Multi-modal Brain MRI in Subjects with PD and iRBD
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
Grantová podpora
P41 EB015894
NIBIB NIH HHS - United States
S10 OD017974
NIH HHS - United States
UL1 TR000114
NCATS NIH HHS - United States
KL2 TR000113
NCATS NIH HHS - United States
P30 NS076408
NINDS NIH HHS - United States
P30 NS057091
NINDS NIH HHS - United States
PubMed
29311789
PubMed Central
PMC5742124
DOI
10.3389/fnins.2017.00709
Knihovny.cz E-zdroje
- Klíčová slova
- DTI, Parkinson's disease, functional connectivity, iRBD, rotating frame MRI,
- Publikační typ
- časopisecké články MeSH
Idiopathic rapid eye movement sleep behavior disorder (iRBD) is a condition that often evolves into Parkinson's disease (PD). Therefore, by monitoring iRBD it is possible to track the neurodegeneration of individuals who may progress to PD. Here we aimed at piloting the characterization of brain tissue properties in mid-brain subcortical regions of 10 healthy subjects, 8 iRBD, and 9 early-diagnosed PD. We used a battery of magnetic resonance imaging (MRI) contrasts at 3 T, including adiabatic and non-adiabatic rotating frame techniques developed by our group, along with diffusion tensor imaging (DTI) and resting-state fMRI. Adiabatic T1ρ and T2ρ, and non-adiabatic RAFF4 (Relaxation Along a Fictitious Field in the rotating frame of rank 4) were found to have lower coefficient of variations and higher sensitivity to detect group differences as compared to DTI parameters such as fractional anisotropy and mean diffusivity. Significantly longer T1ρ were observed in the amygdala of PD subjects vs. controls, along with a trend of lower functional connectivity as measured by regional homogeneity, thereby supporting the notion that amygdalar dysfunction occurs in PD. Significant abnormalities in reward networks occurred in iRBD subjects, who manifested lower network strength of the accumbens. In agreement with previous studies, significantly longer T1ρ occurred in the substantia nigra compacta of PD vs. controls, indicative of neuronal degeneration, while regional homogeneity was lower in the substantia nigra reticulata. Finally, other trend-level findings were observed, i.e., lower RAFF4 and T2ρ in the midbrain of iRBD subjects vs. controls, possibly indicating changes in non-motor features as opposed to motor function in the iRBD group. We conclude that rotating frame relaxation methods along with functional connectivity measures are valuable to characterize iRBD and PD subjects, and with proper validation in larger cohorts may provide pathological signatures of iRBD and PD.
Central European Institute of Technology Masaryk University Brno Czechia
Department of Applied Physics University of Eastern Finland Kuopio Finland
Department of Neurology University of Minnesota Minneapolis MN United States
Department of Pediatrics University of Minnesota Minneapolis MN United States
Division of Biostatistics University of Minnesota Minneapolis MN United States
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Andersson J. L., Skare S., Ashburner J. (2003). How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging. Neuroimage 20, 870–888. 10.1016/S1053-8119(03)00336-7 PubMed DOI
Andersson J. L., Sotiropoulos S. N. (2016). An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. Neuroimage 125, 1063–1078. 10.1016/j.neuroimage.2015.10.019 PubMed DOI PMC
Andronesi O. C., Bhat H., Reuter M., Mukherjee S., Caravan P., Rosen B. R. (2014). Whole brain mapping of water pools and molecular dynamics with rotating frame MR relaxation using gradient modulated low-power adiabatic pulses. Neuroimage 89, 92–109. 10.1016/j.neuroimage.2013.12.007 PubMed DOI PMC
Behzadi Y., Restom K., Liau J., Liu T. T. (2007). A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 37, 90–101. 10.1016/j.neuroimage.2007.04.042 PubMed DOI PMC
Benjamini Y., Hochberg Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300.
Boeve B. F. (2013). Idiopathic REM sleep behaviour disorder in the development of Parkinson's disease. Lancet Neurol. 12, 469–482. 10.1016/S1474-4422(13)70054-1 PubMed DOI PMC
Boeve B. F., Silber M. H., Ferman T. J., Lucas J. A., Parisi J. E. (2001). Association of REM sleep behavior disorder and neurodegenerative disease may reflect an underlying synucleinopathy. Mov. Disord. 16, 622–630. 10.1002/mds.1120 PubMed DOI
Bohnen N. I., Gedela S., Herath P., Constantine G. M., Moore R. Y. (2008). Selective hyposmia in Parkinson disease: association with hippocampal dopamine activity. Neurosci. Lett. 447, 12–16. 10.1016/j.neulet.2008.09.070 PubMed DOI PMC
Bolding M. S., Reid M. A., Avsar K. B., Roberts R. C., Gamlin P. D., Gawne T. J., et al. . (2013). Magnetic transfer contrast accurately localizes substantia nigra confirmed by histology. Biol. Psychiatry 73, 289–294. 10.1016/j.biopsych.2012.07.035 PubMed DOI PMC
Bouchard T. P., Malykhin N., Martin W. R., Hanstock C. C., Emery D. J., Fisher N. J., et al. . (2008). Age and dementia-associated atrophy predominates in the hippocampal head and amygdala in Parkinson's disease. Neurobiol. Aging 29, 1027–1039. 10.1016/j.neurobiolaging.2007.02.002 PubMed DOI
Bunzeck N., Singh-Curry V., Eckart C., Weiskopf N., Perry R. J., Bain P. G., et al. . (2013). Motor phenotype and magnetic resonance measures of basal ganglia iron levels in Parkinson's disease. Parkinsonism Relat. Disord. 19, 1136–1142. 10.1016/j.parkreldis.2013.08.011 PubMed DOI PMC
Bushnell D. M., Martin M. L. (1999). Quality of life and Parkinson's disease: translation and validation of the US Parkinson's Disease Questionnaire (PDQ-39). Qual. Life Res. 8, 345–350. 10.1023/A:1008979705027 PubMed DOI
Casula V., Nissi M. J., Podlipska J., Haapea M., Koski J. M., Saarakkala S., et al. . (2017). Elevated adiabatic T1rho and T2rho in articular cartilage are associated with cartilage and bone lesions in early osteoarthritis: a preliminary study. J. Magn. Reson. Imaging 46, 678–689. 10.1002/jmri.25616 PubMed DOI
Cox R. W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29, 162–173. 10.1006/cbmr.1996.0014 PubMed DOI
Dibble L. E., Cavanaugh J. T., Earhart G. M., Ellis T. D., Ford M. P., Foreman K. B. (2010). Charting the progression of disability in Parkinson disease: study protocol for a prospective longitudinal cohort study. BMC Neurol. 10:110. 10.1186/1471-2377-10-110 PubMed DOI PMC
Double K. L., Rowe D. B., Hayes M., Chan D. K., Blackie J., Corbett A., et al. . (2003). Identifying the pattern of olfactory deficits in parkinson disease using the brief smell identification test. Arch. Neurol. 60, 545–549. 10.1001/archneur.60.4.545 PubMed DOI
Du G., Lewis M. M., Styner M., Shaffer M. L., Sen S., Yang Q. X., et al. . (2011). Combined R2* and diffusion tensor imaging changes in the substantia nigra in Parkinson's disease. Mov. Disord. 26, 1627–1632. 10.1002/mds.23643 PubMed DOI PMC
Ellmore T. M., Castriotta R. J., Hendley K. L., Aalbers B. M., Furr-Stimming E., Hood A. J., et al. . (2013). Altered nigrostriatal and nigrocortical functional connectivity in rapid eye movement sleep behavior disorder. Sleep 36, 1885–1892. 10.5665/sleep.3222 PubMed DOI PMC
Fahn S., Elton R. (1987). Unified parkinson's disease rating scale, in Recent Developments in Parkinson's Disease, Vol. 2, eds Fahn S., Marsden C. D., Calne D. B., Goldstein M. (Florham Park, NJ: Macmillan Healthcare Information; ), 153–163.
Feldmann A., Illes Z., Kosztolanyi P., Illes E., Mike A., Kover F., et al. . (2008). Morphometric changes of gray matter in Parkinson's disease with depression: a voxel-based morphometry study. Mov. Disord. 23, 42–46. 10.1002/mds.21765 PubMed DOI
Fischl B., Salat D. H., Busa E., Albert M., Dieterich M., Haselgrove C., et al. . (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341–355. 10.1016/S0896-6273(02)00569-X PubMed DOI
Gagnon J. F., Postuma R. B., Joncas S., Desjardins C., Latreille V. (2010). The Montreal Cognitive Assessment: a screening tool for mild cognitive impairment in REM sleep behavior disorder. Mov. Disord. 25, 936–940. 10.1002/mds.23079 PubMed DOI
Goetz C. G., Fahn S., Martinez-Martin P., Poewe W., Sampaio C., Stebbins G. T., et al. . (2007). Movement Disorder Society-sponsored revision of the Unified Parkinson's Disease Rating Scale (MDS-UPDRS): process, format, and clinimetric testing plan. Mov. Disord. 22, 41–47. 10.1002/mds.21198 PubMed DOI
Goetz C. G., Tilley B. C., Shaftman S. R., Stebbins G. T., Fahn S., Martinez-Martin P., et al. . (2008). Movement Disorder Society-sponsored revision of the Unified Parkinson's Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov. Disord. 23, 2129–2170. 10.1002/mds.22340 PubMed DOI
Gorell J., Ordidge R., Brown G. (1995). Increased iron -related MRI contrast in the substantia nigra in Parkinson's disease. Neurology 45, 1138–1143. 10.1212/WNL.45.6.1138 PubMed DOI
Greve D. N., Fischl B. (2009). Accurate and robust brain image alignment using boundary-based registration. Neuroimage 48, 63–72. 10.1016/j.neuroimage.2009.06.060 PubMed DOI PMC
Griffith C. J., Wijdicks C. A., Goerke U., Michaeli S., Ellermann J., LaPrade R. F. (2011). Outcomes of untreated posterolateral knee injuries: an in vivo canine model. Knee Surg. Sports Traumatol. Arthrosc. 19, 1192–1197. 10.1007/s00167-010-1358-z PubMed DOI
Hakkarainen H., Sierra A., Mangia S., Garwood M., Michaeli S., Grohn O., et al. . (2016). MRI relaxation in the presence of fictitious fields correlates with myelin content in normal rat brain. Magn. Reson. Med. 75, 161–168. 10.1002/mrm.25590 PubMed DOI PMC
Halliday G. M. (2009). Thalamic changes in Parkinson's disease. Parkinsonism Relat. Disord. 15(Suppl. 3), S152–S155. 10.1016/S1353-8020(09)70804-1 PubMed DOI
Hamilton M. (1959). The assessment of anxiety states by rating. Br. J. Med. Psychol. 32, 50–55. 10.1111/j.2044-8341.1959.tb00467.x PubMed DOI
Hamilton M. (1960). A rating scale for depression. J. Neurol. Neurosurg. Psychiatry 23, 56–62. 10.1136/jnnp.23.1.56 PubMed DOI PMC
Hamilton M. (1980). Rating depressive patients. J. Clin. Psychiatry 41(12 Pt 2), 21–24. PubMed
Hanyu H., Inoue Y., Sakurai H., Kanetaka H., Nakamura M., Miyamoto T., et al. . (2012). Voxel-based magnetic resonance imaging study of structural brain changes in patients with idiopathic REM sleep behavior disorder. Parkinsonism Relat. Disord. 18, 136–139. 10.1016/j.parkreldis.2011.08.023 PubMed DOI
Hawkes C. H., Shephard B. C., Daniel S. E. (1997). Olfactory dysfunction in Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 62, 436–446. 10.1136/jnnp.62.5.436 PubMed DOI PMC
Holm S. (1979). A simple sequentially rejective Bonferroni test procedure. Scand. J. Stat. 6, 65–70.
Hoops S., Nazem S., Siderowf A. D., Duda J. E., Xie S. X., Stern M. B., et al. . (2009). Validity of the MoCA and MMSE in the detection of MCI and dementia in Parkinson disease. Neurology 73, 1738–1745. 10.1212/WNL.0b013e3181c34b47 PubMed DOI PMC
Hughes A. J., Daniel S. E., Kilford L., Lees A. J. (1992). Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J. Neurol. Neurosurg. Psychiatry 55, 181–184. 10.1136/jnnp.55.3.181 PubMed DOI PMC
Ibarretxe-Bilbao N., Junque C., Marti M. J., Valldeoriola F., Vendrell P., Bargallo N., et al. . (2010). Olfactory impairment in Parkinson's disease and white matter abnormalities in central olfactory areas: a voxel-based diffusion tensor imaging study. Mov. Disord. 25, 1888–1894. 10.1002/mds.23208 PubMed DOI
Ibarretxe-Bilbao N., Tolosa E., Junque C., Marti M. J. (2009). MRI and cognitive impairment in Parkinson's disease. Mov. Disord. 24(Suppl. 2), S748–S753. 10.1002/mds.22670 PubMed DOI
Idiyatullin D., Corum C., Park J. Y., Garwood M. (2006). Fast and quiet MRI using a swept radiofrequency. J. Magn. Reson. 181, 342–349. 10.1016/j.jmr.2006.05.014 PubMed DOI
Jellinger K. A. (2015). Neuropathobiology of non-motor symptoms in Parkinson disease. J. Neural. Transm. 122, 1429–1440. 10.1007/s00702-015-1405-5 PubMed DOI
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. 10.1006/nimg.2002.1132 PubMed DOI
Jenkinson M., Beckmann C. F., Behrens T. E., Woolrich M. W., Smith S. M. (2012). Fsl. Neuroimage 62, 782–790. 10.1016/j.neuroimage.2011.09.015 PubMed DOI
Jokivarsi K. T., Niskanen J. P., Michaeli S., Grohn H. I., Garwood M., Kauppinen R. A., et al. . (2009). Quantitative assessment of water pools by T 1 rho and T 2 rho MRI in acute cerebral ischemia of the rat. J. Cereb. Blood Flow Metab. 29, 206–216. 10.1038/jcbfm.2008.113 PubMed DOI PMC
Kamagata K., Motoi Y., Abe O., Shimoji K., Hori M., Nakanishi A., et al. . (2012). White matter alteration of the cingulum in Parkinson disease with and without dementia: evaluation by diffusion tensor tract-specific analysis. AJNR Am. J. Neuroradiol. 33, 890–895. 10.3174/ajnr.A2860 PubMed DOI PMC
Karagulle Kendi A. T., Lehericy S., Luciana M., Ugurbil K., Tuite P. (2008). Altered diffusion in the frontal lobe in Parkinson disease. AJNR Am. J. Neuroradiol. 29, 501–505. 10.3174/ajnr.A0850 PubMed DOI PMC
Kaur D., Lee D., Ragapolan S., Andersen J. K. (2009). Glutathione depletion in immortalized midbrain-derived dopaminergic neurons results in increases in the labile iron pool: implications for Parkinson's disease. Free Radic. Biol. Med. 46, 593–598. 10.1016/j.freeradbiomed.2008.11.012 PubMed DOI PMC
Kostic V. S., Agosta F., Petrovic I., Galantucci S., Spica V., Jecmenica-Lukic M., et al. . (2010). Regional patterns of brain tissue loss associated with depression in Parkinson disease. Neurology 75, 857–863. 10.1212/WNL.0b013e3181f11c1d PubMed DOI
Li S. X., Wing Y. K., Lam S. P., Zhang J., Yu M. W., Ho C. K., et al. . (2010). Validation of a new REM sleep behavior disorder questionnaire (RBDQ-HK). Sleep Med. 11, 43–48. 10.1016/j.sleep.2009.06.008 PubMed DOI
Liimatainen T., Hakkarainen H., Mangia S., Huttunen J. M., Storino C., Idiyatullin D., et al. . (2015). MRI contrasts in high rank rotating frames. Magn. Reson. Med. 73, 254–262. 10.1002/mrm.25129 PubMed DOI PMC
Liimatainen T., Mangia S., Ling W., Ellermann J., Sorce D. J., Garwood M., et al. . (2011). Relaxation dispersion in MRI induced by fictitious magnetic fields. J. Magn. Reson. 209, 269–276. 10.1016/j.jmr.2011.01.022 PubMed DOI PMC
Liimatainen T., Sierra A., Hanson T., Sorce D. J., Yla-Herttuala S., Garwood M., et al. . (2012). Glioma cell density in a rat gene therapy model gauged by water relaxation rate along a fictitious magnetic field. Magn. Reson. Med. 67, 269–277. 10.1002/mrm.22997 PubMed DOI PMC
Liimatainen T., Sorce D. J., O'Connell R., Garwood M., Michaeli S. (2010). MRI contrast from relaxation along a fictitious field (RAFF). Magn. Reson. Med. 64, 983–994. 10.1002/mrm.22372 PubMed DOI PMC
Luk K. C., Kehm V., Carroll J., Zhang B., O'Brien P., Trojanowski J. Q., et al. . (2012). Pathological alpha-synuclein transmission initiates Parkinson-like neurodegeneration in nontransgenic mice. Science 338, 949–953. 10.1126/science.1227157 PubMed DOI PMC
Mangia S., Carpenter A. F., Tyan A. E., Eberly L. E., Garwood M., Michaeli S. (2013). Magnetization transfer and adiabatic T1rho MRI reveal abnormalities in normal-appearing white matter of subjects with multiple sclerosis. Mult. Scler. 20, 1066–1073. 10.1177/1352458513515084 PubMed DOI PMC
Mangia S., Liimatainen T., Garwood M., Michaeli S. (2009). Rotating frame relaxation during adiabatic pulses vs. conventional spin lock: simulations and experimental results at 4 T. Magn. Reson. Imaging 27, 1074–1087. 10.1016/j.mri.2009.05.023 PubMed DOI PMC
Martin W. R., Wieler M., Gee M. (2008). Midbrain iron content in early Parkinson disease: a potential biomarker of disease status. Neurology 70(16 Pt 2), 1411–1417. 10.1212/01.wnl.0000286384.31050.b5 PubMed DOI
Maximo J. O., Keown C. L., Nair A., Muller R. A. (2013). Approaches to local connectivity in autism using resting state functional connectivity MRI. Front. Hum. Neurosci. 7:605. 10.3389/fnhum.2013.00605 PubMed DOI PMC
Menke R. A., Jbabdi S., Miller K. L., Matthews P. M., Zarei M. (2010). Connectivity-based segmentation of the substantia nigra in human and its implications in Parkinson's disease. Neuroimage 52, 1175–1180. 10.1016/j.neuroimage.2010.05.086 PubMed DOI
Menke R. A., Scholz J., Miller K. L., Deoni S., Jbabdi S., Matthews P. M., et al. . (2009). MRI characteristics of the substantia nigra in Parkinson's disease: a combined quantitative T1 and DTI study. Neuroimage 47, 435–441. 10.1016/j.neuroimage.2009.05.017 PubMed DOI
Michaeli S. (2007). Novel MRI contrasts measure in vivo characteristics of Parkinson's disease. Nat. Clin. Pract. Neurol. 3, 122–123. 10.1038/ncpneuro0411 DOI
Michaeli S., Grohn H., Grohn O., Sorce D. J., Kauppinen R., Springer C. S., et al. . (2005). Exchange-influenced T2rho contrast in human brain images measured with adiabatic radio frequency pulses. Magn. Reson. Med. 53, 823–829. 10.1002/mrm.20428 PubMed DOI
Michaeli S., Oz G., Sorce D. J., Garwood M., Ugurbil K., Majestic S., et al. . (2007). Assessment of brain iron and neuronal integrity in patients with Parkinson's disease using novel MRI contrasts. Mov. Disord. 22, 334–340. 10.1002/mds.21227 PubMed DOI
Michaeli S., Sorce D. J., Garwood M. (2008). T-2 rho and T-1 rho adiabatic relaxations and contrasts. Curr. Anal. Chem. 4, 8–25. 10.2174/157341108783339115 DOI
Michaeli S., Sorce D. J., Idiyatullin D., Ugurbil K., Garwood M. (2004). Transverse relaxation in the rotating frame induced by chemical exchange. J. Magn. Reson. 169, 293–239. 10.1016/j.jmr.2004.05.010 PubMed DOI
Michaeli S., Sorce D. J., Springer C. S., Jr., Ugurbil K., Garwood M. (2006). T1rho MRI contrast in the human brain: modulation of the longitudinal rotating frame relaxation shutter-speed during an adiabatic RF pulse. J. Magn. Reson. 181, 135–147. 10.1016/j.jmr.2006.04.002 PubMed DOI
Nasreddine Z. S., Phillips N. A., Bedirian V., Charbonneau S., Whitehead V., Collin I., et al. . (2005). The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J. Am. Geriatr. Soc. 53, 695–699. 10.1111/j.1532-5415.2005.53221.x PubMed DOI
Nestrasil I., Michaeli S., Liimatainen T., Rydeen C. E., Kotz C. M., Nixon J. P., et al. . (2010). T1rho and T2rho MRI in the evaluation of Parkinson's disease. J. Neurol. 257, 964–968. 10.1007/s00415-009-5446-2 PubMed DOI PMC
Ogisu K., Kudo K., Sasaki M., Sakushima K., Yabe I., Sasaki H., et al. . (2013). 3D neuromelanin-sensitive magnetic resonance imaging with semi-automated volume measurement of the substantia nigra pars compacta for diagnosis of Parkinson's disease. Neuroradiology 55, 719–724. 10.1007/s00234-013-1171-8 PubMed DOI
Okuaki T., Takayama Y., Nishie A., Ogino T., Obara M., Honda H., et al. . (2017). T1rho mapping improvement using stretched-type adiabatic locking pulses for assessment of human liver function at 3T. Magn. Reson. Imaging 40, 17–23. 10.1016/j.mri.2017.03.006 PubMed DOI
Peran P., Cherubini A., Assogna F., Piras F., Quattrocchi C., Peppe A., et al. . (2010). Magnetic resonance imaging markers of Parkinson's disease nigrostriatal signature. Brain 133, 3423–3433. 10.1093/brain/awq212 PubMed DOI
Power J. D., Barnes K. A., Snyder A. Z., Schlaggar B. L., Petersen S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59, 2142–2154. 10.1016/j.neuroimage.2011.10.018 PubMed DOI PMC
Prodoehl J., Li H., Planetta P. J., Goetz C. G., Shannon K. M., Tangonan R., et al. . (2013). Diffusion tensor imaging of Parkinson's disease, atypical parkinsonism, and essential tremor. Mov. Disord. 28, 1816–1822. 10.1002/mds.25491 PubMed DOI PMC
Rolheiser T. M., Fulton H. G., Good K. P., Fisk J. D., McKelvey J. R., Scherfler C., et al. . (2011). Diffusion tensor imaging and olfactory identification testing in early-stage Parkinson's disease. J. Neurol. 258, 1254–1260. 10.1007/s00415-011-5915-2 PubMed DOI
Satzer D., DiBartolomeo C., Ritchie M. M., Storino C., Liimatainen T., Hakkarainen H., et al. . (2015). Assessment of dysmyelination with RAFFn MRI: application to murine MPS I. PLoS ONE 10:e0116788. 10.1371/journal.pone.0116788 PubMed DOI PMC
Schenck C. H., Bundlie S. R., Ettinger M. G., Mahowald M. W. (1986). Chronic behavioral disorders of human REM sleep: a new category of parasomnia. Sleep 9, 293–308. 10.1093/sleep/9.2.293 PubMed DOI
Schenck C. H., Bundlie S. R., Mahowald M. W. (1996). Delayed emergence of a parkinsonian disorder in 38% of 29 older men initially diagnosed with idiopathic rapid eye movement sleep behaviour disorder. Neurology 46, 388–393. 10.1212/WNL.46.2.388 PubMed DOI
Scherfler C., Frauscher B., Schocke M., Iranzo A., Gschliesser V., Seppi K., et al. . (2011). White and gray matter abnormalities in idiopathic rapid eye movement sleep behavior disorder: a diffusion-tensor imaging and voxel-based morphometry study. Ann. Neurol. 69, 400–407. 10.1002/ana.22245 PubMed DOI
Sierra A., Michaeli S., Niskanen J. P., Valonen P. K., Grohn H. I., Yla-Herttuala S., et al. . (2008). Water spin dynamics during apoptotic cell death in glioma gene therapy probed by T1rho and T2rho. Magn. Reson. Med. 59, 1311–1319. 10.1002/mrm.21600 PubMed DOI PMC
Silveira-Moriyama L., Petrie A., Williams D. R., Evans A., Katzenschlager R., Barbosa E. R., et al. . (2009). The use of a color coded probability scale to interpret smell tests in suspected parkinsonism. Mov. Disord. 24, 1144–1153. 10.1002/mds.22494 PubMed DOI
Smith S. M. (2002). Fast robust automated brain extraction. Hum. Brain Mapp. 17, 143–155. 10.1002/hbm.10062 PubMed DOI PMC
Song S. K., Lee J. E., Park H. J., Sohn Y. H., Lee J. D., Lee P. H. (2011). The pattern of cortical atrophy in patients with Parkinson's disease according to cognitive status. Mov. Disord. 26, 289–296. 10.1002/mds.23477 PubMed DOI
Tuite P. J., Mangia S., Tyan A. E., Lee M. K., Garwood M., Michaeli S. (2012). Magnetization transfer and adiabatic R 1rho MRI in the brainstem of Parkinson's disease. Parkinsonism Relat. Disord. 18, 623–625. 10.1016/j.parkreldis.2012.01.003 PubMed DOI PMC
Vaillancourt D. E., Spraker M. B., Prodoehl J., Abraham I., Corcos D. M., Zhou X. J., et al. . (2009). High-resolution diffusion tensor imaging in the substantia nigra of de novo Parkinson disease. Neurology 72, 1378–1384. 10.1212/01.wnl.0000340982.01727.6e PubMed DOI PMC
van Mierlo T. J., Chung C., Foncke E. M., Berendse H. W., van den Heuvel O. A. (2015). Depressive symptoms in Parkinson's disease are related to decreased hippocampus and amygdala volume. Mov. Disord. 30, 245–252. 10.1002/mds.26112 PubMed DOI
Vriend C., Boedhoe P. S., Rutten S., Berendse H. W., van der Werf Y. D., van den Heuvel O. A. (2016). A smaller amygdala is associated with anxiety in Parkinson's disease: a combined FreeSurfer-VBM study. J. Neurol. Neurosurg. Psychiatry 87, 493–500. 10.1136/jnnp-2015-310383 PubMed DOI
Yushkevich P. A., Piven J., Hazlett H. C., Smith R. G., Ho S., Gee J. C., et al. . (2006). User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31, 1116–1128. 10.1016/j.neuroimage.2006.01.015 PubMed DOI
Zang Y., Jiang T., Lu Y., He Y., Tian L. (2004). Regional homogeneity approach to fMRI data analysis. Neuroimage 22, 394–400. 10.1016/j.neuroimage.2003.12.030 PubMed DOI
Zecca L., Casella L., Albertini A., Bellei C., Zucca F. A., Engelen M., et al. . (2008). Neuromelanin can protect against iron-mediated oxidative damage in system modeling iron overload of brain aging and Parkinson's disease. J. Neurochem. 106, 1866–1875. 10.1111/j.1471-4159.2008.05541.x PubMed DOI
Zhang J., Nissi M. J., Idiyatullin D., Michaeli S., Garwood M., Ellermann J. (2016). Capturing fast relaxing spins with SWIFT adiabatic rotating frame spin-lattice relaxation (T1ρ) mapping. NMR Biomed. 29, 420–430. 10.1002/nbm.3474 PubMed DOI PMC