Skip to main content

Advertisement

SpringerLink
Log in

Brain FDG-PET correlates of saccadic disorders in early PSP

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

Background

New diagnostic criteria of Progressive Supranuclear Palsy (PSP) have highlighted the interest of Eye Movement Records (EMR) at the early stage of the disease.

Objectives

To investigate the metabolic brain correlates of ocular motor dysfunction using [18F] Fluorodeoxyglucose Positron Emission Tomography (FDG-PET) in early PSP.

Methods

Retrospective observational descriptive study on longitudinal data with patients who underwent EMR and FDG-PET at the stage of suggestive and possible PSP according to Movement Disorders Society criteria. Longitudinal follow-up enables to confirm diagnosis of probable PSP. Using the Statistical Parametric Mapping software, we performed whole-brain voxel-based correlations between oculomotor variables and FDG-PET metabolism.

Results

Thirty-seven patients with early PSP who fulfilled criteria of probable PSP during the follow-up were included. Decrease in the gain of vertical saccades correlated with reduced metabolism in Superior Colliculi (SC). We also found a positive correlation between mean velocity of horizontal saccades and SC metabolism as well as dorsal nuclei in the pons. Finally, increase in horizontal saccades latencies correlated with decrease of posterior parietal metabolism.

Conclusions

These findings suggest the early involvement of SC in saccadic dysfunction in the course of PSP.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Anonymized data can be shared by request from any qualified investigator as long as data transfer is in agreement with EU legislation.

References

  1. Litvan I, Agid Y, Calne D et al (1996) Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP International Workshop*. Neurology 47:1–9. https://doi.org/10.1212/WNL.47.1.1

    Article  CAS  PubMed  Google Scholar 

  2. 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 10:333–359. https://doi.org/10.1001/archneur.1964.00460160003001

    Article  CAS  PubMed  Google Scholar 

  3. Respondek G, Kurz C, Arzberger T et al (2017) Which ante mortem clinical features predict progressive supranuclear palsy pathology? Mov Disord 32:995–1005. https://doi.org/10.1002/mds.27034

    Article  PubMed  PubMed Central  Google Scholar 

  4. Respondek G, Stamelou M, Kurz C et al (2014) The phenotypic spectrum of progressive supranuclear palsy: a retrospective multicenter study of 100 definite cases. Mov Disord 29:1758–1766. https://doi.org/10.1002/mds.26054

    Article  PubMed  Google Scholar 

  5. Marx S, Respondek G, Stamelou M et al (2012) Validation of mobile eye-tracking as novel and efficient means for differentiating progressive supranuclear palsy from Parkinson’s disease. Front Behav Neurosci. https://doi.org/10.3389/fnbeh.2012.00088

    Article  PubMed  PubMed Central  Google Scholar 

  6. Shaikh AG, Factor SA, Juncos JL (2017) Saccades in progressive supranuclear palsy-maladapted, irregular, curved, and slow. Mov Disord Clin Pract 4:671–681. https://doi.org/10.1002/mdc3.12491

    Article  PubMed  PubMed Central  Google Scholar 

  7. Rivaud-Pechoux S, Vidailhet M, Gallouedec G et al (2000) Longitudinal ocular motor study in corticobasal degeneration and progressive supranuclear palsy. Neurology 54:1029–1032. https://doi.org/10.1212/WNL.54.5.1029

    Article  CAS  PubMed  Google Scholar 

  8. Höglinger GU, Respondek G, Stamelou M et al (2017) Clinical diagnosis of progressive supranuclear palsy: the movement disorder society criteria: MDS Clinical Diagnostic Criteria for PSP. Mov Disord 32:853–864. https://doi.org/10.1002/mds.26987

    Article  PubMed  PubMed Central  Google Scholar 

  9. Garbutt S (2012) Saccade abnormalities in autopsy-confirmed frontotemporal lobar degeneration and alzheimer disease. Arch Neurol 69:509. https://doi.org/10.1001/archneurol.2011.1021

    Article  PubMed  PubMed Central  Google Scholar 

  10. Groschel K, Kastrup A, Litvan I et al (2006) Penguins and hummingbirds: midbrain atrophy in progressive supranuclear palsy. Neurology 66:949–950. https://doi.org/10.1212/01.wnl.0000203342.77115.bf

    Article  PubMed  Google Scholar 

  11. Amtage F, Maurer C, Hellwig S et al (2014) Functional correlates of vertical gaze palsy and other ocular motor deficits in PSP: an FDG-PET study. Parkinsonism Relat Disord 20:898–906. https://doi.org/10.1016/j.parkreldis.2014.05.013

    Article  PubMed  Google Scholar 

  12. Verger A, Grimaldi S, Ribeiro M et al (2021) Single photon emission computed tomography/positron emission tomography molecular imaging for parkinsonism: a fast-developing field. Ann Neurol 90:711–719. https://doi.org/10.1002/ana.26187

    Article  PubMed  PubMed Central  Google Scholar 

  13. Grimm M-J, Respondek G, Stamelou M et al (2019) How to apply the movement disorder society criteria for diagnosis of progressive supranuclear palsy. Mov Disord 34:1228–1232. https://doi.org/10.1002/mds.27666

    Article  PubMed  PubMed Central  Google Scholar 

  14. Buch KA, Bouffard MA, Kardon RH et al (2022) Clinical correlation between vertical gaze palsy and midbrain volume in progressive supranuclear palsy. J Neuroophthalmol 42:246–250. https://doi.org/10.1097/WNO.0000000000001393

    Article  PubMed  Google Scholar 

  15. Jaillard A, Petyt G, Morelle M (2016) [18F]-Fdg pet identified superior colliculi hypometabolism in progressive supranuclear palsy. J Alzheimers Dis Parkinsonism. https://doi.org/10.4172/2161-0460.1000278

    Article  Google Scholar 

  16. Bhidayasiri R, Riley DE, Somers JT et al (2001) Pathophysiology of slow vertical saccades in progressive supranuclear palsy. Neurology 57:2070–2077. https://doi.org/10.1212/wnl.57.11.2070

    Article  CAS  PubMed  Google Scholar 

  17. Soetedjo R, Kaneko CRS, Fuchs AF (2002) Evidence that the superior colliculus participates in the feedback control of saccadic eye movements. J Neurophysiol 87:679–695. https://doi.org/10.1152/jn.00886.2000

    Article  PubMed  Google Scholar 

  18. Hanes DP, Smith MK, Optican LM et al (2005) Recovery of saccadic dysmetria following localized lesions in monkey superior colliculus. Exp Brain Res 160:312–325. https://doi.org/10.1007/s00221-004-2013-z

    Article  PubMed  Google Scholar 

  19. Terao Y, Fukuda H, Ugawa Y et al (2013) New perspectives on the pathophysiology of Parkinson’s disease as assessed by saccade performance: a clinical review. Clin Neurophysiol 124:1491–1506. https://doi.org/10.1016/j.clinph.2013.01.021

    Article  PubMed  Google Scholar 

  20. Blekher T, Weaver M, Rupp J et al (2009) Multiple step pattern as a biomarker in Parkinson disease. Parkinsonism Relat Disord 15:506–510. https://doi.org/10.1016/j.parkreldis.2009.01.002

    Article  PubMed  PubMed Central  Google Scholar 

  21. Horn AKE (2006) The reticular formation. Prog Brain Res 151:127–155. https://doi.org/10.1016/S0079-6123(05)51005-7

    Article  PubMed  Google Scholar 

  22. Büttner-Ennever JA, Horn AK, Henn V et al (1999) Projections from the superior colliculus motor map to omnipause neurons in monkey. J Comp Neurol 413:55–67. https://doi.org/10.1002/(sici)1096-9861(19991011)413:1%3c55::aid-cne3%3e3.0.co;2-k

    Article  PubMed  Google Scholar 

  23. Stanton GB, Goldberg ME, Bruce CJ (1988) Frontal eye field efferents in the macaque monkey: II. Topography of terminal fields in midbrain and pons. J Comp Neurol 271:493–506. https://doi.org/10.1002/cne.902710403

    Article  CAS  PubMed  Google Scholar 

  24. Shinoda Y, Sugiuchi Y, Takahashi M et al (2011) Neural substrate for suppression of omnipause neurons at the onset of saccades. Ann N Y Acad Sci 1233:100–106. https://doi.org/10.1111/j.1749-6632.2011.06171.x

    Article  PubMed  Google Scholar 

  25. Sparks D, Rohrer WH, Zhang Y (2000) The role of the superior colliculus in saccade initiation: a study of express saccades and the gap effect. Vis Res 40:2763–2777. https://doi.org/10.1016/s0042-6989(00)00133-4

    Article  CAS  PubMed  Google Scholar 

  26. Bisley JW, Goldberg ME (2010) Attention, intention, and priority in the parietal lobe. Annu Rev Neurosci 33:1–21. https://doi.org/10.1146/annurev-neuro-060909-152823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Pierrot-Deseilligny C, Rosa A, Masmoudi K et al (1991) Saccade deficits after a unilateral lesion affecting the superior colliculus. J Neurol Neurosurg Psychiatry 54:1106–1109. https://doi.org/10.1136/jnnp.54.12.1106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Ghika J, Tennis M, Growdon J et al (1995) Environment-driven responses in progressive supranuclear palsy. J Neurol Sci 130:104–111. https://doi.org/10.1016/0022-510X(95)00015-T

    Article  CAS  PubMed  Google Scholar 

  29. Shires J, Joshi S, Basso MA (2010) Shedding new light on the role of the basal ganglia-superior colliculus pathway in eye movements. Curr Opin Neurobiol 20:717–725. https://doi.org/10.1016/j.conb.2010.08.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Jamadar SD, Fielding J, Egan GF (2013) Quantitative meta-analysis of fMRI and PET studies reveals consistent activation in fronto-striatal-parietal regions and cerebellum during antisaccades and prosaccades. Front Psychol. https://doi.org/10.3389/fpsyg.2013.00749

    Article  PubMed  PubMed Central  Google Scholar 

  31. Kang SS, Dionisio DP, Sponheim SR (2011) Abnormal mechanisms of antisaccade generation in schizophrenia patients and unaffected biological relatives of schizophrenia patients. Psychophysiology 48:350–361. https://doi.org/10.1111/j.1469-8986.2010.01074.x

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurology and Neuropsychology, and CMMR PACA Ouest, CHU Timone, Assistance Publique Hôpitaux de Marseille, Marseille, France

    G. Pin, J. Labouré, O. Felician, M. Ceccaldi & L. Koric

  2. Department of Nuclear Medecine, CHU Timone, Assistance Publique Hôpitaux de Marseille, Marseille, France

    E. Guedj

  3. CERIMED, Aix-Marseille University, Marseille, France

    E. Guedj

  4. Aix-Marseille University, UMR 7249, CNRS, Centrale Marseille, Institut Fresnel, Marseille, France

    E. Guedj & L. Koric

  5. Department of Neurology and Movement Disorders, CHU Timone, Assistance Publique Hôpitaux de Marseille, Marseille, France

    S. Grimaldi & J. P. Azulay

Authors
  1. G. Pin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Labouré
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. Guedj
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. O. Felician
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. Grimaldi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. P. Azulay
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. Ceccaldi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. L. Koric
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

GP: reviewing and editing. JL: conceptualization, data curation, formal analysis, writing original draft, visualization. EG: conceptualization, data curation, formal analysis, writing original draft, supervision. OF: reviewing and editing. SG: reviewing and editing. JPA: reviewing and editing. MC: reviewing and editing. LK: conceptualization, data curation, formal analysis, writing original draft, visualization, supervision.

Corresponding author

Correspondence to G. Pin.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflict of interest. All authors have approved the final article.

Ethical standard statement

Our study was approved by a local expert ethical comity for research study.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pin, G., Labouré, J., Guedj, E. et al. Brain FDG-PET correlates of saccadic disorders in early PSP. J Neurol 270, 4841–4850 (2023). https://doi.org/10.1007/s00415-023-11824-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-023-11824-w

Keywords

Search

Navigation