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Journal of Neurology, Neurosurgery, and Psychiatry logoLink to Journal of Neurology, Neurosurgery, and Psychiatry
. 2004 Feb;75(2):246–249.

Voxel based morphometry reveals a distinct pattern of frontal atrophy in progressive supranuclear palsy

C Brenneis 1, K Seppi 1, M Schocke 1, T Benke 1, G Wenning 1, W Poewe 1
PMCID: PMC1738933  PMID: 14742598

Abstract

Background: Frontal lobe atrophy is a well known neuropathological feature of progressive supranuclear palsy (PSP), accompanied by characteristic neuropsychological deficits.

Objective: To determine subregional frontal lobe atrophy patterns in patients with PSP using voxel based morphometry (VBM).

Methods: VBM is an observer unbiased volumetry which allows the investigation of the entire brain. An optimised protocol for normalisation, segmentation, and correction for volume changes in preprocessing was used. Grey matter, white matter, and cerebrospinal fluid (CSF) partitions in 12 patients with probable PSP were compared with 12 healthy controls matched for age and sex.

Results: In PSP patients, the following cortical areas were decreased in volume (pcorr<0.05): the prefrontal cortex, predominantly the medial frontal gyri and a cluster in the left lateral middle frontal gyrus; the insular region including the frontal opercula; both supplementary motor areas; and the left medio-temporal area (V5). White matter comparisons revealed a volume reduction in both frontotemporal regions and the mesencephalon. Analysis of the CSF compartment showed no significant regional changes between the groups.

Conclusions: Frontal atrophy in PSP predominantly involves mesio-frontal targets of striatal projections. This atrophy pattern probably accounts for cardinal PSP associated behavioural deficits.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abe K., Terakawa H., Takanashi M., Watanabe Y., Tanaka H., Fujita N., Hirabuki N., Yanagihara T. Proton magnetic resonance spectroscopy of patients with parkinsonism. Brain Res Bull. 2000 Aug;52(6):589–595. doi: 10.1016/s0361-9230(00)00321-x. [DOI] [PubMed] [Google Scholar]
  2. Asato R., Akiguchi I., Masunaga S., Hashimoto N. Magnetic resonance imaging distinguishes progressive supranuclear palsy from multiple system atrophy. J Neural Transm (Vienna) 2000;107(12):1427–1436. doi: 10.1007/s007020070006. [DOI] [PubMed] [Google Scholar]
  3. Ashburner J., Friston K. J. Nonlinear spatial normalization using basis functions. Hum Brain Mapp. 1999;7(4):254–266. doi: 10.1002/(SICI)1097-0193(1999)7:4&#x0003c;254::AID-HBM4&#x0003e;3.0.CO;2-G. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ashburner J., Friston K. J. Voxel-based morphometry--the methods. Neuroimage. 2000 Jun;11(6 Pt 1):805–821. doi: 10.1006/nimg.2000.0582. [DOI] [PubMed] [Google Scholar]
  5. Ashburner J., Friston K. J. Why voxel-based morphometry should be used. Neuroimage. 2001 Dec;14(6):1238–1243. doi: 10.1006/nimg.2001.0961. [DOI] [PubMed] [Google Scholar]
  6. Baron J. C., Chételat G., Desgranges B., Perchey G., Landeau B., de la Sayette V., Eustache F. In vivo mapping of gray matter loss with voxel-based morphometry in mild Alzheimer's disease. Neuroimage. 2001 Aug;14(2):298–309. doi: 10.1006/nimg.2001.0848. [DOI] [PubMed] [Google Scholar]
  7. Blin J., Baron J. C., Dubois B., Pillon B., Cambon H., Cambier J., Agid Y. Positron emission tomography study in progressive supranuclear palsy. Brain hypometabolic pattern and clinicometabolic correlations. Arch Neurol. 1990 Jul;47(7):747–752. doi: 10.1001/archneur.1990.00530070035009. [DOI] [PubMed] [Google Scholar]
  8. Burn David J., Lees Andrew J. Progressive supranuclear palsy: where are we now? Lancet Neurol. 2002 Oct;1(6):359–369. doi: 10.1016/s1474-4422(02)00161-8. [DOI] [PubMed] [Google Scholar]
  9. Cambier J., Masson M., Viader F., Limodin J., Strube A. Le syndrome frontal de la paralysie supranucléaire progressive. Rev Neurol (Paris) 1985;141(8-9):528–536. [PubMed] [Google Scholar]
  10. Cordato N. J., Pantelis C., Halliday G. M., Velakoulis D., Wood S. J., Stuart G. W., Currie J., Soo M., Olivieri G., Broe G. A. Frontal atrophy correlates with behavioural changes in progressive supranuclear palsy. Brain. 2002 Apr;125(Pt 4):789–800. doi: 10.1093/brain/awf082. [DOI] [PubMed] [Google Scholar]
  11. Daniel S. E., de Bruin V. M., Lees A. J. The clinical and pathological spectrum of Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy): a reappraisal. Brain. 1995 Jun;118(Pt 3):759–770. doi: 10.1093/brain/118.3.759. [DOI] [PubMed] [Google Scholar]
  12. Defer G. L., Widner H., Marié R. M., Rémy P., Levivier M. Core assessment program for surgical interventional therapies in Parkinson's disease (CAPSIT-PD). Mov Disord. 1999 Jul;14(4):572–584. doi: 10.1002/1531-8257(199907)14:4<572::aid-mds1005>3.0.co;2-c. [DOI] [PubMed] [Google Scholar]
  13. Foster N. L., Gilman S., Berent S., Morin E. M., Brown M. B., Koeppe R. A. Cerebral hypometabolism in progressive supranuclear palsy studied with positron emission tomography. Ann Neurol. 1988 Sep;24(3):399–406. doi: 10.1002/ana.410240308. [DOI] [PubMed] [Google Scholar]
  14. Goffinet A. M., De Volder A. G., Gillain C., Rectem D., Bol A., Michel C., Cogneau M., Labar D., Laterre C. Positron tomography demonstrates frontal lobe hypometabolism in progressive supranuclear palsy. Ann Neurol. 1989 Feb;25(2):131–139. doi: 10.1002/ana.410250205. [DOI] [PubMed] [Google Scholar]
  15. Good C. D., Johnsrude I. S., Ashburner J., Henson R. N., Friston K. J., Frackowiak R. S. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage. 2001 Jul;14(1 Pt 1):21–36. doi: 10.1006/nimg.2001.0786. [DOI] [PubMed] [Google Scholar]
  16. Grafman J., Litvan I., Gomez C., Chase T. N. Frontal lobe function in progressive supranuclear palsy. Arch Neurol. 1990 May;47(5):553–558. doi: 10.1001/archneur.1990.00530050077015. [DOI] [PubMed] [Google Scholar]
  17. Hanihara T., Amano N., Takahashi T., Nagatomo H., Yagashita S. Distribution of tangles and threads in the cerebral cortex in progressive supranuclear palsy. Neuropathol Appl Neurobiol. 1995 Aug;21(4):319–326. doi: 10.1111/j.1365-2990.1995.tb01066.x. [DOI] [PubMed] [Google Scholar]
  18. Hauw J. J., Daniel S. E., Dickson D., Horoupian D. S., Jellinger K., Lantos P. L., McKee A., Tabaton M., Litvan I. Preliminary NINDS neuropathologic criteria for Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Neurology. 1994 Nov;44(11):2015–2019. doi: 10.1212/wnl.44.11.2015. [DOI] [PubMed] [Google Scholar]
  19. Hof P. R., Delacourte A., Bouras C. Distribution of cortical neurofibrillary tangles in progressive supranuclear palsy: a quantitative analysis of six cases. Acta Neuropathol. 1992;84(1):45–51. doi: 10.1007/BF00427214. [DOI] [PubMed] [Google Scholar]
  20. Jellinger K. A., Bancher C., Hauw J. J., Verny M. Progressive supranuclear palsy: neuropathologically based diagnostic clinical criteria. J Neurol Neurosurg Psychiatry. 1995 Jul;59(1):106–106. doi: 10.1136/jnnp.59.1.106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Johnson K. A., Sperling R. A., Holman B. L., Nagel J. S., Growdon J. H. Cerebral perfusion in progressive supranuclear palsy. J Nucl Med. 1992 May;33(5):704–709. [PubMed] [Google Scholar]
  22. Litvan I., Mangone C. A., McKee A., Verny M., Parsa A., Jellinger K., D'Olhaberriague L., Chaudhuri K. R., Pearce R. K. Natural history of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome) and clinical predictors of survival: a clinicopathological study. J Neurol Neurosurg Psychiatry. 1996 Jun;60(6):615–620. doi: 10.1136/jnnp.60.6.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Litvan I., Mega M. S., Cummings J. L., Fairbanks L. Neuropsychiatric aspects of progressive supranuclear palsy. Neurology. 1996 Nov;47(5):1184–1189. doi: 10.1212/wnl.47.5.1184. [DOI] [PubMed] [Google Scholar]
  24. Litvan I. Progressive supranuclear palsy revisited. Acta Neurol Scand. 1998 Aug;98(2):73–84. [PubMed] [Google Scholar]
  25. Maher E. R., Smith E. M., Lees A. J. Cognitive deficits in the Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). J Neurol Neurosurg Psychiatry. 1985 Dec;48(12):1234–1239. doi: 10.1136/jnnp.48.12.1234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mega M. S., Cummings J. L. Frontal-subcortical circuits and neuropsychiatric disorders. J Neuropsychiatry Clin Neurosci. 1994 Fall;6(4):358–370. doi: 10.1176/jnp.6.4.358. [DOI] [PubMed] [Google Scholar]
  27. O'Driscoll G. A., Wolff A. L., Benkelfat C., Florencio P. S., Lal S., Evans A. C. Functional neuroanatomy of smooth pursuit and predictive saccades. Neuroreport. 2000 Apr 27;11(6):1335–1340. doi: 10.1097/00001756-200004270-00037. [DOI] [PubMed] [Google Scholar]
  28. Petit L., Haxby J. V. Functional anatomy of pursuit eye movements in humans as revealed by fMRI. J Neurophysiol. 1999 Jul;82(1):463–471. doi: 10.1152/jn.1999.82.1.463. [DOI] [PubMed] [Google Scholar]
  29. Pillon B., Deweer B., Michon A., Malapani C., Agid Y., Dubois B. Are explicit memory disorders of progressive supranuclear palsy related to damage to striatofrontal circuits? Comparison with Alzheimer's, Parkinson's, and Huntington's diseases. Neurology. 1994 Jul;44(7):1264–1270. doi: 10.1212/wnl.44.7.1264. [DOI] [PubMed] [Google Scholar]
  30. Pillon B., Dubois B., Ploska A., Agid Y. Severity and specificity of cognitive impairment in Alzheimer's, Huntington's, and Parkinson's diseases and progressive supranuclear palsy. Neurology. 1991 May;41(5):634–643. doi: 10.1212/wnl.41.5.634. [DOI] [PubMed] [Google Scholar]
  31. Pillon B., Gouider-Khouja N., Deweer B., Vidailhet M., Malapani C., Dubois B., Agid Y. Neuropsychological pattern of striatonigral degeneration: comparison with Parkinson's disease and progressive supranuclear palsy. J Neurol Neurosurg Psychiatry. 1995 Feb;58(2):174–179. doi: 10.1136/jnnp.58.2.174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Price J. L., Morris J. C. Tangles and plaques in nondemented aging and "preclinical" Alzheimer's disease. Ann Neurol. 1999 Mar;45(3):358–368. doi: 10.1002/1531-8249(199903)45:3<358::aid-ana12>3.0.co;2-x. [DOI] [PubMed] [Google Scholar]
  33. Rombouts S. A., Barkhof F., Witter M. P., Scheltens P. Unbiased whole-brain analysis of gray matter loss in Alzheimer's disease. Neurosci Lett. 2000 May 19;285(3):231–233. doi: 10.1016/s0304-3940(00)01067-3. [DOI] [PubMed] [Google Scholar]
  34. Santacruz P., Uttl B., Litvan I., Grafman J. Progressive supranuclear palsy: a survey of the disease course. Neurology. 1998 Jun;50(6):1637–1647. doi: 10.1212/wnl.50.6.1637. [DOI] [PubMed] [Google Scholar]
  35. Schulz J. B., Skalej M., Wedekind D., Luft A. R., Abele M., Voigt K., Dichgans J., Klockgether T. Magnetic resonance imaging-based volumetry differentiates idiopathic Parkinson's syndrome from multiple system atrophy and progressive supranuclear palsy. Ann Neurol. 1999 Jan;45(1):65–74. [PubMed] [Google Scholar]
  36. Spillantini M. G., Bird T. D., Ghetti B. Frontotemporal dementia and Parkinsonism linked to chromosome 17: a new group of tauopathies. Brain Pathol. 1998 Apr;8(2):387–402. doi: 10.1111/j.1750-3639.1998.tb00162.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Tedeschi G., Litvan I., Bonavita S., Bertolino A., Lundbom N., Patronas N. J., Hallett M. Proton magnetic resonance spectroscopic imaging in progressive supranuclear palsy, Parkinson's disease and corticobasal degeneration. Brain. 1997 Sep;120(Pt 9):1541–1552. doi: 10.1093/brain/120.9.1541. [DOI] [PubMed] [Google Scholar]
  38. Van Hoesen G. W., Parvizi J., Chu C. C. Orbitofrontal cortex pathology in Alzheimer's disease. Cereb Cortex. 2000 Mar;10(3):243–251. doi: 10.1093/cercor/10.3.243. [DOI] [PubMed] [Google Scholar]
  39. Verny M., Duyckaerts C., Agid Y., Hauw J. J. The significance of cortical pathology in progressive supranuclear palsy. Clinico-pathological data in 10 cases. Brain. 1996 Aug;119(Pt 4):1123–1136. doi: 10.1093/brain/119.4.1123. [DOI] [PubMed] [Google Scholar]
  40. Verny M., Jellinger K. A., Hauw J. J., Bancher C., Litvan I., Agid Y. Progressive supranuclear palsy: a clinicopathological study of 21 cases. Acta Neuropathol. 1996;91(4):427–431. doi: 10.1007/s004010050446. [DOI] [PubMed] [Google Scholar]
  41. Warmuth-Metz M., Naumann M., Csoti I., Solymosi L. Measurement of the midbrain diameter on routine magnetic resonance imaging: a simple and accurate method of differentiating between Parkinson disease and progressive supranuclear palsy. Arch Neurol. 2001 Jul;58(7):1076–1079. doi: 10.1001/archneur.58.7.1076. [DOI] [PubMed] [Google Scholar]

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