuroImage 2009;44:839-48
49. Beall E, Lowe M. Isolating physiologic noise sources with independently determined spatial measures. NeuroImage 2007;37:1286-300
50. Lowe M, Mock B, Sorenson J. Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. NeuroImage 1998;7:119-32
51. Kurtzke J. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 1983;33:1444-52
52. Delis D, Kramer J, Kaplan E, et al. California Verbal Learning Test-Second Edition. San Antonio, Texas: Psychological Corporation; 2000
53. Benedict R. Brief Visuospatial Memory Test-Revised Professional Manual. Odessa, Florida: Psychological Assessment Resources; 1997
54. Smith A. Symbol Digit Modalities Test: Manual. Los Angeles: Western Psychological Services; 1982
55. Tombaugh T, Kozak J, Rees L. Normative data stratified by age and education for two measures of verbal fluency: FAS and animal naming. Arch Clin Neuropsychol 1999;14:167-77
56. Rao S. A Manual for the Brief, Repeatable Battery of Neuropsychological Tests in Multiple Sclerosis. Milwaukee: Medical College of Wisconsin; 1990
57. Fischl B, Salat D, Busa E, et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002;33:341-55
58. Fischl B, Salat D, van der Kouwe A, et al. Sequence-independent segmentation of magnetic resonance images. NeuroImage 2004;23: S69-84
59. Bermel R, Innus M, Tjoa C, et al. Selective caudate atrophy in multiple sclerosis: a 3D MRI parcellation study. NeuroReport 2003;14: 335-39
60. Nocentini U, Bozzali M, Spanò B, et al. Exploration of the relationships between regional grey matter atrophy and cognition in multiple sclerosis. Brain Imaging Behav 2012 May 15 [Epub ahead of print]
61. Morgen K, Sammer G, Courtney S, et al. Distinct mechanisms of altered brain activation in patients with multiple sclerosis. Neuro-Image 2007;37:937-46
62. Tekok-Kilic A, Benedict R, Weinstock-Guttman B, et al. Independent contributions of cortical gray matter atrophy and ventricle enlargement for predicting neuropsychological impairment in multiple sclerosis. NeuroImage 2007;36:1294-300
63. Gur R, Turetsky B, Matsui M, et al. Sex differences in brain gray and white matter in healthy young adults: correlations with cognitive performance. J Neurosci 1999;19:4065-72
64. Allen J, Damasio H, Grabowski T, et al. Sexual dimorphism and asymmetries in the gray-white composition of the human cerebrum. NeuroImage 2003;18:880-94
65. Grassiot B, Desgranges B, Eustache F, et al. Quantification and clinical relevance of brain atrophy in multiple sclerosis: a review. J Neurol 2009;256:1397-412
66. Sanfilipo M, Benedict R, Sharma J, et al. The relationship between whole brain volume and disability in multiple sclerosis: a comparison of normalized gray vs white matter with misclassification correction. NeuroImage 2005;26:1068-77