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      Mapping track density changes in nigrostriatal and extranigral pathways in Parkinson's disease

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        a , b , a , b , a , a , a , c , * , 1 , b , d , 1
      Neuroimage
      Academic Press
      18F-DOPA, [18F]-l-dihydroxyphenylalanine, APM, average pathlength map, BA, Brodmann area, DA, dopamine, DTI, diffusion tensor imaging, DW, diffusion-weighted, DWI, diffusion-weighted imaging, FA, fractional anisotropy, FDG, 18Fluorodeoxyglucose, FLASH, fast low-angle shot, FOD, fiber orientation distribution, IFO, inferior fronto-occipital fasciculus, ILF, inferior longitudinal fasciculus, LC, locus coeruleus, LEDD, levodopa equivalent daily dose, MD, mean diffusivity, MT, magnetization transfer, NSP, nigrostriatal pathway, PD, proton density, PDQ, Parkinson's disease questionnaire, PET, positron emission tomography, SCP, superior cerebellar peduncle, SLF, superior longitudinal fasciculus, SN, substantia nigra, TDI, track density imaging, TPM, total pathlength map, UPDRS, Unified Parkinson's Disease Rating Scale, VTA, ventral tegmental area, Parkinson's disease, Tractography, Diffusion, White matter, Substantia nigra

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          Abstract

          In Parkinson's disease (PD) the demonstration of neuropathological disturbances in nigrostriatal and extranigral brain pathways using magnetic resonance imaging remains a challenge. Here, we applied a novel diffusion-weighted imaging approach—track density imaging (TDI).

          Twenty-seven non-demented Parkinson's patients (mean disease duration: 5 years, mean score on the Hoehn & Yahr scale = 1.5) were compared with 26 elderly controls matched for age, sex, and education level. Track density images were created by sampling each subject's spatially normalized fiber tracks in 1 mm isotropic intervals and counting the fibers that passed through each voxel. Whole-brain voxel-based analysis was performed and significance was assessed with permutation testing.

          Statistically significant increases in track density were found in the Parkinson's patients, relative to controls. Clusters were distributed in disease-relevant areas including motor, cognitive, and limbic networks. From the lower medulla to the diencephalon and striatum, clusters encompassed the known location of the locus coeruleus and pedunculopontine nucleus in the pons, and from the substantia nigra up to medial aspects of the posterior putamen, bilaterally.

          The results identified in brainstem and nigrostriatal pathways show a large overlap with the known distribution of neuropathological changes in non-demented PD patients. Our results also support an early involvement of limbic and cognitive networks in Parkinson's disease.

          Highlights

          • First whole-brain probabilistic tractography study in Parkinson's disease

          • High quality diffusion-weighted images (120 gradient directions, b = 2500 s/mm 2)

          • Voxel-based group analysis comparing early-stage patients and controls

          • Abnormal reconstructed track density in the nigrostriatal pathway and brainstem

          • Track density also increased in limbic and cognitive circuits.

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          Most cited references63

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          Unified segmentation

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            Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications.

            Autografting of dopamine-producing adrenal medullary tissue to the striatal region of the brain is now being attempted in patients with Parkinson's disease. Since the success of this neurosurgical approach to dopamine-replacement therapy may depend on the selection of the most appropriate subregion of the striatum for implantation, we examined the pattern and degree of dopamine loss in striatum obtained at autopsy from eight patients with idiopathic Parkinson's disease. We found that in the putamen there was a nearly complete depletion of dopamine in all subdivisions, with the greatest reduction in the caudal portions (less than 1 percent of the dopamine remaining). In the caudate nucleus, the only subdivision with severe dopamine reduction was the most dorsal rostral part (4 percent of the dopamine remaining); the other subdivisions still had substantial levels of dopamine (up to approximately 40 percent of control levels). We propose that the motor deficits that are a constant and characteristic feature of idiopathic Parkinson's disease are for the most part a consequence of dopamine loss in the putamen, and that the dopamine-related caudate deficits (in "higher" cognitive functions) are, if present, less marked or restricted to discrete functions only. We conclude that the putamen--particularly its caudal portions--may be the most appropriate site for intrastriatal application of dopamine-producing autografts in patients with idiopathic Parkinson's disease.
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              The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson's disease.

              To achieve accuracy in studying the patterns of loss of midbrain dopamine-containing neurons in Parkinson's disease, we used compartmental patterns of calbindin D(28K) immunostaining to subdivide the substantia nigra with landmarks independent of the degenerative process. Within the substantia nigra pars compacta, we identified dopamine-containing neurons in the calbindin-rich regions ('matrix') and in five calbindin-poor pockets ('nigrosomes') defined by analysis of the three-dimensional networks formed by the calbindin-poor zones. These zones were recognizable in all of the brains, despite severe loss of dopamine-containing neurons. The degree of loss of dopamine-containing neurons in the substantia nigra pars compacta was related to the duration of the disease, and the cell loss followed a strict order. The degree of neuronal loss was significantly higher in the nigrosomes than in the matrix. Depletion was maximum (98%) in the main pocket (nigrosome 1), located in the caudal and mediolateral part of the substantia nigra pars compacta. Progressively less cell loss was detectable in more medial and more rostral nigrosomes, following the stereotyped order of nigrosome 1 > nigrosome 2 > nigrosome 4 > nigrosome 3 > nigrosome 5. A parallel, but lesser, caudorostral gradient of cell loss was observed for dopamine-containing neurons included in the matrix. This pattern of neuronal loss was consistent from one parkinsonian substantia nigra pars compacta to another. The spatiotemporal progression of neuronal loss related to disease duration can thus be drawn in the substantia nigra pars compacta for each Parkinson's disease patient: depletion begins in the main pocket (nigrosome 1) and then spreads to other nigrosomes and the matrix along rostral, medial and dorsal axes of progression.
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                Author and article information

                Contributors
                Journal
                Neuroimage
                Neuroimage
                Neuroimage
                Academic Press
                1053-8119
                1095-9572
                01 October 2014
                01 October 2014
                : 99
                : 100
                : 498-508
                Affiliations
                [a ]Cyclotron Research Centre, University of Liège, Liège, Belgium
                [b ]MoVeRe Group, Cyclotron Research Centre, University of Liège, Liège, Belgium
                [c ]Department of Electrical Engineering and Computer Science, University of Liège, Liège, Belgium
                [d ]Department of Neurology, University of Liège, Liège, Belgium
                Author notes
                [* ]Corresponding author at: Cyclotron Research Centre, Allée du 6 août n° 8, Sart Tilman B30, University of Liège, 4000 Liège, Belgium. Fax: + 32 4 366 29 46. c.phillips@ 123456ulg.ac.be
                [1]

                These authors contributed equally to this work.

                Article
                S1053-8119(14)00510-2
                10.1016/j.neuroimage.2014.06.033
                4121087
                24956065
                590fdca5-a17c-4ebb-9e91-77c4fab5aa34
                © 2014 Elsevier Inc. All rights reserved.
                History
                : 13 June 2014
                Categories
                Article

                Neurosciences
                18f-dopa, [18f]-l-dihydroxyphenylalanine,apm, average pathlength map,ba, brodmann area,da, dopamine,dti, diffusion tensor imaging,dw, diffusion-weighted,dwi, diffusion-weighted imaging,fa, fractional anisotropy,fdg, 18fluorodeoxyglucose,flash, fast low-angle shot,fod, fiber orientation distribution,ifo, inferior fronto-occipital fasciculus,ilf, inferior longitudinal fasciculus,lc, locus coeruleus,ledd, levodopa equivalent daily dose,md, mean diffusivity,mt, magnetization transfer,nsp, nigrostriatal pathway,pd, proton density,pdq, parkinson's disease questionnaire,pet, positron emission tomography,scp, superior cerebellar peduncle,slf, superior longitudinal fasciculus,sn, substantia nigra,tdi, track density imaging,tpm, total pathlength map,updrs, unified parkinson's disease rating scale,vta, ventral tegmental area,parkinson's disease,tractography,diffusion,white matter,substantia nigra

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