Multimodal fMRI resting-state functional connectivity in Granulin mutations: The case of fronto-parietal dementia

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Premi, Enrico ^a   Cauda, Franco ^b,c   Gasparotti, Roberto ^a   Diano, Matteo ^b,c   Archetti, Silvana ^d   Padovani, Alessandro ^a   Borroni, Barbara ^a  

^a UNIVERSITY OF BRESCIA   (Italy)

^b Koelliker Hospital   (Italy)

^c UNIVERSITY OF TURIN   (Italy)

^d Department of Paediatrics   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGE; ARTICLE; BRAIN ATROPHY; CLINICAL ARTICLE; CONNECTOME; CONTROLLED STUDY; DEGREE CENTRALITY; FEMALE; FRACTIONAL AMPLITUDE OF LOW FREQUENCY FLUCTUATION; FRONTAL LOBE; FRONTOTEMPORAL DEMENTIA; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENDER; GENE; GENE MUTATION; GENETIC CORRELATION; GRAY MATTER; GRN GENE; HETEROZYGOTE; HUMAN; INFERIOR PARIETAL LOBULE; MALE; NERVOUS SYSTEM PARAMETERS; NUCLEAR MAGNETIC RESONANCE SCANNER; ORBITAL CORTEX; POSTERIOR CINGULATE; REGIONAL HOMOGENEITY; RESTING STATE FUNCTIONAL MAGNETIC RESONANCE IMAGING; AGED; BRAIN; GENETICS; METABOLISM; MIDDLE AGED; MUTATION; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PROCEDURES;

GRANULIN PRECURSOR PROTEIN; SIGNAL PEPTIDE;

AGED; BRAIN; FEMALE; FRONTOTEMPORAL DEMENTIA; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MUTATION;

EID: 84907048314     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0106500     Document Type: Article

References (75)

1. McKhann GM, Albert MS, Grossman M, Miller B, Dickson D, et al. (2001) Clinical and pathological diagnosis of frontotemporal dementia: report of the Work Group on Frontotemporal Dementia and Pick's Disease. Arch Neurol 58: 1803-1809.
2. Neary D, Snowden JS, Gustafson L, Passant U, Stuss D, et al. (1998) Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology 51: 1546-1554.
3. Rascovsky K, Hodges JR, Knopman D, Mendez MF, Kramer JH, et al. (2011) Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain 134: 2456-2477.
4. Gorno-Tempini ML, Hillis AE, Weintraub S, Kertesz A, Mendez M, et al. (2011) Classification of primary progressive aphasia and its variants. Neurology 76: 1006-1014.
5. Pereira JM, Williams GB, Acosta-Cabronero J, Pengas G, Spillantini MG, et al. (2009) Atrophy patterns in histologic vs clinical groupings of frontotemporal lobar degeneration. Neurology 72: 1653-1660.
6. Rohrer JD, Warren JD, Modat M, Ridgway GR, Douiri A, et al. (2009) Patterns of cortical thinning in the language variants of frontotemporal lobar degeneration. Neurology 72: 1562-1569.
7. Whitwell JL, Josephs KA, Rossor MN, Stevens JM, Revesz T, et al. (2005) Magnetic resonance imaging signatures of tissue pathology in frontotemporal dementia. Arch Neurol 62: 1402-1408.
8. Mackenzie IR, Neumann M, Bigio EH, Cairns NJ, Alafuzoff I, et al. (2010) Nomenclature and nosology for neuropathologic subtypes of frontotemporal lobar degeneration: an update. Acta Neuropathol 119: 1-4.
9. Rohrer JD, Lashley T, Schott JM, Warren JE, Mead S, et al. (2011) Clinical and neuroanatomical signatures of tissue pathology in frontotemporal lobar degeneration. Brain 134: 2565-2581.
10. Rademakers R, Neumann M, Mackenzie IR (2012) Advances in understanding the molecular basis of frontotemporal dementia. Nat Rev Neurol 8: 423-434.
11. Whitwell JL, Jack CR Jr, Baker M, Rademakers R, Adamson J, et al. (2007) Voxel-based morphometry in frontotemporal lobar degeneration with ubiquitin-positive inclusions with and without progranulin mutations. Arch Neurol 64: 371-376.
12. Whitwell JL, Jack CR Jr, Boeve BF, Senjem ML, Baker M, et al. (2009) Voxelbased morphometry patterns of atrophy in FTLD with mutations in MAPT or PGRN. Neurology 72: 813-820.
13. Borroni B, Alberici A, Premi E, Archetti S, Garibotto V, et al. (2008) Brain magnetic resonance imaging structural changes in a pedigree of asymptomatic progranulin mutation carriers. Rejuvenation Res 11: 585-595.
14. Borroni B, Alberici A, Cercignani M, Premi E, Serra L, et al. (2012) Granulin mutation drives brain damage and reorganization from preclinical to symptomatic FTLD. Neurobiol Aging 33: 2506-2520.
15. Premi E, Grassi M, Gazzina S, Paghera B, Pepe D, et al. (2013) The neuroimaging signature of frontotemporal lobar degeneration associated with Granulin mutations: an effective connectivity study. J Nucl Med 54: 1066-1071.
16. Premi E, Formenti A, Gazzina S, Archetti S, Gasparotti R, et al. (2013) Effect of TMEM106B Polymorphism on Functional Network Connectivity in Asymptomatic GRN Mutation Carriers. JAMA Neurol.
17. Dopper EG, Rombouts SA, Jiskoot LC, Heijer T, de Graaf JR, et al. (2013) Structural and functional brain connectivity in presymptomatic familial frontotemporal dementia. Neurology 80: 814-823.
18. Pievani M, Paternico D, Benussi L, Binetti G, Orlandini A, et al. (2014) Pattern of structural and functional brain abnormalities in asymptomatic granulin mutation carriers. Alzheimers Dement.
19. Jacova C, Hsiung GY, Tawankanjanachot I, Dinelle K, McCormick S, et al. (2013) Anterior brain glucose hypometabolism predates dementia in progranulin mutation carriers. Neurology 81: 1322-1331.
20. Baker M, Mackenzie IR, Pickering-Brown SM, Gass J, Rademakers R, et al. (2006) Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17. Nature 442: 916-919.
21. Cruts M, Gijselinck I, van der Zee J, Engelborghs S, Wils H, et al. (2006) Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature 442: 920-924.
22. Tang W, Lu Y, Tian QY, Zhang Y, Guo FJ, et al. (2011) The growth factor progranulin binds to TNF receptors and is therapeutic against inflammatory arthritis in mice. Science 332: 478-484.
23. Toh H, Chitramuthu BP, Bennett HP, Bateman A (2011) Structure, function, and mechanism of progranulin; the brain and beyond. J Mol Neurosci 45: 538 548.
24. Van Damme P, Van Hoecke A, Lambrechts D, Vanacker P, Bogaert E, et al. (2008) Progranulin functions as a neurotrophic factor to regulate neurite outgrowth and enhance neuronal survival. J Cell Biol 181: 37-41.
25. Zang Y, Jiang T, Lu Y, He Y, Tian L (2004) Regional homogeneity approach to fMRI data analysis. Neuroimage 22: 394-400.
26. Kendall MG GJ (1990) Rank Correlation Methods. USA. 272 p.
27. He Y, Wang L, Zang Y, Tian L, Zhang X, et al. (2007) Regional coherence changes in the early stages of Alzheimer's disease: a combined structural and resting-state functional MRI study. Neuroimage 35: 488-500.
28. Zhang Z, Liu Y, Jiang T, Zhou B, An N, et al. (2012) Altered spontaneous activity in Alzheimer's disease and mild cognitive impairment revealed by Regional Homogeneity. Neuroimage 59: 1429-1440.
29. Long XY, Zuo XN, Kiviniemi V, Yang Y, Zou QH, et al. (2008) Default mode network as revealed with multiple methods for resting-state functional MRI analysis. J Neurosci Methods 171: 349-355.
30. Zou QH, Zhu CZ, Yang Y, Zuo XN, Long XY, et al. (2008) An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF. J Neurosci Methods 172: 137-141.
31. Di X, Kim EH, Huang CC, Tsai SJ, Lin CP, et al. (2013) The influence of the amplitude of low-frequency fluctuations on resting-state functional connectivity. Front Hum Neurosci 7: 118.
32. Wang J, Zuo X, He Y (2010) Graph-based network analysis of resting-state functional MRI. Front Syst Neurosci 4: 16.
33. Zuo XN, Ehmke R, Mennes M, Imperati D, Castellanos FX, et al. (2012) Network centrality in the human functional connectome. Cereb Cortex 22: 1862-1875.
34. Zuo XN, Di Martino A, Kelly C, Shehzad ZE, Gee DG, et al. (2010) The oscillating brain: complex and reliable. Neuroimage 49: 1432-1445.
35. Mesmoudi S, Perlbarg V, Rudrauf D, Messe A, Pinsard B, et al. (2013) Resting state networks' corticotopy: the dual intertwined rings architecture. PLoS One 8: e67444.
36. van den Heuvel MP, Sporns O (2013) An anatomical substrate for integration among functional networks in human cortex. J Neurosci 33: 14489-14500.
37. Mesulam MM (1998) From sensation to cognition. Brain 121 (Pt 6): 1013-1052.
38. Song J, Qin W, Liu Y, Duan Y, Liu J, et al. (2013) Aberrant functional organization within and between resting-state networks in AD. PLoS One 8: e63727.
39. Borroni B, Agosti C, Premi E, Cerini C, Cosseddu M, et al. (2010) The FTLD-modified Clinical Dementia Rating scale is a reliable tool for defining disease severity in frontotemporal lobar degeneration: evidence from a brain SPECT study. Eur J Neurol 17: 703-707.
40. Borroni B, Archetti S, Alberici A, Agosti C, Gennarelli M, et al. (2008) Progranulin genetic variations in frontotemporal lobar degeneration: evidence for low mutation frequency in an Italian clinical series. Neurogenetics 9: 197-205.
41. Song XW, Dong ZY, Long XY, Li SF, Zuo XN, et al. (2011) REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One 6: e25031.
42. Ashburner J, Friston KJ (2005) Unified segmentation. Neuroimage 26: 839-851.
43. Ashburner J, Friston KJ (2001) Why voxel-based morphometry should be used. Neuroimage 14: 1238-1243.
44. Friston KJ, Williams S, Howard R, Frackowiak RS, Turner R (1996) Movement-related effects in fMRI time-series. Magn Reson Med 35: 346-355.
45. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59: 2142-2154.
46. Zuo XN, Xu T, Jiang L, Yang Z, Cao XY, et al. (2013) Toward reliable characterization of functional homogeneity in the human brain: preprocessing, scan duration, imaging resolution and computational space. Neuroimage 65: 374-386.
47. Tian L, Ren J, Zang Y (2012) Regional homogeneity of resting state fMRI signals predicts Stop signal task performance. Neuroimage 60: 539-544.
48. Turner JA, Damaraju E, van Erp TG, Mathalon DH, Ford JM, et al. (2013) A multi-site resting state fMRI study on the amplitude of low frequency fluctuations in schizophrenia. Front Neurosci 7: 137.
49. Buckner RL, Sepulcre J, Talukdar T, Krienen FM, Liu H, et al. (2009) Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. J Neurosci 29: 1860-1873.
50. Oakes TR, Fox AS, Johnstone T, Chung MK, Kalin N, et al. (2007) Integrating VBM into the General Linear Model with voxelwise anatomical covariates. Neuroimage 34: 500-508.
51. Filippi M, Valsasina P, Misci P, Falini A, Comi G, et al. (2013) 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 34: 1330-1343.
52. Wang Z, Yan C, Zhao C, Qi Z, Zhou W, et al. (2011) Spatial patterns of intrinsic brain activity in mild cognitive impairment and Alzheimer's disease: a resting-state functional MRI study. Hum Brain Mapp 32: 1720-1740.
53. Yang X, Beason-Held L, Resnick SM, Landman BA (2011) Biological parametric mapping with robust and non-parametric statistics. Neuroimage 57: 423-430.
54. Farb NA, Grady CL, Strother S, Tang-Wai DF, Masellis M, et al. (2013) Abnormal network connectivity in frontotemporal dementia: evidence for prefrontal isolation. Cortex 49: 1856-1873.
55. Casanova R, Srikanth R, Baer A, Laurienti PJ, Burdette JH, et al. (2007) Biological parametric mapping: A statistical toolbox for multimodality brain image analysis. Neuroimage 34: 137-143.
56. Smieskova R, Allen P, Simon A, Aston J, Bendfeldt K, et al. (2012) Different duration of at-risk mental state associated with neurofunctional abnormalities. A multimodal imaging study. Hum Brain Mapp 33: 2281-2294.
57. Hayasaka S, Phan KL, Liberzon I, Worsley KJ, Nichols TE (2004) Nonstationary cluster-size inference with random field and permutation methods. Neuroimage 22: 676-687.
58. Petersson KM, Nichols TE, Poline JB, Holmes AP (1999) Statistical limitations in functional neuroimaging. II. Signal detection and statistical inference. Philos Trans R Soc Lond B Biol Sci 354: 1261-1281.
59. Poldrack RA, Fletcher PC, Henson RN, Worsley KJ, Brett M, et al. (2008) Guidelines for reporting an fMRI study. Neuroimage 40: 409-414.
60. Onoda K, Ishihara M, Yamaguchi S (2012) Decreased functional connectivity by aging is associated with cognitive decline. J Cogn Neurosci 24: 2186-2198.
61. Mowinckel AM, Espeseth T, Westlye LT (2012) Network-specific effects of age and in-scanner subject motion: a resting-state fMRI study of 238 healthy adults. Neuroimage 63: 1364-1373.
62. Mevel K, Landeau B, Fouquet M, La Joie R, Villain N, et al. (2013) Age effect on the default mode network, inner thoughts, and cognitive abilities. Neurobiol Aging 34: 1292-1301.
63. Garibotto V, Borroni B, Kalbe E, Herholz K, Salmon E, et al. (2008) Education and occupation as proxies for reserve in aMCI converters and AD: FDG-PET evidence. Neurology 71: 1342-1349.
64. Chow TW, Alobaidy AA (2013) Incorporating new diagnostic schemas, genetics, and proteinopathy into the evaluation of frontotemporal degeneration. Continuum (Minneap Minn) 19: 438-456.
65. Chhatwal JP, Schultz AP, Johnson K, Benzinger TL, Jack C, Jr., et al. (2013) Impaired default network functional connectivity in autosomal dominant Alzheimer disease. Neurology 81: 736-744.
66. Warren JD, Rohrer JD, Hardy J (2012) Disintegrating brain networks: from syndromes to molecular nexopathies. Neuron 73: 1060-1062.
67. Sieben A, Van Langenhove T, Engelborghs S, Martin JJ, Boon P, et al. (2012) The genetics and neuropathology of frontotemporal lobar degeneration. Acta Neuropathol 124: 353-372.
68. Moreno F, Sala-Llonch R, Barandiaran M, Sanchez-Valle R, Estanga A, et al. (2013) Distinctive age-related temporal cortical thinning in asymptomatic granulin gene mutation carriers. Neurobiol Aging 34: 1462-1468.
69. Rytty R, Nikkinen J, Paavola L, Abou Elseoud A, Moilanen V, et al. (2013) GroupICA dual regression analysis of resting state networks in a behavioral variant of frontotemporal dementia. Front Hum Neurosci 7: 461.
70. Zhou J, Greicius MD, Gennatas ED, Growdon ME, Jang JY, et al. (2010) Divergent network connectivity changes in behavioural variant frontotemporal dementia and Alzheimer's disease. Brain 133: 1352-1367.
71. Maximo JO, Keown CL, Nair A, Muller RA (2013) Approaches to local connectivity in autism using resting state functional connectivity MRI. Front Hum Neurosci 7: 605.
72. Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304: 1926-1929.
73. Deco G, Jirsa VK, McIntosh AR (2011) Emerging concepts for the dynamical organization of resting-state activity in the brain. Nat Rev Neurosci 12: 43-56.
74. Cabral J, Hugues E, Sporns O, Deco G (2011) Role of local network oscillations in resting-state functional connectivity. Neuroimage 57: 130-139.
75. Warren JD, Rohrer JD, Schott JM, Fox NC, Hardy J, et al. (2013) Molecular nexopathies: a new paradigm of neurodegenerative disease. Trends Neurosci 36: 561-569.