Magnetic resonance imaging as an approach towards identifying neuropathological biomarkers for Huntington's disease

Brain Research Reviews

Volumn 58, Issue 1, 2008, Pages 209-225

  Bohanna, India ^a   Georgiou Karistianis, Nellie ^b   Hannan, Anthony J ^a   Egan, Gary F ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Biomarker; Diffusion tensor imaging; Functional magnetic resonance imaging; Huntington's disease; Magnetic resonance imaging

Indexed keywords

BIOLOGICAL MARKER;

AMYGDALOID NUCLEUS; ANISOTROPY; BRAIN ATROPHY; BRAIN BLOOD FLOW; BRAIN CORTEX ATROPHY; BRAIN SIZE; CAUDATE NUCLEUS; CENTRAL NERVOUS SYSTEM DISEASE; CEREBELLUM; CEREBELLUM CORTEX; CLINICAL FEATURE; CLINICAL TRIAL; DIAGNOSTIC ACCURACY; DIFFUSION TENSOR IMAGING; DISEASE COURSE; DISEASE MARKER; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENETIC VARIABILITY; GLOBUS PALLIDUS; HUMAN; HUNTINGTON CHOREA; HYPOTHALAMUS; IMAGE ANALYSIS; NERVE DEGENERATION; NEUROANATOMY; NEUROIMAGING; NEUROPATHOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; PHENOTYPE; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PUTAMEN; RELIABILITY; REVIEW; THALAMUS;

BIOLOGICAL MARKERS; BRAIN; CLINICAL TRIALS AS TOPIC; DISEASE PROGRESSION; HUMANS; HUNTINGTON DISEASE; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING;

EID: 45549085845     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2008.04.001     Document Type: Review

References (102)

1. Alexander G.E., DeLong M.R., and Strick P.L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 9 (1986) 357-381
2. Aylward E.H. Change in MRI striatal volumes as a biomarker in preclinical Huntington's disease. Brain Res. Bull. 72 (2007) 152-158
3. Aylward E.H., Brandt J., Codori A.M., Mangus R.S., Barta P.E., and Harris G.J. Reduced basal ganglia volume associated with the gene for Huntington's disease in asymptomatic at-risk persons. Neurology. 44 (1994) 823-828
4. Aylward E.H., Codori A.M., Barta P.E., Pearlson G.D., Harris G.J., and Brandt J. Basal ganglia volume and proximity to onset in preclinical Huntington disease. Arch. Neurol. 53 (1996) 1293-1296
5. Aylward E.H., Li Q., Stine O.C., Ranen N., Sherr M., Barta P.E., Bylsma F.W., Pearlson G.D., and Ross C.A. Longitudinal change in basal ganglia volume in patients with Huntington's disease. Neurology. 48 (1997) 394-399
6. Aylward E.H., Anderson N.B., Bylsma F.W., Wagster M.V., Barta P.E., Sherr M., Feeney J., Davis A., Rosenblatt A., Pearlson G.D., and Ross C.A. Frontal lobe volume in patients with Huntington's disease. Neurology. 50 (1998) 252-258
7. Aylward E.H., Codori A.M., Rosenblatt A., Sherr M., Brandt J., Stine O.C., Barta P.E., Pearlson G.D., and Ross C.A. Rate of caudate atrophy in preclinical and clinical stages of Huntington's disease. Mov. Disord. 15 (2000) 552-560
8. Aylward E.H., Rosenblatt A., Field K., Yallapragada V., Kieburtz K., McDermott M., Raymond L.A., Almqvist E.W., Hayden M., and Ross C.A. Caudate volume as an outcome measure in clinical trials for Huntington's disease: a pilot study. Brain. Res. Bull. 62 (2003) 137-141
9. Aylward E.H., Sparks B.F., Field K.M., Yallapragada V., Shpritz B.D., Rosenblatt A., Brandt J., Gourley L.M., Liang K., Zhou H., Margolis R.L., and Ross C.A. Onset and rate of striatal atrophy in preclinical Huntington disease. Neurology 63 (2004) 66-72
10. Backman L., Robins-Wahlin T.B., Lundin A., Ginovart N., and Farde L. Cognitive deficits in Huntington's disease are predicted by dopaminergic PET markers and brain volumes. Brain 120 Pt 12 (1997) 2207-2217
11. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed. 15 (2002) 435-455
12. Beglinger L.J., Nopoulos P.C., Jorge R.E., Langbehn D.R., Mikos A.E., Moser D.J., Duff K., Robinson R.G., and Paulsen J.S. White matter volume and cognitive dysfunction in early Huntington's disease. Cogn. Behav. Neurol. 18 (2005) 102-107
13. Behrens T.E., Johansen-Berg H., Woolrich M.W., Smith S.M., Wheeler-Kingshott C.A., Boulby P.A., Barker G.J., Sillery E.L., Sheehan K., Ciccarelli O., Thompson A.J., Brady J.M., and Matthews P.M. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat. Neurosci. 6 (2003) 750-757
14. Berrios G.E., Wagle A.C., Markova I.S., Wagle S.A., Rosser A., and Hodges J.R. Psychiatric symptoms in neurologically clinical Huntington's disease gene carriers: a comparison with gene negative at risk subjects. Acta Psychiatr. Scand. 105 (2002) 224-230
15. Biomarkers Definitions Working Group. Biomarkers and surrogate endpoints: preferred definitions and conceptual framework. Clin. Pharmacol. Ther. 69 (2001) 89-95
16. Brandt J., Quaid K.A., and Folstein S.E. Preclinical DNA testing for Huntington's disease. J. Neuropsychiatry Clin. Neurosci. 1 (1989) 195-197
17. Brandt J., Bylsma F.W., Aylward E.H., Rothlind J., and Gow C.A. Impaired source memory in Huntington's disease and its relation to basal ganglia atrophy. J. Clin. Exp. Neuropsychol. 17 (1995) 868-877
18. Campodonico J.R., Aylward E., Codori A.M., Young C., Krafft L., Magdalinski M., Ranen N., Slavney P.R., and Brandt J. When does Huntington's disease begin?. J. Int. Neuropsychol. Soc. 4 (1998) 467-473
19. Cepeda C., Wu N., Andre V.M., Cummings D.M., and Levine M.S. The corticostriatal pathway in Huntington's disease. Prog. Neurobiol. 81 (2007) 253-271
20. Ciarmiello A., Cannella M., Lastoria S., Simonelli M., Frati L., Rubinsztein D.C., and Squitieri F. Brain white-matter volume loss and glucose hypometabolism precede the clinical symptoms of Huntington's disease. J. Nucl. Med. 47 (2006) 215-222
21. Clark V.P., Lai S., and Deckel A.W. Altered functional MRI responses in Huntington's disease. Neuroreport. 13 (2002) 703-706
22. Conneally P.M. Huntington disease: genetics and epidemiology. Am. J. Hum. Genet. 36 (1984) 506-526
23. Deckel A.W. Nitric oxide and nitric oxide synthase in Huntington's disease. J. Neurosci. Res. 64 (2001) 99-107
24. Douaud G., Gaura V., Ribeiro M.J., Lethimonnier F., Maroy R., Verny C., Krystkowiak P., Damier P., Bachoud-Levi A.C., Hantraye P., and Remy P. Distribution of grey matter atrophy in Huntington's disease patients: a combined ROI-based and voxel-based morphometric study. Neuroimage. 32 (2006) 1562-1575
25. Duff K., Paulsen J.S., Beglinger L.J., Langbehn D.R., and Stout J.C. Psychiatric symptoms in Huntington's disease before diagnosis: the predict-HD study. Biol. Psychiatry. 62 (2007) 1341-1346
26. Feigin A., Tang C., Ma Y., Mattis P., Zgaljardic D., Guttman M., Paulsen J.S., Dhawan V., and Eidelberg D. Thalamic metabolism and symptom onset in preclinical Huntington's disease. Brain 130 (2007) 2858-2867
27. Friston K.J. Functional and effective connectivity in neuroimaging: a synthesis. Hum. Brain Mapp. 2 (1994) 56-78
28. Georgiou-Karistianis N., Sritharan A., Farrow M., Cunnington R., Stout J., Bradshaw J., Churchyard A., Brawn T.L., Chua P., Chiu E., Thiruvady D., and Egan G. Increased cortical recruitment in Huntington's disease using a Simon task. Neuropsychologia. 45 (2007) 1791-1800
29. Giorgio A., Watkins K.E., Douaud G., James A.C., James S., De Stefano N., Matthews P.M., Smith S.M., and Johansen-Berg H. Changes in white matter microstructure during adolescence. Neuroimage. 39 (2008) 52-61
30. Gomez-Tortosa E., MacDonald M.E., Friend J.C., Taylor S.A., Weiler L.J., Cupples L.A., Srinidhi J., Gusella J.F., Bird E.D., Vonsattel J.P., and Myers R.H. Quantitative neuropathological changes in preclinical Huntington's disease. Ann. Neurol. 49 (2001) 29-34
31. Gropman A.L., and Adams D.R. Atypical patterns of inheritance. Semin. Pediatr. Neurol. 14 (2007) 34-45
32. Hagmann P., Jonasson L., Maeder P., Thiran J.P., Wedeen V.J., and Meuli R. Understanding diffusion MR imaging techniques: from scalar diffusion-weighted imaging to diffusion tensor imaging and beyond. Radiographics 26 Suppl 1 (2006) S205-S223
33. Hahn-Barma V., Deweer B., Durr A., Dode C., Feingold J., Pillon B., Agid Y., Brice A., and Dubois B. Are cognitive changes the first symptoms of Huntington's disease? A study of gene carriers. J. Neurol. Neurosurg. Psychiatry. 64 (1998) 172-177
34. Harris G.J., Pearlson G.D., Peyser C.E., Aylward E.H., Roberts J., Barta P.E., Chase G.A., and Folstein S.E. Putamen volume reduction on magnetic resonance imaging exceeds caudate changes in mild Huntington's disease. Ann. Neurol. 31 (1992) 69-75
35. Harris G.J., Codori A.M., Lewis R.F., Schmidt E., Bedi A., and Brandt J. Reduced basal ganglia blood flow and volume in preclinical, gene-tested persons at-risk for Huntington's disease. Brain. 122 Pt 9 (1999) 1667-1678
36. Harvey P.O., Fossati P., Pochon J.B., Levy R., Lebastard G., Lehericy S., Allilaire J.F., and Dubois B. Cognitive control and brain resources in major depression: an fMRI study using the n-back task. Neuroimage 26 (2005) 860-869
37. Hedreen J., Peyser C., Folstein S., and Ross C. Neuronal loss in layers V and VI of cerebral cortex in Huntington's disease. Neurosci. Lett. 133 (1991) 257-261
38. Hennenlotter A., Schroeder U., Erhard P., Haslinger B., Stahl R., Weindl A., von Einsiedel H.G., Lange K.W., and Ceballos-Baumann A.O. Neural correlates associated with impaired disgust processing in preclinical Huntington's disease. Brain. 127 (2004) 1446-1453
39. Hersch S., and Ferrante R.J. Neuropathology and pathophysiology of Huntington's disease. Movement disorders (1997), McGraw-Hill, Columbus, OH
40. Hodges J.R., Salmon D.P., and Butters N. Differential impairment of semantic and episodic memory in Alzheimer's and Huntington's diseases: a controlled prospective study. J. Neurol. Neurosurg. Psychiatry 53 (1990) 1089-1095
41. Horwitz B., Warner B., Fitzer J., Tagamets M.A., Husain F.T., and Long T.W. Investigating the neural basis for functional and effective connectivity. Application to fMRI. Philos. Trans. R. Soc. Lond., B. Biol. Sci. 360 (2005) 1093-1108
42. Hunter M.D., Ganesan V., Wilkinson I.D., and Spence S.A. Impact of modafinil on prefrontal executive function in schizophrenia. Am. J. Psychiatry 163 (2006) 2184-2186
43. Huntington Study Group. Unified Huntington's Disease Rating Scale: reliability and consistency. Mov. Disord. 11 (1996) 136-142
44. Jernigan T.L., Salmon D.P., Butters N., and Hesselink J.R. Cerebral structure on MRI, Part II: Specific changes in Alzheimer's and Huntington's diseases. Biol. Psychiatry 29 (1991) 68-81
45. Karlsgodt K.H., van Erp T.G., Poldrack R.A., Bearden C.E., Nuechterlein K.H., and Cannon T.D. Diffusion tensor imaging of the superior longitudinal fasciculus and working memory in recent-onset schizophrenia. Biol. Psychiatry 63 5 (2008) 512-518
46. Kassubek J., Juengling F.D., Kioschies T., Henkel K., Karitzky J., Kramer B., Ecker D., Andrich J., Saft C., Kraus P., Aschoff A.J., Ludolph A.C., and Landwehrmeyer G.B. Topography of cerebral atrophy in early Huntington's disease: a voxel based morphometric MRI study. J. Neurol. Neurosurg. Psychiatry 75 (2004) 213-220
47. Kassubek J., Juengling F.D., Ecker D., and Landwehrmeyer G.B. Thalamic atrophy in Huntington's disease co-varies with cognitive performance: a morphometric MRI analysis. Cereb. Cortex 15 (2005) 846-853
48. Kim J.S., Reading S.A., Brashers-Krug T., Calhoun V.D., Ross C.A., and Pearlson G.D. Functional MRI study of a serial reaction time task in Huntington's disease. Psychiatry Res. 131 (2004) 23-30
49. Kipps C.M., Duggins A.J., Mahant N., Gomes L., Ashburner J., and McCusker E.A. Progression of structural neuropathology in preclinical Huntington's disease: a tensor based morphometry study. J. Neurol. Neurosurg. Psychiatry 76 (2005) 650-655
50. Kircher T.T., Erb M., Grodd W., and Leube D.T. Cortical activation during cholinesterase-inhibitor treatment in Alzheimer disease: preliminary findings from a pharmaco-fMRI study. Am. J. Geriatr. Psychiatry 13 (2005) 1006-1013
51. Kirkwood S.C., Siemers E., Viken R., Hodes M.E., Conneally P.M., Christian J.C., and Foroud T. Longitudinal personality changes among preclinical Huntington disease gene carriers. Neuropsychiatry Neuropsychol. Behav. Neurol. 15 (2002) 192-197
52. Kloppel S., Draganski B., Golding C.V., Chu C., Nagy Z., Cook P.A., Hicks S.L., Kennard C., Alexander D.C., Parker G.J., Tabrizi S.J., and Frackowiak R.S. White matter connections reflect changes in voluntary-guided saccades in pre-symptomatic Huntington's disease. Brain 131 (2008) 196-204
53. Landau S.M., Garavan H., Schumacher E.H., and D'Esposito M. Regional specificity and practice: dynamic changes in object and spatial working memory. Brain Res. 1180 (2007) 78-89
54. Lawrence A.D., Sahakian B.J., Hodges J.R., Rosser A.E., Lange K.W., and Robbins T.W. Executive and mnemonic functions in early Huntington's disease. Brain 119 Pt 5 (1996) 1633-1645
55. Lawrence A.D., Hodges J.R., Rosser A.E., Kershaw A., ffrench-Constant C., Rubinsztein D.C., Robbins T.W., and Sahakian B.J. Evidence for specific cognitive deficits in preclinical Huntington's disease. Brain 121 Pt 7 (1998) 1329-1341
56. Leh S.E., Ptito A., Chakravarty M.M., and Strafella A.P. Fronto-striatal connections in the human brain: a probabilistic diffusion tractography study. Neurosci. Lett. 419 (2007) 113-118
57. Lekeu F., Van der Linden M., Chicherio C., Collette F., Degueldre C., Franck G., Moonen G., and Salmon E. Brain correlates of performance in a free/cued recall task with semantic encoding in Alzheimer disease. Alzheimer Dis. Assoc. Disord. 17 (2003) 35-45
58. Lemiere J., Decruyenaere M., Evers-Kiebooms G., Vandenbussche E., and Dom R. Cognitive changes in patients with Huntington's disease (HD) and asymptomatic carriers of the HD mutation-a longitudinal follow-up study. J. Neurol. 251 (2004) 935-942
59. Margolis R.L., and Ross C.A. Expansion explosion: new clues to the pathogenesis of repeat expansion neurodegenerative diseases. Trends Mol. Med. 7 (2001) 479-482
60. Mascalchi M., Lolli F., Della Nave R., Tessa C., Petralli R., Gavazzi C., Politi L.S., Macucci M., Filippi M., and Piacentini S. Huntington disease: volumetric, diffusion-weighted, and magnetization transfer MR imaging of brain. Radiology 232 (2004) 867-873
61. Meisenzahl E.M., Scheuerecker J., Zipse M., Ufer S., Wiesmann M., Frodl T., Koutsouleris N., Zetzsche T., Schmitt G., Riedel M., Spellmann I., Dehning S., Linn J., Bruckmann H., and Moller H.J. Effects of treatment with the atypical neuroleptic quetiapine on working memory function: a functional MRI follow-up investigation. Eur. Arch. Psychiatry Clin. Neurosci. 256 (2006) 522-531
62. Montoya A., Price B.H., Menear M., and Lepage M. Brain imaging and cognitive dysfunctions in Huntington's disease. J. Psychiatry Neurosci. 31 (2006) 21-29
63. Muhlau M., Gaser C., Wohlschlager A.M., Weindl A., Stadtler M., Valet M., Zimmer C., Kassubek J., and Peinemann A. Striatal gray matter loss in Huntington's disease is leftward biased. Mov. Disord. 22 (2007) 1169-1173
64. Murphy C., Cerf-Ducastel B., Calhoun-Haney R., Gilbert P.E., and Ferdon S. ERP, fMRI and functional connectivity studies of brain response to odor in normal aging and Alzheimer's disease. Chem. Senses 30 Suppl 1 (2005) i170-i171
65. Nithianantharajah J., and Hannan A.J. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat. Rev. Neurosci. 7 (2006) 697-709
66. Nopolous P., Magnotta V.A., Mikos A., Paulson H., Andreasen N.C., and Paulsen J.S. Morphology of the cerebral cortex in preclinical Huntington's disease. Am. J. Psychiatry 164 (2007) 1428-1434
67. Paulsen J.S., Zhao H., Stout J.C., Brinkman R.R., Guttman M., Ross C.A., Como P., Manning C., Hayden M.R., and Shoulson I. Clinical markers of early disease in persons near onset of Huntington's disease. Neurology. 57 (2001) 658-662
68. Paulsen J.S., Zimbelman J.L., Hinton S.C., Langbehn D.R., Leveroni C.L., Benjamin M.L., Reynolds N.C., and Rao S.M. fMRI biomarker of early neuronal dysfunction in preclinical Huntington's Disease. AJNR Am. J. Neuroradiol. 25 (2004) 1715-1721
69. Paulsen J.S., Hayden M., Stout J.C., Langbehn D.R., Aylward E., Ross C.A., Guttman M., Nance M., Kieburtz K., Oakes D., Shoulson I., Kayson E., Johnson S., and Penziner E. Preparing for preventive clinical trials: the Predict-HD study. Arch. Neurol. 63 (2006) 883-890
70. Paulsen J.S., Magnotta V.A., Mikos A.E., Paulson H.L., Penziner E., Andreasen N.C., and Nopoulos P.C. Brain structure in preclinical Huntington's disease. Biol. Psychiatry 59 (2006) 57-63
71. Peinemann A., Schuller S., Pohl C., Jahn T., Weindl A., and Kassubek J. Executive dysfunction in early stages of Huntington's disease is associated with striatal and insular atrophy: a neuropsychological and voxel-based morphometric study. J. Neurol. Sci. 239 (2005) 11-19
72. Peterson B., Riddle M.A., Cohen D.J., Katz L.D., Smith J.C., Hardin M.T., and Leckman J.F. Reduced basal ganglia volumes in Tourette's syndrome using three-dimensional reconstruction techniques from magnetic resonance images. Neurology 43 (1993) 941-949
73. Puri B.K., Bydder G.M., Counsell S.J., Corridan B.J., Richardson A.J., Hajnal J.V., Appel C., McKee H.M., Vaddadi K.S., and Horrobin D.F. MRI and neuropsychological improvement in Huntington disease following ethyl-EPA treatment. Neuroreport 13 (2002) 123-126
74. Reading S.A., Dziorny A.C., Peroutka L.A., Schreiber M., Gourley L.M., Yallapragada V., Rosenblatt A., Margolis R.L., Pekar J.J., Pearlson G.D., Aylward E., Brandt J., Bassett S.S., and Ross C.A. Functional brain changes in preclinical Huntington's disease. Ann. Neurol. 55 (2004) 879-883
75. Reading S.A., Yassa M.A., Bakker A., Dziorny A.C., Gourley L.M., Yallapragada V., Rosenblatt A., Margolis R.L., Aylward E.H., Brandt J., Mori S., van Zijl P., Bassett S.S., and Ross C.A. Regional white matter change in preclinical Huntington's disease: a diffusion tensor imaging study. Psychiatry Res. 140 (2005) 55-62
76. Rogers B.P., Morgan V.L., Newton A.T., and Gore J.C. Assessing functional connectivity in the human brain by fMRI. Magn. Reson. Imaging 25 (2007) 1347-1357
77. Rosas H.D., Goodman J., Chen Y.I., Jenkins B.G., Kennedy D.N., Makris N., Patti M., Seidman L.J., Beal M.F., and Koroshetz W.J. Striatal volume loss in HD as measured by MRI and the influence of CAG repeat. Neurology 57 (2001) 1025-1028
78. Rosas H.D., Liu A.K., Hersch S., Glessner M., Ferrante R.J., Salat D.H., van der Kouwe A., Jenkins B.G., Dale A.M., and Fischl B. Regional and progressive thinning of the cortical ribbon in Huntington's disease. Neurology 58 (2002) 695-701
79. Rosas H.D., Koroshetz W.J., Chen Y.I., Skeuse C., Vangel M., Cudkowicz M.E., Caplan K., Marek K., Seidman L.J., Makris N., Jenkins B.G., and Goldstein J.M. Evidence for more widespread cerebral pathology in early HD: an MRI-based morphometric analysis. Neurology 60 (2003) 1615-1620
80. Rosas H.D., Feigin A.S., and Hersch S.M. Using advances in neuroimaging to detect, understand, and monitor disease progression in Huntington's disease. NeuroRx 1 (2004) 263-272
81. Rosas H.D., Hevelone N.D., Zaleta A.K., Greve D.N., Salat D.H., and Fischl B. Regional cortical thinning in preclinical Huntington disease and its relationship to cognition. Neurology 65 (2005) 745-747
82. Rosas H.D., Tuch D.S., Hevelone N.D., Zaleta A.K., Vangel M., Hersch S.M., and Salat D.H. Diffusion tensor imaging in preclinical and early Huntington's disease: selective white matter pathology and its relationship to clinical measures. Mov. Disord. 21 (2006) 1317-1325
83. Rosas H.D., Salat D.H., Lee S.Y., Zaleta A.K., Pappu V., Fischl B., Greve D., Hevelone N., and Hersch S.M. Cerebral cortex and the clinical expression of Huntington's disease: complexity and heterogeneity. Brain 131 (2008) 1057-1068
84. Ruocco H.H., Lopes-Cendes I., Li L.M., Santos-Silva M., and Cendes F. Striatal and extrastriatal atrophy in Huntington's disease and its relationship with length of the CAG repeat. Braz. J. Med. Biol. Res. 39 (2006) 1129-1136
85. Ruocco H.H., Bonilha L., Li L.M., Lopes-Cendes I., and Cendes F. Longitudinal analysis of regional grey matter loss in Huntington disease: effects of the length of the expanded CAG repeat. J. Neurol. Neurosurg. Psychiatry 79 (2008) 130-135
86. Saft, C., Schuttke, A., Beste, C., Andrich, J., Heindel W., Pfleiderer, B. in press. fMRI reveals altered auditory processing in manifest and premanifest Huntington's disease. Neuropsychologia. doi:10.1016/j.neuropsychologia.2007.12.002.
87. Sarter M., Gehring W.J., and Kozak R. More attention must be paid: the neurobiology of attentional effort. Brain Res. Rev. 51 (2006) 145-160
88. Seppi K., Schocke M.F., Mair K.J., Esterhammer R., Weirich-Schwaiger H., Utermann B., Egger K., Brenneis C., Granata R., Boesch S., Poewe W., and Wenning G.K. Diffusion-weighted imaging in Huntington's disease. Mov. Disord. 21 (2006) 1043-1047
89. Shanks M.F., McGeown W.J., Forbes-McKay K.E., Waiter G.D., Ries M., and Venneri A. Regional brain activity after prolonged cholinergic enhancement in early Alzheimer's disease. Magn. Reson. Imaging 25 (2007) 848-859
90. Smith S.M., Jenkinson M., Johansen-Berg H., Rueckert D., Nichols T.E., Mackay C.E., Watkins K.E., Ciccarelli O., Cader M.Z., Matthews P.M., and Behrens T.E. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31 (2006) 1487-1505
91. Smith S.M., Johansen-Berg H., Jenkinson M., Rueckert D., Nichols T.E., Miller K.L., Robson M.D., Jones D.K., Klein J.C., Bartsch A.J., and Behrens T.E. Acquisition and voxelwise analysis of multi-subject diffusion data with tract-based spatial statistics. Nat. Protoc. 2 (2007) 499-503
92. Sotrel A., Williams R.S., Kaufman W.E., and Myers R.H. Evidence for neuronal degeneration and dendritic plasticity in cortical pyramidal neurons in Huntington's disease: a quantitative Golgi study. Neurology 43 (1993) 2088-2096
93. Starkstein S.E., Brandt J., Bylsma F., Peyser C., Folstein M., and Folstein S.E. Neuropsychological correlates of brain atrophy in Huntington's disease: a magnetic resonance imaging study. Neuroradiology 34 (1992) 487-489
94. Sun F.T., Miller L.M., and D'Esposito M. Measuring interregional functional connectivity using coherence and partial coherence analyses of fMRI data. Neuroimage 21 (2004) 647-658
95. Sweet L.H., Rao S.M., Primeau M., Durgerian S., and Cohen R.A. Functional magnetic resonance imaging response to increased verbal working memory demands among patients with multiple sclerosis. Hum. Brain Mapp. 27 (2006) 28-36
96. The Huntington's Disease Collaborative Research Group. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72 (1993) 971-983
97. Thieben M.J., Duggins A.J., Good C.D., Gomes L., Mahant N., Richards F., McCusker E., and Frackowiak R.S. The distribution of structural neuropathology in preclinical Huntington's disease. Brain 125 (2002) 1815-1828
98. Thiruvady D.R., Georgiou-Karistianis N., Egan G.F., Ray S., Sritharan A., Farrow M., Churchyard A., Chua P., Bradshaw J.L., Brawn T.L., and Cunnington R. Functional connectivity of the prefrontal cortex in Huntington's disease. J. Neurol. Neurosurg. Psychiatry 78 (2007) 127-133
99. Tomasi D., Ernst T., Caparelli E.C., and Chang L. Practice-induced changes of brain function during visual attention: a parametric fMRI study at 4 Tesla. Neuroimage 23 (2004) 1414-1421
100. Vonsattel J.P., Myers R.H., Stevens T.J., Ferrante R.J., Bird E.D., and Richardson Jr. E.P. Neuropathological classification of Huntington's disease. J. Neuropathol. Exp. Neurol. 44 (1985) 559-577
101. Wolf R.C., Vasic N., Schonfeldt-Lecuona C., Landwehrmeyer G.B., and Ecker D. Dorsolateral prefrontal cortex dysfunction in preclinical Huntington's disease: evidence from event-related fMRI. Brain 130 (2007) 2845-2857
102. Zimbelman J.L., Paulsen J.S., Mikos A., Reynolds N.C., Hoffmann R.G., and Rao S.M. fMRI detection of early neural dysfunction in preclinical Huntington's disease. J. Int. Neuropsychol. Soc. 13 (2007) 758-769