European Radiology

, 21:2202 | Cite as

A novel tract imaging technique of the brainstem using phase difference enhanced imaging: normal anatomy and initial experience in multiple system atrophy

  • Shingo KakedaEmail author
  • Yukunori Korogi
  • Tetsuya Yoneda
  • Johji Nishimura
  • Toru Sato
  • Yasuhiro Hiai
  • Norihiro Ohnari
  • Kazumasa Okada
  • Haruki Hayashi
  • Eiji Matsusue
  • Takenori Uozumi
  • Sadatoshi Tsuji



To develop a new tract imaging technique for visualising small fibre tracts of the brainstem and for detecting the abnormalities in multiple system atrophy of the cerebellar type (MSA-C) using a phase difference enhanced (PADRE) imaging technique, in which the phase difference between the target and surrounding tissue is selectively enhanced.


Two neuroradiologists compared the high-spatial-resolution PADRE imaging, which was acquired from six healthy volunteers, three patients with MSA-C, and 7 patients with other types of neurodegenerative diseases involving the brainstem or cerebellum.


Various fine fibre tracts in the brainstem, the superior and inferior cerebellar peduncles, medial lemniscus, spinothalamic tract, medial longitudinal fasciculus, central tegmental tract, corticospinal tract and transverse pontine fibres, were identified on PADRE imaging. PADRE imaging from MSA-C demonstrated the disappearance of transverse pontine fibres and significant atrophy of the inferior cerebellar peduncles, while the superior cerebellar peduncles were intact. PADRE imaging also demonstrated that the transverse pontine fibres and inferior cerebellar peduncle were not involved in the other neurodegenerative diseases.


PADRE imaging can offer a new form of tract imaging of the brainstem and may have the potential to reinforce the clinical utility of MRI in differentiating MSA from other conditions.


MRI Brainstem anatomy Tract imaging Phase difference enhanced imaging Multiple system atrophy 

Supplementary material

330_2011_2158_Fig4_ESM.jpg (32 kb)
Supplementary Fig. 1

(JPEG 32 kb)

330_2011_2158_MOESM1_ESM.tif (421 kb)
High resolution image (TIFF 421 kb)
330_2011_2158_Fig5_ESM.jpg (34 kb)
Supplementary Fig. 2

(JPEG 34 kb)

330_2011_2158_MOESM2_ESM.tif (433 kb)
High resolution image (TIFF 433 kb)
330_2011_2158_Fig6_ESM.jpg (34 kb)
Supplementary Fig. 3

(JPEG 34 kb)

330_2011_2158_MOESM3_ESM.tif (438 kb)
High resolution image (TIFF 437 kb)
330_2011_2158_Fig7_ESM.jpg (30 kb)
Supplementary Fig. 4

(JPEG 30 kb)

330_2011_2158_MOESM4_ESM.tif (393 kb)
High resolution image (TIFF 393 kb)
330_2011_2158_Fig8_ESM.jpg (30 kb)
Supplementary Fig. 5

(JPEG 30 kb)

330_2011_2158_MOESM5_ESM.tif (393 kb)
High resolution image (TIFF 392 kb)
330_2011_2158_Fig9_ESM.jpg (33 kb)
Supplementary Fig. 6

(JPEG 33 kb)

330_2011_2158_MOESM6_ESM.tif (427 kb)
High resolution image (TIFF 427 kb)
330_2011_2158_Fig10_ESM.jpg (29 kb)
Supplementary Fig. 7

(JPEG 28 kb)

330_2011_2158_MOESM7_ESM.tif (384 kb)
High resolution image (TIFF 384 kb)
330_2011_2158_Fig11_ESM.jpg (36 kb)
Supplementary Fig. 8

(JPEG 35 kb)

330_2011_2158_MOESM8_ESM.tif (451 kb)
High resolution image (TIFF 450 kb)
330_2011_2158_Fig12_ESM.jpg (33 kb)
Supplementary Fig. 9

(JPEG 33 kb)

330_2011_2158_MOESM9_ESM.tif (422 kb)
High resolution image (TIFF 422 kb)
330_2011_2158_Fig13_ESM.jpg (39 kb)
Supplementary Fig. 10

(JPEG 38 kb)

330_2011_2158_MOESM10_ESM.tif (477 kb)
High resolution image (TIFF 476 kb)
330_2011_2158_Fig14_ESM.jpg (32 kb)
Supplementary Fig. 11

(JPEG 32 kb)

330_2011_2158_MOESM11_ESM.tif (415 kb)
High resolution image (TIFF 415 kb)
330_2011_2158_Fig15_ESM.jpg (35 kb)
Supplementary Fig. 12

(JPEG 35 kb)

330_2011_2158_MOESM12_ESM.tif (442 kb)
High resolution image (TIFF 441 kb)
330_2011_2158_Fig16_ESM.jpg (34 kb)
Supplementary Fig. 13

(JPEG 33 kb)

330_2011_2158_MOESM13_ESM.tif (427 kb)
High resolution image (TIFF 427 kb)
330_2011_2158_Fig17_ESM.jpg (36 kb)
Supplementary Fig. 14

(JPEG 35 kb)

330_2011_2158_MOESM14_ESM.tif (451 kb)
High resolution image (TIFF 450 kb)
330_2011_2158_Fig18_ESM.jpg (37 kb)
Supplementary Fig. 15

(JPEG 36 kb)

330_2011_2158_MOESM15_ESM.tif (457 kb)
High resolution image (TIFF 456 kb)
330_2011_2158_Fig19_ESM.jpg (32 kb)
Supplementary Fig. 16

(JPEG 32 kb)

330_2011_2158_MOESM16_ESM.tif (414 kb)
High resolution image (TIFF 413 kb)
330_2011_2158_Fig20_ESM.jpg (34 kb)
Supplementary Fig. 17

(JPEG 34 kb)

330_2011_2158_MOESM17_ESM.tif (433 kb)
High resolution image (TIFF 433 kb)
330_2011_2158_Fig21_ESM.jpg (35 kb)
Supplementary Fig. 18

(JPEG 35 kb)

330_2011_2158_MOESM18_ESM.tif (443 kb)
High resolution image (TIFF 443 kb)
330_2011_2158_Fig22_ESM.jpg (34 kb)
Supplementary Fig. 19

(JPEG 33 kb)

330_2011_2158_MOESM19_ESM.tif (428 kb)
High resolution image (TIFF 427 kb)
330_2011_2158_Fig23_ESM.jpg (28 kb)
Supplementary Fig. 20

(JPEG 28 kb)

330_2011_2158_MOESM20_ESM.tif (379 kb)
High resolution image (TIFF 378 kb)
330_2011_2158_Fig24_ESM.jpg (30 kb)
Supplementary Fig. 21

(JPEG 29 kb)

330_2011_2158_MOESM21_ESM.tif (399 kb)
High resolution image (TIFF 398 kb)
330_2011_2158_Fig25_ESM.jpg (28 kb)
Supplementary Fig. 22

(JPEG 27 kb)

330_2011_2158_MOESM22_ESM.tif (382 kb)
High resolution image (TIFF 381 kb)
330_2011_2158_Fig26_ESM.jpg (31 kb)
Supplementary Fig. 23

(JPEG 30 kb)

330_2011_2158_MOESM23_ESM.tif (410 kb)
High resolution image (TIFF 410 kb)
330_2011_2158_Fig27_ESM.jpg (29 kb)
Supplementary Fig. 24

(JPEG 29 kb)

330_2011_2158_MOESM24_ESM.tif (394 kb)
High resolution image (TIFF 394 kb)
330_2011_2158_Fig28_ESM.jpg (28 kb)
Supplementary Fig. 25

(JPEG 27 kb)

330_2011_2158_MOESM25_ESM.tif (382 kb)
High resolution image (TIFF 382 kb)
330_2011_2158_Fig29_ESM.jpg (25 kb)
Supplementary Fig. 26

(JPEG 24 kb)

330_2011_2158_MOESM26_ESM.tif (352 kb)
High resolution image (TIFF 352 kb)


  1. 1.
    Wakana S, Jiang H, Nagae-Poetscher LM, van Zijl PC, Mori S (2004) Fiber tract-based atlas of human white matter anatomy. Radiology 230:77–87PubMedCrossRefGoogle Scholar
  2. 2.
    Nagae-Poetscher LM, Jiang H, Wakana S, Golay X, van Zijl PC, Mori S (2004) High-resolution diffusion tensor imaging of the brain stem at 3T. AJNR Am J Neuroradiol 25:1325–1330PubMedGoogle Scholar
  3. 3.
    Haacke EM, Xu Y, Cheng YC, Reichenbach JR (2004) Susceptibility weighted imaging (SWI). Magn Reson Med 52:612–618PubMedCrossRefGoogle Scholar
  4. 4.
    Haacke EM, Cheng NY, House MJ, Liu Q, Neelavalli J, Ogg RJ, Khan A, Ayaz M, Kirsch W, Obenaus A (2005) Imaging iron stores in the brain using magnetic resonance imaging. Magn Reson Imaging 23:1–25PubMedCrossRefGoogle Scholar
  5. 5.
    Haacke EM, Ayaz M, Khan A, Manova ES, Krishnamurthy B, Gollapalli L, Ciulla C, Kim I, Petersen F, Kirsch W (2007) Establishing a baseline phase behavior in magnetic resonance imaging to determine normal vs. abnormal iron content in the brain. J Magn Reson Imaging 26:256–264PubMedCrossRefGoogle Scholar
  6. 6.
    Kakeda S, Korogi Y, Kamada K, Ohnari N, Moriya J, Sato T, Kitajima M, Hasnine H, Hirata N (2008) Signal intensity of the motor cortex on phase-weighted imaging at 3T. AJNR Am J Neuroradiol 29:1171–1175PubMedCrossRefGoogle Scholar
  7. 7.
    Yoneda T (2009) Triple-layer appearance of human cerebral cortices on phase-difference enhanced imaging using 3D principle of echo shifting with a train of observations (PRESTO) sequence. Proc Int Soc Magn Reson Med 17:27Google Scholar
  8. 8.
    Wenning GK, Ben Shlomo Y, Magalhaes M, Daniel SE, Quinn NP (1994) Clinical features and natural history of multiple system atrophy. An analysis of 100 cases. Brain 117(Pt 4):835–845PubMedCrossRefGoogle Scholar
  9. 9.
    Gilman S, Low PA, Quinn N, Albanese A, Ben-Shlomo Y, Fowler CJ, Kaufmann H, Klockgether T, Lang AE, Lantos PL, Litvan I, Mathias CJ, Oliver E, Robertson D, Schatz I, Wenning GK (1999) Consensus statement on the diagnosis of multiple system atrophy. J Neurol Sci 163:94–98PubMedCrossRefGoogle Scholar
  10. 10.
    Harding AE, Deufel T (eds) (1993) Inherited ataxias. In: Advances in neurology, vol 61. New York: RavenGoogle Scholar
  11. 11.
    Nolte J (2003) The human brain, 5th edn. Mosby Year Book, St LouisGoogle Scholar
  12. 12.
    Matsusue E, Fujii S, Kanasaki Y, Kaminou T, Ohama E, Ogawa T (2009) Cerebellar lesions in multiple system atrophy: postmortem MR imaging-pathologic correlations. AJNR Am J Neuroradiol 30:1725–1730PubMedCrossRefGoogle Scholar
  13. 13.
    Wenning GK, Tison F, Elliott L, Quinn NP, Daniel SE (1996) Olivopontocerebellar pathology in multiple system atrophy. Mov Disord 11:157–162PubMedCrossRefGoogle Scholar
  14. 14.
    Papp MI, Kahn JE, Lantos PL (1989) Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (striatonigral degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome). J Neurol Sci 94:79–100PubMedCrossRefGoogle Scholar
  15. 15.
    Dickson DW, Lin W, Liu WK, Yen SH (1999) Multiple system atrophy: a sporadic synucleinopathy. Brain Pathol 9:721–732PubMedCrossRefGoogle Scholar
  16. 16.
    Naka H, Ohshita T, Murata Y, Imon Y, Mimori Y, Nakamura S (2002) Characteristic MRI findings in multiple system atrophy: comparison of the three subtypes. Neuroradiology 44:204–209PubMedCrossRefGoogle Scholar
  17. 17.
    Schott JM, Simon JE, Fox NC, King AP, Khan MN, Cipolotti L, Paviour DC, Stevens JM, Rossor MN (2003) Delineating the sites and progression of in vivo atrophy in multiple system atrophy using fluid-registered MRI. Mov Disord 18:955–958PubMedCrossRefGoogle Scholar
  18. 18.
    Lee EA, Cho HI, Kim SS, Lee WY (2004) Comparison of magnetic resonance imaging in subtypes of multiple system atrophy. Parkinsonism Relat Disord 10:363–368PubMedCrossRefGoogle Scholar
  19. 19.
    Papp MI, Lantos PL (1994) The distribution of oligodendroglial inclusions in multiple system atrophy and its relevance to clinical symptomatology. Brain 117(Pt 2):235–243PubMedCrossRefGoogle Scholar
  20. 20.
    Steele JC, Richardson JC, Olszewski J (1964) Progressive supranuclear palsy. A heterogeneous degeneration involving the brain stem, basal ganglia and cerebellum with vertical gaze and pseudobulbar palsy, nuchal dystonia and dementia. Arch Neurol 10:333–359PubMedGoogle Scholar
  21. 21.
    Tsuboi Y, Slowinski J, Josephs KA, Honer WG, Wszolek ZK, Dickson DW (2003) Atrophy of superior cerebellar peduncle in progressive supranuclear palsy. Neurology 60:1766–1769PubMedGoogle Scholar
  22. 22.
    Giussani C, Poliakov A, Ferri RT, Plawner LL, Browd SR, Shaw DW, Filardi TZ, Hoeppner C, Geyer JR, Olson JM, Douglas JG, Villavicencio EH, Ellenbogen RG, Ojemann JG (2010) DTI fiber tracking to differentiate demyelinating diseases from diffuse brain stem glioma. Neuroimage 52:217–223PubMedCrossRefGoogle Scholar
  23. 23.
    Griswold MA, Jakob PM, Nittka M, Goldfarb JW, Haase A (2000) Partially parallel imaging with localized sensitivities (PILS). Magn Reson Med 44:602–609PubMedCrossRefGoogle Scholar

Copyright information

© European Society of Radiology 2011

Authors and Affiliations

  • Shingo Kakeda
    • 1
    Email author
  • Yukunori Korogi
    • 1
  • Tetsuya Yoneda
    • 2
  • Johji Nishimura
    • 1
  • Toru Sato
    • 1
  • Yasuhiro Hiai
    • 2
  • Norihiro Ohnari
    • 1
  • Kazumasa Okada
    • 3
  • Haruki Hayashi
    • 4
  • Eiji Matsusue
    • 5
  • Takenori Uozumi
    • 3
  • Sadatoshi Tsuji
    • 3
  1. 1.Department of RadiologyUniversity of Occupational and Environmental Health School of MedicineKitakyushuJapan
  2. 2.Department of Course of Radiological SciencesKumamoto University School of Health SciencesKumamotoJapan
  3. 3.Department of NeurologyUniversity of Occupational and Environmental Health School of MedicineKitakyushuJapan
  4. 4.Department of Anatomy and Anthropology, School of MedicineUniversity of Occupational and Environmental HealthKitakyushuJapan
  5. 5.Division of Radiology, Department of Pathophysiological and Therapeutic Science, Faculty of MedicineTottori UniversityTottoriJapan

Personalised recommendations