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Imaging correlates of depression in progressive supranuclear palsy

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Abstract

Depression is highly common in Progressive Supranuclear Palsy (PSP) and is a meaningful determinant of quality of life. However, neurobiological and neuroimaging correlates of this neuropsychiatric disturbance in PSP patients are still unknown. In this study, we aimed to investigate the topographical distribution of morphometric changes associated with depression in PSP patients using cortical thickness. Forty patients with PSP were evaluated at baseline with clinical rating scales and MRI scans. Based on the response to the 15-item Geriatric Depression Scale we identified 21 PSP patients with depression (GDS-15 score ≥ 5) and 19 PSP patients without depression (GDS-15 score < 5). In vertex-wise analysis, comparison of cortical thickness between PSP patients with and without depression was performed using a general linear model. PSP patients with depressions showed reduced cortical thickness in temporo-parieto-occipital areas, more pronounced in the right hemisphere. These findings propose neurobiological conceptualizations of depression in PSP as being associated with a multiregional pattern of morphometric grey matter reduction.

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References

  1. Boxer AL, Yu JT, Golbe LI, Litvan I, Lang AE, Höglinger GU (2017) Advances in progressive supranuclear palsy: new diagnostic criteria, biomarkers, and therapeutic approaches. Lancet Neurol 16(7):552–563

    Article  PubMed  PubMed Central  Google Scholar 

  2. Hauw JJ, Daniel SE, Dickson D, Horoupian DS, Jellinger K, Lantos PL et al (1994) Preliminary NINDS neuropathologic criteria for Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Neurology 44(11):2015–2019

    Article  CAS  PubMed  Google Scholar 

  3. Jellinger KA, Bancher C, Hauw JJ, Verny M (1995) Progressive supranuclear palsy: neuropathologically based diagnostic clinical criteria. J Neurol Neurosurg Psychiatry 59(1):106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bloise MC, Berardelli I, Roselli V, Pasquini M, Stirpe P, Colosimo C et al (2014) Psychiatric disturbances in patients with progressive supranuclear palsy: a case-control study. Parkinsonism Relat Disord 20(9):965–968

    Article  PubMed  Google Scholar 

  5. Santangelo G, Cuoco S, Pellecchia MT, Erro R, Barone P, Picillo M (2018) Comparative cognitive and neuropsychiatric profiles between Parkinson’s disease, multiple system atrophy and progressive supranuclear palsy. J Neurol 265(11):2602–2613

    Article  PubMed  Google Scholar 

  6. Esmonde T, Giles E, Gibson M, Hodges JR (1996) Neuropsychological performance, disease severity, and depression in progressive supranuclear palsy. J Neurol 243(9):638–643

    Article  CAS  PubMed  Google Scholar 

  7. Radicati FG, Martinez Martin P, Fossati C, Chaudhuri KR, Torti M, Rodriguez Blazquez C et al (2017) Non motor symptoms in progressive supranuclear palsy: prevalence and severity. NPJ Parkinsons Dis 3:35

    Article  PubMed  PubMed Central  Google Scholar 

  8. Flavell J, Nestor PJ (2021) A systematic review of apathy and depression in progressive supranuclear palsy. J Geriatr Psychiatry Neurol. https://doi.org/10.1177/0891988721993545

    Article  PubMed  Google Scholar 

  9. Winter Y, Spottke AE, Stamelou M, Cabanel N, Eggert K, Höglinger GU et al (2011) Health-related quality of life in multiple system atrophy and progressive supranuclear palsy. Neurodegener Dis 8(6):438–446

    Article  PubMed  Google Scholar 

  10. Aarsland D, Litvan I, Larsen JP (2001) Neuropsychiatric symptoms of patients with progressive supranuclear palsy and Parkinson’s disease. J Neuropsychiatry Clin Neurosci 13(1):42–49

    Article  CAS  PubMed  Google Scholar 

  11. Painous C, Martí MJ, Simonet C, Garrido A, Valldeoriola F, Muñoz E et al (2020) Prediagnostic motor and non-motor symptoms in progressive supranuclear palsy: the step-back PSP study. Parkinsonism Relat Disord 74:67–73

    Article  PubMed  Google Scholar 

  12. Schrag A, Sheikh S, Quinn NP, Lees AJ, Selai C, Mathias C et al (2010) A comparison of depression, anxiety, and health status in patients with progressive supranuclear palsy and multiple system atrophy. Mov Disord 25(8):1077–1081

    Article  PubMed  Google Scholar 

  13. Tsai RM, Lobach I, Bang J, Whitwell JL, Senjem ML, Jack CR Jr et al (2016) Clinical correlates of longitudinal brain atrophy in progressive supranuclear palsy. Parkinsonism Relat Disord 28:29–35

    Article  PubMed  PubMed Central  Google Scholar 

  14. Bang J, Lobach IV, Lang AE, Grossman M, Knopman DS, Miller BL et al (2016) Predicting disease progression in progressive supranuclear palsy in multicenter clinical trials. Parkinsonism Relat Disord 28:41–48

    Article  PubMed  PubMed Central  Google Scholar 

  15. Lamb R, Rohrer JD, Lees AJ, Morris HR (2016) Progressive supranuclear palsy and corticobasal degeneration: pathophysiology and treatment options. Curr Treat Options Neurol 18(9):42

    Article  PubMed  PubMed Central  Google Scholar 

  16. Wise T, Cleare AJ, Herane A, Young AH, Arnone D (2014) Diagnostic and therapeutic utility of neuroimaging in depression: an overview. Neuropsychiatr Dis Treat 10:1509–1522

    PubMed  PubMed Central  Google Scholar 

  17. Kandilarova S, Stoyanov D, Sirakov N, Maes M, Specht K (2019) Reduced grey matter volume in frontal and temporal areas in depression: contributions from voxel-based morphometry study. Acta Neuropsychiatr 31(5):252–257

    Article  PubMed  Google Scholar 

  18. Arnone D, Job D, Selvaraj S, Abe O, Amico F, Cheng Y et al (2016) Computational meta-analysis of statistical parametric maps in major depression. Hum Brain Mapp 37(4):1393–1404

    Article  PubMed  PubMed Central  Google Scholar 

  19. Chagas MH, Linares IM, Garcia GJ, Hallak JE, Tumas V, Crippa JA (2013) Neuroimaging of depression in Parkinson’s disease: a review. Int Psychogeriatr 25(12):1953–1961

    Article  PubMed  Google Scholar 

  20. 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(1):42–46

    Article  PubMed  Google Scholar 

  21. Abé C, Ekman CJ, Sellgren C, Petrovic P, Ingvar M, Landén M (2016) Cortical thickness, volume and surface area in patients with bipolar disorder types I and II. J Psychiatry Neurosci 41(4):240–250

    Article  PubMed  Google Scholar 

  22. Zuo Z, Ran S, Wang Y, Li C, Han Q, Tang Q et al (2019) Asymmetry in cortical thickness and subcortical volume in treatment-naïve major depressive disorder. NeuroImage Clinical. 21:101614

    Article  PubMed  Google Scholar 

  23. Niu M, Wang Y, Jia Y, Wang J, Zhong S, Lin J et al (2017) Common and specific abnormalities in cortical thickness in patients with major depressive and bipolar disorders. EBioMedicine 16:162–171

    Article  PubMed  PubMed Central  Google Scholar 

  24. Peterson BS, Weissman MM (2011) A brain-based endophenotype for major depressive disorder. Annu Rev Med 62:461–474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC 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):1–9

    Article  CAS  PubMed  Google Scholar 

  26. Boxer AL, Lang AE, Grossman M, Knopman DS, Miller BL, Schneider LS et al (2014) Davunetide in patients with progressive supranuclear palsy: a randomised, double-blind, placebo-controlled phase 2/3 trial. Lancet Neurol 13(7):676–685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12(3):189–198

    Article  CAS  PubMed  Google Scholar 

  28. Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, 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(15):2129–2170

    Article  PubMed  Google Scholar 

  29. Golbe LI, Ohman-Strickland PA (2007) A clinical rating scale for progressive supranuclear palsy. Brain 130(Pt 6):1552–1565

    Article  PubMed  Google Scholar 

  30. Morris JC (1993) The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology 43(11):2412–2414

    Article  CAS  PubMed  Google Scholar 

  31. Pfeffer RI, Kurosaki TT, Harrah CH Jr, Chance JM, Filos S (1982) Measurement of functional activities in older adults in the community. J Gerontol 37(3):323–329

    Article  CAS  PubMed  Google Scholar 

  32. Yesavage JA, Brink TL, Rose TL, Lum O, Huang V, Adey M et al (1982) Development and validation of a geriatric depression screening scale: a preliminary report. J Psychiatr Res 17(1):37–49

    Article  PubMed  Google Scholar 

  33. Dahnke R, Yotter RA, Gaser C (2013) Cortical thickness and central surface estimation. Neuroimage 65:336–348

    Article  PubMed  Google Scholar 

  34. Goel V, Gold B, Kapur S, Houle S (1998) Neuroanatomical correlates of human reasoning. J Cogn Neurosci 10(3):293–302

    Article  CAS  PubMed  Google Scholar 

  35. Pourtois G, de Gelder B, Bol A, Crommelinck M (2005) Perception of facial expressions and voices and of their combination in the human brain. Cortex 41(1):49–59

    Article  PubMed  Google Scholar 

  36. Wildgruber D, Riecker A, Hertrich I, Erb M, Grodd W, Ethofer T et al (2005) Identification of emotional intonation evaluated by fMRI. Neuroimage 24(4):1233–1241

    Article  CAS  PubMed  Google Scholar 

  37. Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain’s default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 1124:1–38

    Article  PubMed  Google Scholar 

  38. Ferri J, Schmidt J, Hajcak G, Canli T (2016) Emotion regulation and amygdala-precuneus connectivity: focusing on attentional deployment. Cogn Affect Behav Neurosci 16(6):991–1002

    Article  PubMed  Google Scholar 

  39. Mulders PC, van Eijndhoven PF, Schene AH, Beckmann CF, Tendolkar I (2015) Resting-state functional connectivity in major depressive disorder: a review. Neurosci Biobehav Rev 56:330–344

    Article  PubMed  Google Scholar 

  40. Zanigni S, Sambati L, Evangelisti S, Testa C, Calandra-Buonaura G, Manners DN et al (2017) Precuneal thickness and depression in parkinson disease. Neurodegener Dis 17(2–3):97–102

    Article  PubMed  Google Scholar 

  41. Brenneis C, Seppi K, Schocke M, Benke T, Wenning GK, Poewe W (2004) Voxel based morphometry reveals a distinct pattern of frontal atrophy in progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 75(2):246–249

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Cordato NJ, Pantelis C, Halliday GM, Velakoulis D, Wood SJ, Stuart GW et al (2002) Frontal atrophy correlates with behavioural changes in progressive supranuclear palsy. Brain 125(Pt 4):789–800

    Article  CAS  PubMed  Google Scholar 

  43. Blin J, Baron JC, Dubois B, Pillon B, Cambon H, Cambier J et al (1990) Positron emission tomography study in progressive supranuclear palsy. Brain hypometabolic pattern and clinicometabolic correlations. Arch Neurol 47(7):747–752

    Article  CAS  PubMed  Google Scholar 

  44. Mackin RS, Tosun D, Mueller SG, Lee J-Y, Insel P, Schuff N et al (2013) Patterns of reduced cortical thickness in late-life depression and relationship to psychotherapeutic response. Am J Geriatr Psychiatry 21(8):794–802

    Article  PubMed  Google Scholar 

  45. 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

    Article  CAS  PubMed  Google Scholar 

  46. Murley AG, Rowe JB (2018) Neurotransmitter deficits from frontotemporal lobar degeneration. Brain 141(5):1263–1285

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Data used in preparation of this article were obtained from the 4-Repeat Tauopathy Neuroimaging Initiative (4RTNI) database (http://4rtni-ftldni.ini.usc.edu). The investigators at 4RTNI contributed to the design and implementation of 4RTNI and/or provided data, but did not participate in analysis or writing of this report (unless otherwise listed).

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Author notes

  1. Daniele Urso, Benedetta Tafuri have contributed equally.

Authors and Affiliations

  1. Department of Clinical Research in Neurology, Center for Neurodegenerative Diseases and the Aging Brain, University of Bari ‘Aldo Moro’, “Pia Fondazione Cardinale G. Panico”, Tricase, Lecce, Italy

    Daniele Urso, Benedetta Tafuri, Salvatore Nigro & Giancarlo Logroscino

  2. Department of Neurosciences, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, De Crespigny Park, London, UK

    Daniele Urso

  3. Department of Basic Medicine, Neuroscience, and Sense Organs, University of Bari ‘Aldo Moro’, Bari, Italy

    Benedetta Tafuri & Giancarlo Logroscino

  4. Department of Diagnostic Imaging, Pia Fondazione di Culto e Religione “Card. G. Panico”, Tricase, Italy

    Roberto De Blasi

  5. Institute of Nanotechnology (NANOTEC), National Research Council, Lecce, Italy

    Salvatore Nigro

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  1. Daniele Urso
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for the 4-Repeat Tauopathy Neuroimaging Initiative

Corresponding author

Correspondence to Giancarlo Logroscino.

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Ethical approval

Approval for the 4RTNI protocol has been granted by institutional review board at the study site. Research involves only previously collected and fully anonymised data so further ethical approval was not required.

Additional information

Data used in preparation of this article were obtained from the 4-Repeat Tauopathy Neuroimaging Initiative (4RTNI) database (http://4rtni-ftldni.ini.usc.edu). The investigators at 4RTNI contributed to the design and implementation of 4RTNI and/or provided data, but did not participate in analysis or writing of this report (unless otherwise listed).

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Urso, D., Tafuri, B., De Blasi, R. et al. Imaging correlates of depression in progressive supranuclear palsy. J Neurol 269, 3522–3528 (2022). https://doi.org/10.1007/s00415-021-10939-2

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  • DOI: https://doi.org/10.1007/s00415-021-10939-2

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