Functional overlap and divergence between ALS and bvFTD

Neurobiology of Aging

Volumn 36, Issue 1, 2015, Pages 413-423

  Trojsi, Francesca ^a   Esposito, Fabrizio ^a,b   de Stefano, Manuela ^a   Buonanno, Daniela ^a   Conforti, Francesca L ^c   Corbo, Daniele ^a,d   Piccirillo, Giovanni ^a   Cirillo, Mario ^a   Monsurrò, Maria Rosaria ^a   Montella, Patrizia ^a   Tedeschi, Gioacchino ^a  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b UNIVERSITY OF SALERNO   (Italy)

^c INSTITUTE OF NEUROLOGICAL SCIENCES   (Italy)

^d Neurological Institute for Diagnosis and Care Hermitage Capodimonte   (Italy)

Author keywords

Amyotrophic lateral sclerosis; Behavioral variant frontotemporal dementia; Connectivity; Pathologic continuum; RS fMRI

Indexed keywords

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DEFAULT MODE NETWORK; DISEASE COURSE; EXECUTIVE NETWORK; FEMALE; FRONTAL VARIANT FRONTOTEMPORAL DEMENTIA; FRONTOPARIETAL CORTEX; FUNCTIONAL ASSESSMENT; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENE EXPRESSION; HUMAN; MALE; NERVE DEGENERATION; NEUROANATOMY; NUCLEAR MAGNETIC RESONANCE SCANNER; PARIETAL CORTEX; PHENOTYPE; POSTERIOR CINGULATE; RESTING STATE NETWORK; SALIENCE NETWORK; SENSORIMOTOR CORTEX; BRAIN; COMPARATIVE STUDY; FRONTOTEMPORAL DEMENTIA; GENETICS; MIDDLE AGED; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY;

AGED; AMYOTROPHIC LATERAL SCLEROSIS; BRAIN; FEMALE; FRONTOTEMPORAL DEMENTIA; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NERVE NET;

EID: 84920603106     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.06.025     Document Type: Article

References (67)

1. Agosta F., Canu E., Valsasina P., Riva N., Prelle A., Comi G., Filippi M. Divergent brain network connectivity in amyotrophic lateral sclerosis. Neurobiol. Aging 2013, 34:419-427.
2. Ashburner J. Afast diffeomorphic image registration algorithm. Neuroimage 2007, 38:95-113.
3. Benajiba L., Le Ber I., Camuzat A., Lacoste M., Thomas-Anterion C., Couratier P., Legallic S., Salachas F., Hannequin D., Decousus M., Lacomblez L., Guedj E., Golfier V., Camu W., Dubois B., Campion D., Meininger V., Brice A. TARDBP mutations in motoneuron disease with frontotemporal lobar degeneration. Ann. Neurol. 2009, 65:470-473. French Clinical and Genetic Research Network on Frontotemporal Lobar Degeneration/Frontotemporal Lobar Degeneration with Motoneuron Disease.
4. Biswal B., Yetkin F.Z., Haughton V.M., Hyde J.S. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 1995, 34:537-541.
5. Blair I.P., Williams K.L., Warraich S.T., Durnall J.C., Thoeng A.D., Manavis J., Blumbergs P.C., Vucic S., Kiernan M.C., Nicholson G.A. FUS mutations in amyotrophic lateral sclerosis: clinical, pathological, neurophysiological and genetic analysis. J. Neurol. Neurosurg. Psychiatry 2010, 81:639-645.
6. Borroni B., Brambati S.M., Agosti C., Gipponi S., Bellelli G., Gasparotti R., Garibotto V., Di Luca M., Scifo P., Perani D., Padovani A. Evidence of white matter changes on diffusion tensor imaging in frontotemporal dementia. Arch. Neurol. 2007, 64:246-251.
7. Brooks B.R., Miller R.G., Swash M., Munsat T.L. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 2000, 1:293-299. World Federation of Neurology Research Group on Motor Neuron Diseases.
8. Burrell J.R., Kiernan M.C., Vucic S., Hodges J.R. Motor neuron dysfunction in frontotemporal dementia. Brain 2011, 134:2582-2594.
9. Caffarra P., Vezzadini G., Dieci F., Zonato F., Venneri A. Reye Osterrieth complex figure: normative values in an Italian population sample. Neurol. Sci. 2002, 22:443-447.
10. Cedarbaum J.M., Stambler N., Malta E., Fuller C., Hilt D., Thurmond B., Nakanishi A. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function: BDNF ALS Study Group (Phase III). J.Neurol. Sci. 1999, 169:13-21. BDNF ALS Study Group (Phase III).
11. Chang J.L., Lomen-Hoerth C., Murphy J., Henry R.G., Kramer J.H., Miller B.L., Gorno-Tempini M.L. Avoxel-based morphometry study of patterns of brain atrophy in ALS and ALS/FTLD. Neurology 2005, 65:75-80.
12. Cirillo M., Esposito F., Tedeschi G., Caiazzo G., Sagnelli A., Piccirillo G., Conforti R., Tortora F., Monsurrò M.R., Cirillo S., Trojsi F. Widespread microstructural white matter involvement in amyotrophic lateral sclerosis: a whole brain DTI study. Am. J. Neuroradiol. 2012, 33:1102-1108.
13. Clark C.M., Forman M.S. Frontotemporal lobar degeneration with motor neuron disease: a clinical and pathological spectrum. Arch. Neurol. 2006, 63:489-490.
14. Cole D.M., Beckmann C.F., Searle G.E., Plisson C., Tziortzi A.C., Nichols T.E., Gunn R.G., Matthews P.M., Rabiner E.A., Beaver J.D. Orbitofrontal connectivity with resting-state networks is associated with midbrain dopamine D3 receptor availability. Cereb. Cortex 2012, 22:2784-2793.
15. d'Ambrosio A., Gallo A., Trojsi F., Corbo D., Esposito F., Cirillo M., Monsurrò M.R., Tedeschi G. Frontotemporal cortical thinning in amyotrophic lateral sclerosis. Am. J. Neuroradiol. 2014, 35:304-310.
16. 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. U.S.A 2006, 103:13848-13853.
17. Dejesus-Hernandez M., Mackenzie I.R., Boeve B.F., Boxer A.L., Baker M., Rutherford N.J., Nicholson A.M., Finch N.A., Flynn H., Adamson J., Kouri N., Wojtas A., Sengdy P., Hsiung G.Y., Karydas A., Seeley W.W., Josephs K.A., Coppola G., Geschwind D.H., Wszolek Z.K., Feldman H., Knopman D.S., Petersen R.C., Miller B.L., Dickson D.W., Boylan K.B., Graff-Radford N.R., Rademakers R. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 2011, 72:245-256.
18. Deng H.X., Chen W., Hong S.T., Boycott K.M., Gorrie G.H., Siddique N., Yang Y., Fecto F., Shi Y., Zhai H., Jiang H., Hirano M., Rampersaud E., Jansen G.H., Donkervoort S., Bigio E.H., Brooks B.R., Ajroud K., Sufit R.L., Haines J.L., Mugnaini E., Pericak-Vance M.A., Siddique T. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 2011, 477:211-215.
19. Douaud G., Filippini N., Knight S., Talbot K., Turner M.R. Integration of structural and functional magnetic resonance imaging in amyotrophic lateral sclerosis. Brain 2011, 134:3470-3479.
20. Dubois B., Slachevsky A., Litvan I., Pillon B. The FAB: a frontal assessment battery at bedside. Neurology 2000, 55:1621-1626.
21. Ellis C.M., Suckling J., Amaro E., Bullmore E.T., Simmons A., Williams S.C., Leigh P.N. Volumetric analysis reveals corticospinal tract degeneration and extramotor involvement in ALS. Neurology 2001, 57:1571-1578.
22. Esposito F., Scarabino T., Hyvärinen A., Himberg J., Formisano E., Comani S., Tedeschi G., Goebel R., Seifritz E., Di Salle F. Independent component analysis of fMRI group studies by self-organizing clustering. Neuroimage 2005, 25:193-205.
23. Farb N.A.S., Grady C.L., Strother S., Tang-Wai D.F., Masellis M., Black S., Freedman M., Pollock B.G., Campbell K.L., Hasher L., Chow T.W. Abnormal network connectivity in frontotemporal dementia: evidence for prefrontal isolation. Cortex 2013, 49:1856-1873.
24. Filippi M., Agosta F., Scola E., Canu E., Magnani G., Marcone A., Valsasina P., Caso F., Copetti M., Comi G., Cappa S.F., Falini A. Functional network connectivity in the behavioral variant of frontotemporal dementia. Cortex 2013, 49:2389-2401.
25. 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.
26. 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.
27. Geser F., Brandmeir N.J., Kwong L.K., Martinez-Lage M., Elman L., McCluskey L., Xie S.X., Lee V.M.-Y., Trojanowski J.Q. Evidence of multisystem disorder in whole-brain map of pathological TDP-43 in amyotrophic lateral sclerosis. Arch. Neurol. 2008, 65:636-641.
28. Geser F., Martinez-Lage M., Robinson J., Uryu K., Neumann M., Brandmeir N.J., Xie S.X., Kwong L.K., Elman L., McCluskey L., Clark C.M., Malunda J., Miller B.L., Zimmerman E.A., Qian J., Van Deerlin V., Grossman M., Lee V.M., Trojanowski J.Q. Clinical and pathological continuum of multisystem TDP-43 proteinopathies. Arch. Neurol. 2009, 66:180-189.
29. Grace J., Stout J.C., Malloy P.F. Assessing frontal lobe behavioral syndromes with the frontal lobe personality scale. Assessment 1999, 6:269-284.
30. Greicius M.D., Flores B.H., Menon V., Glover G.H., Solvason H.B., Kenna H., Reiss A.L., Schatzberg A.F. Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol. Psychiatry 2007, 62:429-437.
31. Hyvärinen A., Karhunen J., Oja E. Independent component analysis 2001, John Wiley and Sons, New York.
32. Kawashima T., Dohura K., Kikuchi H., Iwaki T. Cognitive dysfunction in patients with amyotrophic lateral sclerosis is associated with spherical or crescent-shaped ubiquitinated intraneuronal inclusions in the parahippocampal gyrus and amygdala, but not in the neostriatum. Acta Neuropathol. 2001, 102:467-472.
33. Kipps C.M., Hodges J.R., Hornberger M. Nonprogressive behavioural frontotemporal dementia: recent developments and clinical implications of the "bvFTD phenocopy syndrome". Curr. Opin. Neurol. 2010, 23:628-632.
34. Lillo P., Mioshi E., Burrell J.R., Kiernan M.C., Hodges J.R., Hornberger M. Grey and white matter changes across the amyotrophic lateral sclerosis-frontotemporal dementia continuum. PLoS One 2012, 7:e43993.
35. Ling S.C., Polymenidou M., Cleveland D.V. Converging mechanisms in ALS and FTD: disrupted RNA and protein homeostasis. Neuron 2013, 79:416-438.
36. Lomen-Hoerth C. Characterization of amyotrophic lateral sclerosis and frontotemporal dementia. Dement. Geriatr. Cogn. Disord. 2004, 17:337-341.
37. Lomen-Hoerth C., Anderson T., Miller B. The overlap of amyotrophic lateral sclerosis and frontotemporal dementia. Neurology 2002, 59:1077-1079.
38. Lulé D., Diekmann V., Kassubek J., Kurt A., Birbaumer N., Ludolph A.C., Kraft E. Cortical plasticity in amyotrophic lateral sclerosis: motor imagery and function. Neurorehabil. Neural Repair 2007, 21:518-526.
39. Mantini D., Perrucci M.G., Del Gratta C., Romani G.L., Corbett M. Electrophysiological signatures of resting state networks in the human brain. Proc. Natl. Acad. Sci. U.S.A 2007, 104:13170-13175.
40. Mioshi E., Dawson K., Mitchell J., Arnold R., Hodges J.R. The Addenbrooke's Cognitive Examination Revised (ACE-R): a brief cognitive test battery for dementia screening. Int. J. Geriatr. Psychiatry 2006, 21:1078-1085.
41. Mioshi E., Hsieh S., Savage S., Hornberger M., Hodges J.R. Clinical staging and disease progression in frontotemporal dementia. Neurology 2010, 74:1591-1597.
42. Mohammadi B., Kollewe K., Samii A., Krampfl K., Dengler R., Münte T.F. Changes of resting state brain networks in amyotrophic lateral sclerosis. Exp. Neurol. 2009, 217:147-153.
43. Murphy J.M., Henry R.G., Langmore S., Kramer J.H., Miller B.L., Lomen-Hoerth C. Continuum of frontal lobe impairment in amyotrophic lateral sclerosis. Arch. Neurol. 2007, 64:530-534.
44. Neumann M., Sampathu D.M., Kwong L.K., Truax A.C., Micsenyi M.C., Chou T.T., Bruce J., Schuck T., Grossman M., Clark C.M., McCluskey L.F., Miller B.L., Masliah E., Mackenzie I.R., Feldman H., Feiden W., Kretzschmar H.A., Trojanowski J.Q., Lee V.M. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006, 314:130-133.
45. Novelli G., Papagno C., Capitani E., Laiacona N., Vallar G., Cappa S.F. Tre test clinici di ricerca e produzione lessicale. Taratura su soggetti normali. Arch. Psicol. Neurol. Psichiatr. 1986, 47:477-506.
46. Orsini A., Grossi D., Capitani E., Laiacona M., Papagno C., Vallar G. Verbal and spatial immediate memory span: normative data from 1355 adults and 1112 children. Ital. J. Neurol. Sci. 1987, 8:539-548.
47. Raichle M.E., MacLeod A.M., Snyder A.Z., Powers W.J., Gusnard D.A., Shulman G.L. Adefault mode of brain function. Proc. Natl. Acad. Sci. U.S.A 2001, 98:676-682.
48. Rascovsky K., Hodges J.R., Knopman D., Mendez M.F., Kramer J.H., Neuhaus J., van Swieten J.C., Seelaar H., Dopper E.G., Onyike C.U., Hillis A.E., Josephs K.A., Boeve B.F., Kertesz A., Seeley W.W., Rankin K.P., Johnson J.K., Gorno-Tempini M.L., Rosen H., Prioleau-Latham C.E., Lee A., Kipps C.M., Lillo P., Piguet O., Rohrer J.D., Rossor M.N., Warren J.D., Fox N.C., Galasko D., Salmon D.P., Black S.E., Mesulam M., Weintraub S., Dickerson B.C., Diehl-Schmid J., Pasquier F., Deramecourt V., Lebert F., Pijnenburg Y., Chow T.W., Manes F., Grafman J., Cappa S.F., Freedman M., Grossman M., Miller B.L. Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain 2011, 134:2456-2477.
49. Renton A.E., Majounie E., Waite A., Simon-Sanchez J., Rollinson S., Gibbs J.R., Schymick J.C., Laaksovirta H., van Swieten J.C., Myllykangas L., Kalimo H., Paetau A., Abramzon Y., Remes A.M., Kaganovich A., Scholz S.W., Duckworth J., Ding J., Harmer D.W., Hernandez D.G., Johnson J.O., Mok K., Ryten M., Trabzuni D., Guerreiro R.J., Orrell R.W., Neal J., Murray A., Pearson J., Jansen I.E., Sondervan D., Seelaar H., Blake D., Young K., Halliwell N., Callister J.B., Toulson G., Richardson A., Gerhard A., Snowden J., Mann D., Neary D., Nalls M.A., Peuralinna T., Jansson L., Isoviita V.M., Kaivorinne A.L., Hölttä-Vuori M., Ikonen E., Sulkava R., Benatar M., Wuu J., Chiò A., Restagno G., Borghero G., Sabatelli M., Heckerman D., Rogaeva E., Zinman L., Rothstein J.D., Sendtner M., Drepper C., Eichler E.E., Alkan C., Abdullaev Z., Pack S.D., Dutra A., Pak E., Hardy J., Singleton A., Williams N.M., Heutink P., Pickering-Brown S., Morris H.R., Tienari P.J., Traynor B.J. Ahexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS- FTD. Neuron 2011, 72:257-268. ITALSGEN Consortium.
50. Ringholz G.M., Appel S.H., Bradshaw M., Cooke N.A., Mosnik D.M., Schulz P.E. Prevalence and patterns of cognitive impairment in sporadic ALS. Neurology 2005, 65:586-590.
51. Schuster C., Kasper E., Dyrba M., Machts J., Bittner D., Kaufmann J., Mitchell A.J., Benecke R., Teipel S., Vielhaber S., Prudlo J. Cortical thinning and its relation to cognition in amyotrophic lateral sclerosis. Neurobiol. Aging 2014, 35:240-246.
52. Seeley W.W., Menon V., Schatzberg A.F., Keller J., Glover G.H., Kenna H., Reiss A.L., Greicius M.D. Dissociable intrinsic connectivity networks for salience processing and executive control. J.Neurosci. 2007, 27:2349-2356.
53. Seeley W.W., Crawford R., Rascovsky K., Kramer J.H., Weiner M., Miller B.L., Gorno-Tempini M.L. Frontal paralimbic network atrophy in very mild behavioral variant frontotemporal dementia. Arch. Neurol. 2008, 65:249-255.
54. Seeley W.W., Crawford R.K., Zhou J., Miller B.L., Greicius M.D. Neurodegenerative diseases target large-scale human brain networks. Neuron 2009, 16:42-52.
55. Smith S.M., Fox P.T., Miller K.L., Glahn D.C., Fox P.M., Mackay C.E., Filippini N., Watkins K.E., Toro R., Laird A.R., Beckmann C.F. Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. U.S.A 2009, 106:13040-13045.
56. Spinnler M., Tognoni G. Standardizzazione e taratura italiana di test neuropsicologici. Ital. J. Neurol. Sci. 1987, 6(Suppl 8):1-120.
57. Tedeschi G., Trojsi F., Tessitore A., Corbo D., Sagnelli A., Paccone A., d'Ambrosio A., Piccirillo G., Cirillo M., Cirillo S., Monsurroỳ M.R., Esposito F. Interaction between aging and neurodegeneration in amyotrophic lateral sclerosis. Neurobiol. Aging 2012, 33:886-898.
58. Thomas M., Alegre-Abarrategui J., Wade-Martins R. RNA dysfunction and aggrephagy at the centre of an amyotrophic lateral sclerosis/frontotemporal dementia disease continuum. Brain 2012, 136:1345-1360.
59. Turner M.R., Cagnin A., Turkheimer F.E., Miller C.C., Shaw C.E., Brooks D.J., Leigh P.N., Banati R.B. Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: an [(11)C](R)-PK11195 positron emission tomography study. Neurobiol. Dis. 2004, 15:601-609.
60. Turner M.R., Osei-Lah A.D., Hammers A., Al-Chalabi A., Shaw C.E., Andersen P.M., Brooks D.J., Leigh P.N., Mills K.R. Abnormal cortical excitability in sporadic but not homozygous D90A SOD1 ALS. J.Neurol. Neurosurg. Psychiatry 2005, 76:1279-1285.
61. van de Ven V.G., Formisano E., Prvulovic D., Roeder C.H., Linden D.E. Functional connectivity as revealed by spatial independent component analysis of fMRI measurements during rest. Hum. Brain Mapp. 2004, 22:165-178.
62. Verstraete E., van den Heuvel M.P., Veldink J.H., Blanken N., Mandl R.C., Hulshoff H.E., van den Berg L.H. Motor network degeneration in amyotrophic lateral sclerosis: a structural and functional connectivity study. PLoS One 2010, 5:e13664.
63. Whitwell J.L., Avula R., Senjem M.L., Kantarci K., Weigand S.D., Samikoglu A., Edmonson H.A., Vemuri P., Knopman D.S., Boeve B.F., Petersen R.C., Josephs K.A., Jack C.R. Gray and white matter water diffusion in the syndromic variants of frontotemporal dementia. Neurology 2010, 74:1279-1287.
64. Whitwell J.L., Josephs K.A., Avula R., Tosakulwong N., Weigand S.D., Senjem M.L., Vemuri P., Jones D.T., Gunter J.L., Baker M., Wszolek Z.K., Knopman D.S., Rademakers R., Petersen R.C., Boeve B.F., Jack C.R. Altered functional connectivity in asymptomatic MAPT subjects: a comparison to bvFTD. Neurology 2011, 77:866-874.
65. Wilson C.M., Grace G.M., Munoz D.G., He B.P., Strong M.J. Cognitive impairment in sporadic ALS: a pathologic continuum underlying a multisystem disorder. Neurology 2001, 57:651-657.
66. Yang W.W., Sidman R.L., Taksir T.V., Treleaven C.M., Fidler J.A., Cheng S.H., Dodge J.C., Shihabuddin L.S. Relationship between neuropathology and disease progression in the SOD1(G93A) ALS mouse. Exp. Neurol. 2011, 227:287-295.
67. Zhou J., Greicius M.D., Gennatas E.D., Growdon M.E., Jang J.Y., Rabinovici G.D., Kramer J.H., Weiner M., Miller B.L., Seeley W.W. Divergent network connectivity changes in behavioural variant frontotemporal dementia and Alzheimer's disease. Brain 2010, 133:1352-1367.