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Imaging changes associated with cognitive abnormalities in Parkinson’s disease

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Abstract

The current study investigates both gray and white matter changes in non-demented Parkinson’s disease (PD) patients with varying degrees of mild cognitive deficits and elucidates the relationships between the structural changes and clinical sequelae of PD. Twenty-six PD patients and 15 healthy controls (HCs) were enrolled in the study. Participants underwent T1-weighted and diffusion tensor imaging (DTI) scans. Their cognition was assessed using a neuropsychological battery. Compared with HCs, PD patients showed significant cortical thinning in sensorimotor (left pre- and postcentral gyri) and cognitive (left dorsolateral superior frontal gyrus [DLSFG]) regions. The DLSFG cortical thinning correlated with executive and global cognitive impairment in PD patients. PD patients showed white matter abnormalities as well, primarily in bilateral frontal and temporal regions, which also correlated with executive and global cognitive impairment. These results seem to suggest that both gray and white matter changes in the frontal regions may constitute an early pathological substrate of cognitive impairment of PD providing a sensitive biomarker for brain changes in PD.

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References

  • Acosta-Cabronero J, Williams GB, Pengas G, Nestor PJ (2010) Absolute diffusivities define the landscape of white matter degeneration in Alzheimer’s disease. Brain 133:529–539

    PubMed  Google Scholar 

  • Agosta F, Canu E, Stefanova E, Sarro L, Tomic A, Spica V, Comi G, Kostic VS, Filippi M (2013a) Mild cognitive impairment in Parkinson’s disease is associated with a distributed pattern of brain white matter damage. Hum Brain Mapp. doi:10.1002/hbm.22302

    Google Scholar 

  • Agosta F, Canu E, Stojkovic T, Pievani M, Tomic A, Sarro L, Dragasevic N, Copetti M, Comi G, Kostic VS, Filippi M (2013b) The topography of brain damage at different stages of Parkinson’s disease. Hum Brain Mapp 34:2798–2807

    PubMed  Google Scholar 

  • Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357–381

    CAS  PubMed  Google Scholar 

  • Andersson JLR, Jenkinson M, Smith S (2007a). Non-linear optimisation. FMRIB technical report TR07JA1 from www.fmrib.ox.ac.uk/analysis/techrep

  • Andersson JLR, Jenkinson M, Smith S (2007b) Non-linear registration, aka Spatial normalisation FMRIB technical report TR07JA2 from www.fmrib.ox.ac.uk/analysis/techrep

  • Baggio HC, Segura B, Ibarretxe-Bilbao N, Valldeoriola F, Marti MJ, Compta Y, Tolosa E, Junque C (2012) Structural correlates of facial emotion recognition deficits in Parkinson’s disease patients. Neuropsychologia 50:2121–2128

    CAS  PubMed  Google Scholar 

  • Barnum CJ, Tansey MG (2012) Neuroinflammation and non-motor symptoms: the dark passenger of Parkinson’s disease? Curr Neurol Neurosci Rep 12:350–358

    CAS  PubMed  Google Scholar 

  • Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J (1961) An inventory for measuring depression. Arch Gen Psychiatry 4:561–571

    CAS  PubMed  Google Scholar 

  • Benton AB, Sivan KD, Hamsher NR, Varney NR, Spreen O (1994) Contributions to neuropsychological assessment-2nd Edition. Psycholog Assess Resour, Orland

    Google Scholar 

  • Beyer MK, Janvin CC, Larsen JP, Aarsland D (2007) A magnetic resonance imaging study of patients with Parkinson’s disease with mild cognitive impairment and dementia using voxel-based morphometry. J Neurol Neurosurg Psychiatry 78:254–259

    PubMed Central  PubMed  Google Scholar 

  • Biundo R, Formento-Dojo P, Facchini S, Vallelunga A, Ghezzo L, Foscolo L, Meneghello F, Antonini A (2011) Brain volume changes in Parkinson’s disease and their relationship with cognitive and behavioural abnormalities. J Neurol Sci 310:64–69

    PubMed  Google Scholar 

  • Bonnet AM, Jutras MF, Czernecki V, Corvol JC, Vidailhet M (2012) Nonmotor symptoms in Parkinson’s disease in 2012: relevant clinical aspects. Parkinsons Dis. doi:10.1155/2012/198316

    PubMed Central  PubMed  Google Scholar 

  • Braak H, Braak E (2000) Pathoanatomy of Parkinson’s disease. J Neurol 247 Suppl 2:3–10

    Google Scholar 

  • Braak H, Braak E, Yilmazer D, de Vos RA, Jansen EN, Bohl J, Jellinger K (1994) Amygdala pathology in Parkinson’s disease. Acta Neuropathol 88:493–500

    CAS  PubMed  Google Scholar 

  • Braak H, Braak E, Yilmazer D, Schultz C, de Vos RA, Jansen EN (1995) Nigral and extranigral pathology in Parkinson’s disease. J Neural Transm Suppl 46:15–31

    CAS  PubMed  Google Scholar 

  • Braak H, de Vos RA, Jansen EN, Bratzke H, Braak E (1998) Neuropathological hallmarks of Alzheimer’s and Parkinson’s diseases. Prog Brain Res 117:267–285

    CAS  PubMed  Google Scholar 

  • Braak H, Ghebremedhin E, Rub U, Bratzke H, Del Tredici K (2004) Stages in the development of Parkinson’s disease-related pathology. Cell Tissue Res 318:121–134

    PubMed  Google Scholar 

  • Braak H, Bohl JR, Muller CM, Rub U, de Vos RA, Del Tredici K (2006) Stanley Fahn lecture 2005: the staging procedure for the inclusion body pathology associated with sporadic Parkinson’s disease reconsidered. Mov Disord 21:2042–2051

    PubMed  Google Scholar 

  • Brenneis C, Seppi K, Schocke MF, Muller J, Luginger E, Bosch S, Loscher WN, Buchel C, Poewe W, Wenning GK (2003) Voxel-based morphometry detects cortical atrophy in the Parkinson variant of multiple system atrophy. Mov Disord 18:1132–1138

    PubMed  Google Scholar 

  • Burton EJ, McKeith IG, Burn DJ, Williams ED, O’Brien JT (2004) Cerebral atrophy in Parkinson’s disease with and without dementia: a comparison with Alzheimer’s disease, dementia with Lewy bodies and controls. Brain 127:791–800

    PubMed  Google Scholar 

  • Camicioli R, Gee M, Bouchard TP, Fisher NJ, Hanstock CC, Emery DJ, Martin WR (2009) Voxel-based morphometry reveals extra-nigral atrophy patterns associated with dopamine refractory cognitive and motor impairment in parkinsonism. Parkinsonism Relat Disord 15:187–195

    PubMed  Google Scholar 

  • Chaudhuri KR, Odin P, Antonini A, Martinez-Martin P (2011) Parkinson’s disease: the non-motor issues. Parkinsonism Relat Disord 17:717–723

    PubMed  Google Scholar 

  • Christopher L, Strafella AP (2013) Neuroimaging of brain changes associated with cognitive impairment in Parkinson’s disease. J neuropsychol 7:225–240

    PubMed Central  PubMed  Google Scholar 

  • Cochrane CJ, Ebmeier KP (2013) Diffusion tensor imaging in parkinsonian syndromes: a systematic review and meta-analysis. Neurology 80:857–864

    PubMed Central  PubMed  Google Scholar 

  • Compta Y, Ibarretxe-Bilbao N, Pereira JB, Junque C, Bargallo N, Tolosa E, Valldeoriola F, Munoz E, Camara A, Buongiorno M, Marti MJ (2012) Grey matter volume correlates of cerebrospinal markers of Alzheimer-pathology in Parkinson’s disease and related dementia. Parkinsonism Relat Disord 18:941–947

    PubMed  Google Scholar 

  • Compta Y, Pereira JB, Rios J, Ibarretxe-Bilbao N, Junque C, Bargallo N, Camara A, Buongiorno M, Fernandez M, Pont-Sunyer C, Marti MJ (2013) Combined dementia-risk biomarkers in Parkinson’s disease: a prospective longitudinal study. Parkinsonism Relat Disord 19:717–724

    PubMed  Google Scholar 

  • Corbetta M, Patel G, Shulman GL (2008) The reorienting system of the human brain: from environment to theory of mind. Neuron 58:306–324

    CAS  PubMed Central  PubMed  Google Scholar 

  • Courtney SM, Petit L, Maisog JM, Ungerleider LG, Haxby JV (1998) An area specialized for spatial working memory in human frontal cortex. Science 279:1347–1351

    CAS  PubMed  Google Scholar 

  • Cubon VA, Putukian M, Boyer C, Dettwiler A (2011) A diffusion tensor imaging study on the white matter skeleton in individuals with sports-related concussion. J Neurotrauma 28:189–201

    PubMed Central  PubMed  Google Scholar 

  • Dale AM, Sereno MI (1993) Improved localizadon of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach. J Cogn Neurosci 5:162–176

    CAS  PubMed  Google Scholar 

  • Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179–194

    CAS  PubMed  Google Scholar 

  • Defer GL, Widner H, Marie RM, Remy P, Levivier M (1999) Core assessment program for surgical interventional therapies in Parkinson’s disease (CAPSIT-PD). Mov Disord 14:572–584

    CAS  PubMed  Google Scholar 

  • Delis DC, Kaplan E, Kramer JH (2001) Examiner’s manual for the Delis-Kaplan executive function system. The Psychological Corporation, San Antonio

    Google Scholar 

  • Deng B, Zhang Y, Wang L, Peng K, Han L, Nie K, Yang H, Zhang L, Wang J (2013) Diffusion tensor imaging reveals white matter changes associated with cognitive status in patients with Parkinson’s disease. Am J Alzheimers Dis Other Demen 28:154–164

    PubMed  Google Scholar 

  • Desgranges B, Baron JC, Eustache F (1998) The functional neuroanatomy of episodic memory: the role of the frontal lobes, the hippocampal formation, and other areas. Neuroimage 8:198–213

    CAS  PubMed  Google Scholar 

  • du Boisgueheneuc F, Levy R, Volle E, Seassau M, Duffau H, Kinkingnehun S, Samson Y, Zhang S, Dubois B (2006) Functions of the left superior frontal gyrus in humans: a lesion study. Brain 129:3315–3328

    PubMed  Google Scholar 

  • Evans AH, Katzenschlager R, Paviour D, O’Sullivan JD, Appel S, Lawrence AD, Lees AJ (2004) Punding in Parkinson’s disease: its relation to the dopamine dysregulation syndrome. Mov Disord 19:397–405

    PubMed  Google Scholar 

  • Feldmann A, Illes Z, Kosztolanyi P, Illes E, Mike A, Kover F, Balas I, Kovacs N, Nagy F (2008) Morphometric changes of gray matter in Parkinson’s disease with depression: a voxel-based morphometry study. Mov Disord 23:42–46

    PubMed  Google Scholar 

  • Ferrer I, Martinez A, Blanco R, Dalfo E, Carmona M (2011) Neuropathology of sporadic Parkinson disease before the appearance of Parkinsonism: preclinical Parkinson disease. J Neural Transm 118:821–839

    PubMed  Google Scholar 

  • Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97:11050–11055

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fischl B, Liu A, Dale AM (2001) Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans Med Imaging 20:70–80

    CAS  PubMed  Google Scholar 

  • Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33:341–355

    CAS  PubMed  Google Scholar 

  • Foley P, Riederer P (1999) Pathogenesis and preclinical course of Parkinson’s disease. J Neural Transm Suppl 56:31–74

    CAS  PubMed  Google Scholar 

  • Gallagher C, Bell B, Bendlin B, Palotti M, Okonkwo O, Sodhi A, Wong R, Buyan-Dent L, Johnson S, Wilette A, Harding S, Ninman N, Kastman E, Alexander A (2013) White matter microstructural integrity and executive function in Parkinson’s disease. J Int Neuropsychol Soc 19:349–354

    PubMed Central  PubMed  Google Scholar 

  • Gattellaro G, Minati L, Grisoli M, Mariani C, Carella F, Osio M, Ciceri E, Albanese A, Bruzzone MG (2009) White matter involvement in idiopathic Parkinson disease: a diffusion tensor imaging study. AJNR Am J Neuroradiol 30:1222–1226

    CAS  PubMed  Google Scholar 

  • Goldman JG, Stebbins GT, Bernard B, Stoub TR, Goetz CG, deToledo-Morrell L (2012) Entorhinal cortex atrophy differentiates Parkinson’s disease patients with and without dementia. Mov Disord 27:727–734

    PubMed Central  PubMed  Google Scholar 

  • Hanganu A, Bedetti C, Jubault T, Gagnon JF, Mejia-Constain B, Degroot C, Lafontaine AL, Chouinard S, Monchi O (2013) Mild cognitive impairment in patients with Parkinson’s disease is associated with increased cortical degeneration. Mov Disord 28:1360–1369

    PubMed  Google Scholar 

  • Hattori T, Orimo S, Aoki S, Ito K, Abe O, Amano A, Sato R, Sakai K, Mizusawa H (2012) Cognitive status correlates with white matter alteration in Parkinson’s disease. Hum Brain Mapp 33:727–739

    PubMed  Google Scholar 

  • Hu MT, White SJ, Chaudhuri KR, Morris RG, Bydder GM, Brooks DJ (2001) Correlating rates of cerebral atrophy in Parkinson’s disease with measures of cognitive decline. J Neural Transm 108:571–580

    CAS  PubMed  Google Scholar 

  • Hua K, Zhang J, Wakana S, Jiang H, Li X, Reich DS, Calabresi PA, Pekar JJ, van Zijl PC, Mori S (2008) Tract probability maps in stereotaxic spaces: analyses of white matter anatomy and tract-specific quantification. Neuroimage 39:336–347

    PubMed Central  PubMed  Google Scholar 

  • Ibarretxe-Bilbao N, Junque C, Tolosa E, Marti MJ, Valldeoriola F, Bargallo N, Zarei M (2009) Neuroanatomical correlates of impaired decision-making and facial emotion recognition in early Parkinson’s disease. Eur J Neurosci 30:1162–1171

    PubMed  Google Scholar 

  • Ibarretxe-Bilbao N, Ramirez-Ruiz B, Junque C, Marti MJ, Valldeoriola F, Bargallo N, Juanes S, Tolosa E (2010) Differential progression of brain atrophy in Parkinson’s disease with and without visual hallucinations. J Neurol Neurosurg Psychiatry 81:650–657

    PubMed  Google Scholar 

  • Ibarretxe-Bilbao N, Junque C, Segura B, Baggio HC, Marti MJ, Valldeoriola F, Bargallo N, Tolosa E (2012) Progression of cortical thinning in early Parkinson’s disease. Mov Disord 27:1746–1753

    PubMed  Google Scholar 

  • Janvin CC, Larsen JP, Aarsland D, Hugdahl K (2006) Subtyptes of mild cognitive impairment in Parkinson’s disease: progression to dementia. Mov Disord 21:1343–1349

    PubMed  Google Scholar 

  • Jellinger KA (1991) Pathology of Parkinson’s disease. Changes other than the nigrostriatal pathway. Mol Chem Neuropathol 14:153–197

    CAS  PubMed  Google Scholar 

  • Jellinger KA (2012) Neurobiology of cognitive impairment in Parkinson’s disease. Expert Rev Neurother 12:1451–1466

    CAS  PubMed  Google Scholar 

  • Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143–156

    CAS  PubMed  Google Scholar 

  • Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825–841

    PubMed  Google Scholar 

  • Jubault T, Gagnon JF, Karama S, Ptito A, Lafontaine AL, Evans AC, Monchi O (2011) Patterns of cortical thickness and surface area in early Parkinson’s disease. Neuroimage 55:462–467

    PubMed  Google Scholar 

  • Kehagia AA, Barker RA, Robbins TW (2010) Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson’s disease. Lancet Neurol 9:1200–1213

    PubMed  Google Scholar 

  • Kim HJ, Kim SJ, Kim HS, Choi CG, Kim N, Han S, Jang EH, Chung SJ, Lee CS (2013) Alterations of mean diffusivity in brain white matter and deep gray matter in Parkinson’s disease. Neurosci Lett 550:64–68

    CAS  PubMed  Google Scholar 

  • Kostic VS, Agosta F, Petrovic I, Galantucci S, Spica V, Jecmenica-Lukic M, Filippi M (2010) Regional patterns of brain tissue loss associated with depression in Parkinson disease. Neurology 75:857–863

    CAS  PubMed  Google Scholar 

  • Langston JW, Widner H, Goetz CG, Brooks D, Fahn S, Freeman T, Watts R (1992) Core assessment program for intracerebral transplantations (CAPIT). Mov Disord 7:2–13

    CAS  PubMed  Google Scholar 

  • Levy R, Goldman-Rakic PS (2000) Segregation of working memory functions within the dorsolateral prefrontal cortex. Exp Brain Res 133:23–32

    CAS  PubMed  Google Scholar 

  • Litvan I, Aarsland D, Adler CH, Goldman JG, Kulisevsky J, Mollenhauer B, Rodriguez-Oroz MC, Tröster AI, Weintraub D (2011) MDS task force on mild cognitive impairment in Parkinson’s disease: critical review of PD-MCI. Mov Disord 26:1814–1824

    PubMed Central  PubMed  Google Scholar 

  • Litvan I, Goldman JG, Troster AI, Schmand BA, Weintraub D, Petersen RC, Mollenhauer B, Adler CH, Marder K, Williams-Gray CH, Aarsland D, Kulisevsky J, Rodriguez-Oroz MC, Burn DJ, Barker RA, Emre M (2012) Diagnostic criteria for mild cognitive impairment in Parkinson’s disease: Movement Disorder Society Task Force guidelines. Mov Disord 27:349–356

    PubMed Central  PubMed  Google Scholar 

  • Lyoo CH, Ryu YH, Lee MS (2011) Cerebral cortical areas in which thickness correlates with severity of motor deficits of Parkinson’s disease. J Neurol 258:1871–1876

    PubMed  Google Scholar 

  • MacDonald AA, Monchi O, Seerqobin KN, Ganjavi H, Tamjeedi R, MacDonald PA (2013) Parkinson’s disease duration determines effect of dopaminergic therapy on ventral striatum function. Mov Disord 28:153–1560

    CAS  PubMed  Google Scholar 

  • Matsui H, Nishinaka K, Oda M, Niikawa H, Komatsu K, Kubori T, Udaka F (2007) Depression in Parkinson’s disease. Diffusion tensor imaging study. J Neurol 254:1170–1173

    PubMed  Google Scholar 

  • Melzer TR, Watts R, MacAskill MR, Pitcher TL, Livingston L, Keenan RJ, Dalrymple-Alford JC, Anderson TJ (2012) Grey matter atrophy in cognitively impaired Parkinson’s disease. J Neurol Neurosurg Psychiatry 83:188–194

    PubMed  Google Scholar 

  • Melzer TR, Watts R, Macaskill MR, Pitcher TL, Livingston L, Keenan RJ, Dalrymple-Alford JC, Anderson TJ (2013) White matter microstructure deteriorates across cognitive stages in Parkinson disease. Neurology 80:1841–1849

    CAS  PubMed  Google Scholar 

  • Mori S, Wakana S, Nagae-Poetscher LM, van Zijl PCM (2005) MRI Atlas of Human White Matter. Elsevier, Amsterdam

    Google Scholar 

  • Morrison JH, Hof PR (1997) Life and death of neurons in the aging brain. Science 278:412–419

    CAS  PubMed  Google Scholar 

  • Nagano-Saito A, Habak C, Mejia-Constain B, Degroot C, Monetta L, Jubault T, Bedetti C, Lafontaine AL, Chouinard S, Soland V, Ptito A, Strafella AP, Monchi O (2013) Effect of mild cognitive impairment on the patterns of neural activity in early Parkinson’s disease. Neurobiol Aging 35:223–231

    PubMed  Google Scholar 

  • Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H (2005) The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53:695–699

    PubMed  Google Scholar 

  • Owen AM (2004) Cognitive dysfunction in Parkinson’s disease: the role of frontostriatal circuitry. Neuroscientist 10:525–537

    PubMed  Google Scholar 

  • Owen AM, Stern CE, Look RB, Tracey I, Rosen BR, Petrides M (1998) Functional organization of spatial and nonspatial working memory processing within the human lateral frontal cortex. Proc Natl Acad Sci USA 95:7721–7726

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pagonabarraga J, Kulisevsky J (2012) Cognitive impairment and dementia in Parkinson’s disease. Neurobiol Dis 46:590–596

    PubMed  Google Scholar 

  • Pan PL, Song W, Shang HF (2012) Voxel-wise meta-analysis of gray matter abnormalities in idiopathic Parkinson’s disease. Eur J Neurol 19:199–206

    CAS  PubMed  Google Scholar 

  • Pellicano C, Assogna F, Piras F, Caltagirone C, Pontieri FE, Spalletta G (2012) Regional cortical thickness and cognitive functions in non-demented Parkinson’s disease patients: a pilot study. Eur J Neurol 19:172–175

    CAS  PubMed  Google Scholar 

  • Pereira JB, Ibarretxe-Bilbao N, Marti MJ, Compta Y, Junque C, Bargallo N, Tolosa E (2012) Assessment of cortical degeneration in patients with Parkinson’s disease by voxel-based morphometry, cortical folding, and cortical thickness. Hum Brain Mapp 33:2521–2534

    PubMed  Google Scholar 

  • Rae CL, Correia MM, Altena E, Hughes LE, Barker RA, Rowe JB (2012) White matter pathology in Parkinson’s disease: the effect of imaging protocol differences and relevance to executive function. Neuroimage 62:1675–1684

    PubMed Central  PubMed  Google Scholar 

  • Ramirez-Ruiz B, Marti MJ, Tolosa E, Gimenez M, Bargallo N, Valldeoriola F, Junque C (2007) Cerebral atrophy in Parkinson’s disease patients with visual hallucinations. Eur J Neurol 14:750–756

    CAS  PubMed  Google Scholar 

  • Rosenberg-Katz K, Herman T, Jacob Y, Giladi N, Hendler T, Hausdorff JM (2013) Gray matter atrophy distinguishes between Parkinson disease motor subtypes. Neurology 80:1476–1484

    PubMed Central  PubMed  Google Scholar 

  • Ryterska A, Jahanshahi M, Osman M (2013) What are people with Parkinson’s disease really impaired on when it comes to making decisions? A meta-analysis of the evidence. Neurosci Biobehav Rev 37:2836–2846

    PubMed  Google Scholar 

  • Segonne F, Pacheco J, Fischl B (2007) Geometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Trans Med Imaging 26:518–529

    PubMed  Google Scholar 

  • Shenton ME, Hamoda HM, Schneiderman JS, Bouix S, Pasternak O, Rathi Y, Vu MA, Purohit MP, Helmer K, Koerte I, Lin AP, Westin CF, Kikinis R, Kubicki M, Stern RA, Zafonte R (2012) A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury. Brain Imaging Behav 6:137–192

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sled JG, Zijdenbos AP, Evans AC (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17:87–97

    CAS  PubMed  Google Scholar 

  • Smith SM (2002) Fast robust automated brain extraction. Hum Brain Mapp 17:143–155

    PubMed  Google Scholar 

  • Smith SM, Nichols TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44:83–98

    PubMed  Google Scholar 

  • Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 Suppl 1:208–219

    Google Scholar 

  • Song SK, Lee JE, Park HJ, Sohn YH, Lee JD, Lee PH (2011) The pattern of cortical atrophy in patients with Parkinson’s disease according to cognitive status. Mov Disord 26:289–296

    PubMed  Google Scholar 

  • Theilmann RJ, Reed JD, Song DD, Huang MX, Lee RR, Litvan I, Harrington DL (2013) White-matter changes correlate with cognitive functioning in Parkinson’s disease. Front Neurol 4:37

    PubMed Central  PubMed  Google Scholar 

  • Tinaz S, Courtney MG, Stern CE (2011) Focal cortical and subcortical atrophy in early Parkinson’s disease. Mov Disord 26:436–441

    PubMed  Google Scholar 

  • Tison F, Dartigues JF, Auriacombe S, Letenneur L, Boller F, Alperovitch A (1995) Dementia in Parkinson’s disease: a population-based study in ambulatory and institutionalized individuals. Neurology 45:705–708

    CAS  PubMed  Google Scholar 

  • Wakana S, Caprihan A, Panzenboeck MM, Fallon JH, Perry M, Gollub RL, Hua K, Zhang J, Jiang H, Dubey P, Blitz A, van Zijl P, Mori S (2007) Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage 36:630–644

    PubMed Central  PubMed  Google Scholar 

  • Wattendorf E, Welge-Lussen A, Fiedler K, Bilecen D, Wolfensberger M, Fuhr P, Hummel T, Westermann B (2009) Olfactory impairment predicts brain atrophy in Parkinson’s disease. J Neurosci 29:15410–15413

    CAS  PubMed  Google Scholar 

  • Wechsler D (1997) Manual for the Wechsler Memeory Scale, 3rd edn. The Psychological Corporation, New York

    Google Scholar 

  • Weintraub D, Doshi J, Koka D, Davatzikos C, Siderowf AD, Duda JE, Wolk DA, Moberg PJ, Xie SX, Clark CM (2011) Neurodegeneration across stages of cognitive decline in Parkinson disease. Arch Neurol 68:1562–1568

    PubMed Central  PubMed  Google Scholar 

  • Wicklund AH, Johnson N, Weintraub S (2004) Preservation of reasoning in primary progressive aphasia: further differentiation from Alzheimer’s disease and the behavioral presentation of frontotemporal dementia. J Clin Exp Neuropsychol 26:347–355

    PubMed  Google Scholar 

  • Woolrich MW, Jbabdi S, Patenaude B, Chappell M, Makni S, Behrens T, Beckmann C, Jenkinson M, Smith SM (2009) Bayesian analysis of neuroimaging data in FSL. Neuroimage 45 Suppl 1:173–186

    Google Scholar 

  • Zarei M, Ibarretxe-Bilbao N, Compta Y, Hough M, Junque C, Bargallo N, Tolosa E, Marti MJ (2013) Cortical thinning is associated with disease stages and dementia in Parkinson’s disease. J Neurol Neurosurg Psychiatry 84:875–881

    PubMed Central  PubMed  Google Scholar 

  • Zgaljardic DJ, Borod JC, Foldi NS, Mattis PJ, Gordon MF, Feigin A, Eidelberg D (2006) An examination of executive dysfunction associated with frontostriatal circuitry in Parkinson’s disease. J Clin Exp Neuropsychol 28:1127–1144

    PubMed Central  PubMed  Google Scholar 

  • Zhan W, Kang GA, Glass GA, Zhang Y, Shirley C, Millin R, Possin KL, Nezamzadeh M, Weiner MW, Marks WJ Jr, Schuff N (2012) Regional alterations of brain microstructure in Parkinson’s disease using diffusion tensor imaging. Mov Disord 27:90–97

    PubMed Central  PubMed  Google Scholar 

  • Zhang K, Yu C, Zhang Y, Wu X, Zhu C, Chan P, Li K (2011) Voxel-based analysis of diffusion tensor indices in the brain in patients with Parkinson’s disease. Eur J Radiol 77:269–273

    PubMed  Google Scholar 

  • Zheng Z, Shemmassian S, Wijekoon C, Kim W, Bookheimer SY, Pouratian N (2014) DTI correlates of distinct cognitive impairments in Parkinson’s disease. Hum Brain Mapp 35:1325–1333

    PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This study was supported by Canadian Institutes of Health Research (MOP 117891). A.P.S. is supported by the Canada Research Chair program. Yuko Koshimori was supported by a scholarship from Parkinson Society Canada.

Conflict of interest

There are no actual or potential conflicts of interest.

Author information

Authors and Affiliations

  1. Morton and Gloria Shulman Movement Disorder Unit and E.J. Safra Parkinson Disease Program, Toronto Western Hospital, UHN, University of Toronto, 399 Bathurst St, Toronto, ON, M5T 2S8, Canada

    Sarah Duff-Canning, Anthony E. Lang & Antonio P. Strafella

  2. Division of Brain, Imaging and Behaviour–Systems Neuroscience, Toronto Western Research Institute, UHN, University of Toronto, 399 Bathurst St, Toronto, ON, M5T 2S8, Canada

    Yuko Koshimori, Leigh Christopher, Kelly Aminian & Antonio P. Strafella

  3. Research Imaging Centre, Centre for Addiction and Mental Health (CAMH), University of Toronto, 250 College St, Toronto, ON, M5T 1R8, Canada

    Yuko Koshimori, Barbara Segura, Leigh Christopher, Nancy Lobaugh, Romina Mizrahi, Kelly Aminian, Sylvain Houle & Antonio P. Strafella

  4. Division of Neurosurgery, Toronto Western Hospital, UHN, University of Toronto, 399 Bathurst St, Toronto, ON, M5T 2S8, Canada

    Clement Hamani

  5. Department of Psychiatry and Clinical Psychobiology, Faculty of Medicine, University of Barcelona, Casanova 146, 08035, Barcelona, Spain

    Barbara Segura

  6. Department of Neuropsychology, Toronto Western Hospital, 399 Bathurst St, Toronto, ON, M5T 2S8, Canada

    Sarah Duff-Canning

  7. Toronto Western Hospital and Institute, CAMH-Research Imaging Centre, University of Toronto, Toronto, ON, Canada

    Antonio P. Strafella

Authors
  1. Yuko Koshimori
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  2. Barbara Segura
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  3. Leigh Christopher
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  4. Nancy Lobaugh
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  5. Sarah Duff-Canning
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  6. Romina Mizrahi
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  7. Clement Hamani
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  8. Anthony E. Lang
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  9. Kelly Aminian
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  10. Sylvain Houle
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  11. Antonio P. Strafella
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Corresponding author

Correspondence to Antonio P. Strafella.

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Koshimori, Y., Segura, B., Christopher, L. et al. Imaging changes associated with cognitive abnormalities in Parkinson’s disease. Brain Struct Funct 220, 2249–2261 (2015). https://doi.org/10.1007/s00429-014-0785-x

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  • DOI: https://doi.org/10.1007/s00429-014-0785-x

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