Diffusion tensor MRI changes in gray structures of the frontal-subcortical circuits in amyotrophic lateral sclerosis

Neurological Sciences

Volumn 35, Issue 6, 2014, Pages 911-918

  Barbagallo, Gaetano ^b   Nicoletti, Giuseppe ^a   Cherubini, Andrea ^a   Trotta, Maria ^b   Tallarico, Tiziana ^b   Chiriaco, Carmelina ^a   Nisticò, Rita ^a   Salvino, Dania ^b   Bono, Francesco ^b   Valentino, Paola ^b   Quattrone, Aldo ^a,b  

^a CNR   (Italy)

^b UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

Author keywords

Amyotrophic lateral sclerosis; Diffusion tensor imaging; Frontal impairment; Frontal subcortical circuits

Indexed keywords

ADULT; AGED; AMYGDALOID NUCLEUS; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CAUDATE NUCLEUS; CLINICAL ARTICLE; CLINICAL FEATURE; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; FEMALE; FRACTIONAL ANISOTROPY; FRONTAL CORTEX; GLOBUS PALLIDUS; GRAY MATTER; HIPPOCAMPUS; HUMAN; MALE; NEUROPSYCHOLOGICAL TEST; PUTAMEN; THALAMUS; BASAL GANGLION; BRAIN; DIFFUSION WEIGHTED IMAGING; FRONTAL LOBE; MIDDLE AGED; PATHOLOGY; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; AMYGDALA; AMYOTROPHIC LATERAL SCLEROSIS; BASAL GANGLIA; BRAIN; DIFFUSION MAGNETIC RESONANCE IMAGING; DIFFUSION TENSOR IMAGING; FEMALE; FRONTAL LOBE; HUMANS; MALE; MIDDLE AGED;

EID: 84903374323     PISSN: 15901874     EISSN: 15903478     Source Type: Journal    
DOI: 10.1007/s10072-013-1626-z     Document Type: Article

References (70)

1. Rowland LP (1998) Diagnosis of amyotrophic lateral sclerosis. J Neurol Sci 160(Suppl 1):6-24
2. Smith MC (1960) Nerve fibre degeneration in the brain in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 23:269-282
3. Bigio EH, Lipton AM, White CL 3rd, Dickson DW, Hirano A (2003) Frontotemporal and motor neurone degeneration with neurofilament inclusion bodies: additional evidence for overlap between FTD and ALS. Neuropathol Appl Neurobiol 29:239-253 (Pubitemid 36718172)
4. Ringholz GM, Appel SH, Bradshaw M, Cooke NA, Mosnik DM, Schulz PE (2005) Prevalence and pattern of cognitive impairment in sporadic amyotrophic lateral sclerosis. Neurology 65:586-590 (Pubitemid 41170719)
5. Talbot PR, Goulding PJ, Lloyd JJ, Snowden JS, Neary D, Testa HJ (1995) Inter-relation between "classic" motor neuron disease and frontotemporal dementia: neuropsychological and single photon emission computed tomography study. J Neurol Neurosurg Psychiatry 58:541-547
6. Thivard L, Pradat PF, Lehéricy S, Lacomblez L, Dormont D, Chiras J, Benali H, Meininger V (2007) Diffusion tension imaging and voxel based morphometry study in amyotrophic lateral sclerosis: relationships with motor disability. J Neurol Neurosurg Psychiatry 78:889-892 (Pubitemid 47204601)
7. Chenevert TL, Brunberg JA, Pipe JG (1990) Anisotropic diffusion in human white matter: demonstration with MR techniques in vivo. Radiology 177:401-405 (Pubitemid 20374856)
8. Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusiontensor MRI. J Magn Reson B 111:209-219 (Pubitemid 126758682)
9. Ellis CM, Simmons A, Jones DK, Bland J, Dawson JM, Horsfield MA, Williams SC, Leigh PN (1999) Diffusion tensor MRI assesses corticospinal tract damage in ALS. Neurology 53:1051-1058 (Pubitemid 29442122)
10. Graham JM, Papadakis N, Evans J, Widjaja E, Romanowski CA, Paley MN, Wallis LI, Wilkinson ID, Shaw PJ, Griffiths PD (2004) Diffusion tensor imaging for the assessment of upper motor neuron integrity in ALS. Neurology 63:2111-2119 (Pubitemid 39636260)
11. Toosy AT, Werring DJ, Orrell RW, Howard RS, King MD, Barker GJ, Miller DH, Thompson AJ (2003) Diffusion tensor imaging detects corticospinal tract involvement at multiple levels in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 74:1250-1257
12. Ciccarelli O, Behrens TE, Johansen-Berg H, Talbot K, Orrell RW, Howard RS, Nunes RG, Miller DH, Matthews PM, Thompson AJ, Smith SM (2009) Investigation of white matter pathology in ALS and PLS using tract-based spatial statistics. Hum Brain Mapp 30:615-624
13. Filippini N, Douaud G, Mackay CE, Knight S, Talbot K, Turner MR (2010) Corpus callosum involvement is a consistent feature of amyotrophic lateral sclerosis. Neurology 75:1645-1652
14. Cirillo M, Esposito F, Tedeschi G, Caiazzo G, Sagnelli A, Piccirillo G, Conforti R, Tortora F, Monsurrò MR, Cirillo S, Trojsi F (2012) Widespread microstructural white matter involvement in amyotrophic lateral sclerosis: a whole-brain DTI study. AJNR Am J Neuroradiol 33:1102-1108
15. Canu E, Agosta F, Riva N, Sala S, Prelle A, Caputo D, Perini M, Comi G, Filippi M (2011) The topography of brain microstructural damage in amyotrophic lateral sclerosis assessed using diffusion tensor MR imaging. AJNR Am J Neuroradiol 32:1307-1314
16. Sharma KR, Sheriff S, Maudsley A, Govind V (2013) Diffusion tensor imaging of basal ganglia and thalamus in amyotrophic lateral sclerosis. J Neuroimaging 23:368-374
17. Kawashima T, Doh-ura K, Kikuchi H, Iwaki T (2001) 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 102:467-472 (Pubitemid 32976080)
18. Takeda T, Uchihara T, Arai N, Mizutani T, Iwata M (2009) Progression of hippocampal degeneration in amyotrophic lateral sclerosis with or without memory impairment: distinction from Alzheimer disease. Acta Neuropathol 117:35-44
19. Anderson VE, Cairns NJ, Leigh PN (1995) Involvement of the amygdala, dentate and hippocampus in motor neuron disease. J Neurol Sci 129(Suppl):75-78
20. Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357-381 (Pubitemid 16055790)
21. Brooks BR, Miller RG, Swash M, Munsat TL, World Federation of Neurology Research Group on Motor Neuron Diseases (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 1:293-299
22. Cedarbaum JM, Stambler N, Malta E, Fuller C, Hilt D, Thurmond B, Nakanishi A (1999) The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J Neurol Sci 169:13-21 (Pubitemid 29502501)
23. Folstein MF, Folstein SE, McHugh PR (1975) "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189-198
24. Beck AT, Steer RA, Brown GK (1996) Manual for beck depression inventory-II. Psychological Corporation, San Antonio
25. Rey A (1958) Memorisation d'une serie de 15 mots en 5 repetitions. Presses Universitaries des France, Paris
26. Benton A, Hamsher KD (1989) Multilingual aphasia examination. AJA Associates, Iowa City
27. Nelson HE (1976) A modified card sorting test sensitive to frontal lobe defects. Cortex 12:313-324
28. Dubois B, Slachevsky A, Litvan I, Pillon B (2000) The FAB: a frontal assessment battery at bedside. Neurology 55:1621-1626
29. Cherubini A, Péran P, Caltagirone C, Sabatini U, Spalletta G (2009) Aging of subcortical nuclei: microstructural, mineralization and atrophy modifications measured in vivo using MRI. Neuroimage 48:29-36
30. Nicoletti G, Lodi R, Condino F, Tonon C, Fera F, Malucelli E, Manners D, Zappia M, Morgante L, Barone P, Barbiroli B, Quattrone A (2006) Apparent diffusion coefficient measurements of the middle cerebellar peduncle differentiate the Parkinson variant of MSA from Parkinson's disease and progressive supranuclear palsy. Brain 129:2679-2687 (Pubitemid 44522101)
31. Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G (1996) Diffusion tensor MR imaging of the human brain. Radiology 201:637-648
32. Senda J, Kato S, Kaga T, Ito M, Atsuta N, Nakamura T, Watanabe H, Tanaka F, Naganawa S, Sobue G (2011) Progressive and widespread brain damage in ALS: MRI voxel-based morphometry and diffusion tensor imaging study. Amyotroph Lateral Scler 12:59-69
33. Lillo P, Mioshi E, Burrell JR, Kiernan MC, Hodges JR, Hornberger M (2012) Grey and white matter changes across the amyotrophic lateral sclerosis-frontotemporal dementia continuum. PLoS ONE 7:e43993
34. Sharma KR, Saigal G, Maudsley AA, Govind V (2011) 1H MRS of basal ganglia and thalamus in amyotrophic lateral sclerosis. NMR Biomed 24:1270-1276
35. Al-Sarraj S, Maekawa S, Kibble M, Everall I, Leigh N (2002) Ubiquitin-only intraneuronal inclusion in the substantia nigra is a characteristic feature of motor neurone disease with dementia. Neuropathol Appl Neurobiol 28:120-128 (Pubitemid 34415730)
36. Geser F, Martinez-Lage M, Robinson J, Uryu K, Neumann M, Brandmeir NJ, Xie SX, Kwong LK, Elman L, McCluskey L, Clark CM, Malunda J, Miller BL, Zimmerman EA, Qian J, Van Deerlin V, Grossman M, Lee VM, Trojanowski JQ (2009) Clinical and pathological continuum of multisystem TDP-43 proteinopathies. Arch Neurol 66:180-189
37. Geser F, Brandmeir NJ, Kwong LK, Martinez-Lage M, Elman L, McCluskey L, Xie SX, Lee VM, Trojanowski JQ (2008) Evidence of multisystem disorder in whole-brain map of pathological TDP-43 in amyotrophic lateral sclerosis. Arch Neurol 65:636-641 (Pubitemid 351679659)
38. Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M (1986) MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161:401-407 (Pubitemid 17173295)
39. Verstraete E, Veldink JH, Hendrikse J, Schelhaas HJ, van den Heuvel MP, van den Berg LH (2012) Structural MRI reveals cortical thinning in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 83:383-388
40. D'Ambrosio A, Gallo A, Trojsi F, Corbo D, Esposito F, Cirillo M, Monsurró MR, Tedeschi G (2013) Frontotemporal cortical thinning in amyotrophic lateral sclerosis. AJNR Am J Neuroradiol. doi:10.3174/ajnr.A3753
41. DeLong MR, Wichmann T (2007) Circuits and circuit disorders of the basal ganglia. Arch Neurol 64:20-24 (Pubitemid 46072419)
42. Strong MJ, Grace GM, Freedman M, Lomen-Hoerth C, Woolley S, Goldstein LH, Murphy J, Shoesmith C, Rosenfeld J, Leigh PN, Bruijn L, Ince P, Figlewicz D (2009) Consensus criteria for the diagnosis of frontotemporal cognitive and behavioural syndromes in amyotrophic lateral sclerosis. Amyotroph Lateral Scler 10:131-146
43. Cummings JL (1995) Anatomic and behavioral aspects of frontal-subcortical circuits. Ann N Y Acad Sci 15(769):1-13
44. Bonelli RM, Cummings JL (2007) Frontal-subcortical circuitry and behavior. Dialogues Clin Neurosci 9:141-151 (Pubitemid 47075462)
45. Tekin S, Cummings JL (2002) Frontal-subcortical neuronal circuits and clinical neuropsychiatry: an update. J Psychosom Res 53:647-654 (Pubitemid 36292444)
46. Agosta F, Pagani E, Petrolini M, Caputo D, Perini M, Prelle A, Salvi F, Filippi M (2010) Assessment of white matter tract damage in patients with amyotrophic lateral sclerosis: a diffusion tensor MR imaging tractography study. AJNR Am J Neuroradiol 31:1457-1461
47. Sato K, Aoki S, Iwata NK, Masutani Y, Watadani T, Nakata Y, Yoshida M, Terao Y, Abe O, Ohtomo K, Tsuji S (2010) Diffusion tensor tract-specific analysis of the uncinate fasciculus in patients with amyotrophic lateral sclerosis. Neuroradiology 52:729-733
48. Sarro L, Agosta F, Canu E, Riva N, Prelle A, Copetti M, Riccitelli G, Comi G, Filippi M (2011) Cognitive functions and white matter tract damage in amyotrophic lateral sclerosis: a diffusion tensor tractography study. AJNR Am J Neuroradiol 32:1866-1872
49. Sage CA, Peeters RR, Görner A, Robberecht W, Sunaert S (2007) Quantitative diffusion tensor imaging in amyotrophic lateral sclerosis. Neuroimage 34:486-499 (Pubitemid 44830171)
50. Tsujimoto M, Senda J, Ishihara T, Niimi Y, Kawai Y, Atsuta N, Watanabe H, Tanaka F, Naganawa S, Sobue G (2011) Behavioral changes in early ALS correlate with voxel-based morphometry and diffusion tensor imaging. J Neurol Sci 307:34-40
51. Li J, Pan P, Song W, Huang R, Chen K, Shang H (2012) A meta-analysis of diffusion tensor imaging studies in amyotrophic lateral sclerosis. Neurobiol Aging 33:1833-1838
52. Phukan J, Pender NP, Hardiman O (2007) Cognitive impairment in amyotrophic lateral sclerosis. Lancet Neurol 6:994-1003 (Pubitemid 47562321)
53. Christidi F, Zalonis I, Smyrnis N, Evdokimidis I (2012) Selective attention and the three-process memory model for the interpretation of verbal free recall in amyotrophic lateral sclerosis. J Int Neuropsychol Soc 18:809-818
54. Ludolph AC, Langen KJ, Regard M, Herzog H, Kempo B, Kurwert T (1992) Frontal lobe function in amyotrophic lateral sclerosis: a neuropsychologic and positron emission tomography study. Acta Neurol Scand 85:81-89
55. Gallassi R, Montagna P, Ciardulli C, Lorusso S, Mussuto V, Stracciari A (1985) Cognitive impairment in motor neuron disease. Acta Neurol Scand 71:480-484 (Pubitemid 15002114)
56. Moretti R, Torre P, Antonello RM, Carraro N, Cazzato G, Bava A (2002) Complex cognitive disruption in motor neuron disease. Dement Geriatr Cogn Disord 14:141-150
57. Ahn SW, Kim SH, Kim JE, Kim SM, Kim SH, Sung JJ, Lee KW, Hong YH (2011) Frontal assessment battery to evaluate frontal lobe dysfunction in ALS patients. Can J Neurol Sci 38:242-246
58. Stukovnik V, Zidar J, Podnar S, Repovs G (2010) Amyotrophic lateral sclerosis patients show executive impairments on standard neuropsychological measures and an ecologically valid motor-free test of executive functions. J Clin Exp Neuropsychol 32:1095-1109
59. Achi EY, Rudnicki SA (2012) ALS and frontotemporal dysfunction: a review. Neurol Res Int 2012:806306
60. Mioshi E, Lillo P, Yew B, Hsieh S, Savage S, Hodges JR, Kiernan MC, Hornberger M (2013) Cortical atrophy in ALS is critically associated with neuropsychiatric and cognitive changes. Neurology 80:1117-1123
61. Cerami C, Dodich A, Canessa N, Crespi C, Iannaccone S, Corbo M, Lunetta C, Consonni M, Scola E, Falini A, Cappa SF (2013) Emotional empathy in amyotrophic lateral sclerosis: a behavioural and voxel-based morphometry study. Amyotroph Lateral Scler Frontotemporal Degener. doi:10.3109/21678421.2013.785568
62. Passamonti L, Fera F, Tessitore A, Russo A, Cerasa A, Gioia CM, Monsurrò MR, Migliaccio R, Tedeschi G, Quattrone A (2013) Dysfunctions within limbic-motor networks in amyotrophic lateral sclerosis. Neurobiol Aging 34:2499-2509
63. Massman PJ, Sims J, Cooke N, Haverkamp LJ, Appel V, Appel SH (1996) Prevalence and correlates of neuropsychological deficits in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 61:450-455 (Pubitemid 26394900)
64. Averill AJ, Kasarskis EJ, Segerstrom SC (2007) Psychological health in patients with amyotrophic lateral sclerosis. Amyotroph Lateral Scler 8:243-254 (Pubitemid 47190229)
65. Atassi N, Cook A, Pineda CM, Yerramilli-Rao P, Pulley D, Cudkowicz M (2011) Depression in amyotrophic lateral sclerosis. Amyotroph Lateral Scler 12:109-112
66. Jelsone-Swain L, Persad C, Votruba KL, Weisenbach SL, Johnson T, Gruis KL, Welsh RC (2012) The relationship between depressive symptoms, disease state, and cognition in amyotrophic lateral sclerosis. Front Psychol 3:542
67. Grossman AB, Woolley-Levine S, Bradley WG, Miller RG (2007) Detecting neurobehavioral changes in amyotrophic lateral sclerosis. Amyotroph Lateral Scler 8:56-61 (Pubitemid 46322941)
68. Gibbons ZC, Richardson A, Neary D, Snowden JS (2008) Behaviour in amyotrophic lateral sclerosis. Amyotroph Lateral Scler 9:67-74 (Pubitemid 351584031)
69. Woolley SC, Zhang Y, Schuff N, Weiner MW, Katz JS (2011) Neuroanatomical correlates of apathy in ALS using 4 Tesla diffusion tensor MRI. Amyotroph Lateral Scler 12:52-58
70. Eslinger PJ, Moore P, Antani S, Anderson C, Grossman M (2012) Apathy in frontotemporal dementia: behavioral and neuroimaging correlates. Behav Neurol 25:127-136