Skip to main content

Advertisement

SpringerLink
Log in

Extrastriatal dopaminergic and serotonergic pathways in Parkinson’s disease and in dementia with Lewy bodies: a 123I-FP-CIT SPECT study

  • Original Article
  • Published:
European Journal of Nuclear Medicine and Molecular Imaging Aims and scope Submit manuscript

Abstract

Purpose

The aim of the study was to evaluate extrastriatal dopaminergic and serotonergic pathways in patients with Parkinson’s disease (PD) and dementia with Lewy bodies (DLB) using 123I-FP-CIT SPECT imaging.

Methods

The study groups comprised 56 PD patients without dementia, 41 DLB patients and 54 controls. Each patient underwent a standardized neurological examination and 123I-FP-CIT SPECT. Binding in nigrostriatal and extrastriatal regions of interest was calculated in each patient from spatially normalized images. The occipital-adjusted specific to nondisplaceable binding ratio (SBR) in the different regions was compared among the PD patients, DLB patients and controls adjusting for the effects of age, sex, disease duration and serotonergic/dopaminergic treatment. Covariance analysis was used to determine the correlates of local and long-distance regions with extrastriatal 123I-FP-CIT deficits.

Results

Both PD and DLB patients showed lower 123I-FP-CIT SPECT SBR in several regions beyond the nigrostriatal system, especially the insula, cingulate and thalamus. DLB patients showed significantly lower 123I-FP-CIT SBR in the thalamus than controls and PD patients. Thalamic and cingulate 123I-FP-CIT SBR deficits were correlated, respectively, with limbic serotonergic and widespread cortical monoaminergic projections only in DLB patients but exhibited only local correlations in PD patients and controls.

Conclusion

PD and DLB patients both showed insular dopamine deficits, whereas impairment of thalamic serotonergic pathways was specifically associated with DLB. Longitudinal studies are necessary to determine the clinical value of the assessment of extrastriatal 123I-FP-CIT SPECT.

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

Similar content being viewed by others

References

  1. Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W, et al. MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord. 2015;30:1591–601.

    Article  PubMed  Google Scholar 

  2. McKeith IG, Boeve BF, Dickson DW, Halliday G, Taylor J-P, Weintraub D, et al. Diagnosis and management of dementia with Lewy bodies. Neurology. 2017;89(1):88–100. https://doi.org/10.1212/WNL.0000000000004058.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W, et al. Abolishing the 1-year rule: how much evidence will be enough? Mov Disord. 2016;31(11):1623–7. https://doi.org/10.1002/mds.26796.

    Article  PubMed  Google Scholar 

  4. Maetzler W, Pilotto A, Apel A, Deuschle C, Kuebart G, Heinzel S, et al. In vivo markers of Parkinson’s disease and dementia with Lewy bodies: current value of the 5G4 α-synuclein antibody. Acta Neuropathol. 2014;128(6):893–5.

    PubMed  Google Scholar 

  5. Halliday GM, Holton JL, Revesz T, Dickson DW. Neuropathology underlying clinical variability in patients with synucleinopathies. Acta Neuropathol. 2011;122:187–204. https://doi.org/10.1007/s00401-011-0852-9.

    Article  CAS  PubMed  Google Scholar 

  6. Goedert M, Jakes R, Grazia M, Neurosciences C, Building CA. The synucleinopathies: twenty years on. J Parkinsons Dis. 2017;7(s1):S51–69. https://doi.org/10.3233/JPD-179005.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Roselli F, Pisciotta NM, Pennelli M, Aniello MS, Gigante A, De Caro MF, et al. Midbrain SERT in degenerative parkinsonisms: a 123I-FP-CIT SPECT study. Mov Disord. 2010;25:1853–9.

    Article  PubMed  Google Scholar 

  8. Koch W, Unterrainer M, Xiong G, Bartenstein P, Diemling M, Varrone A, et al. Extrastriatal binding of [123I]FP-CIT in the thalamus and pons: gender and age dependencies assessed in a European multicentre database of healthy controls. Eur J Nucl Med Mol Imaging. 2014;41(10):1938–46. https://doi.org/10.1007/s00259-014-2785-8.

    Article  CAS  PubMed  Google Scholar 

  9. Joling M, Vriend C, van der Zande JJ, Lemstra AW, van den Heuvel OA, Booij J, et al. Lower 123I-FP-CIT binding to the striatal dopamine transporter, but not to the extrastriatal serotonin transporter, in Parkinson’s disease compared with dementia with Lewy bodies. Neuroimage Clin. 2018;19:130–6. https://doi.org/10.1016/j.nicl.2018.04.009.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Walker Z, Costa DC, Walker RWH, Lee L, Livingston G, Jaros E, et al. Striatal dopamine transporter in dementia with Lewy bodies and Parkinson disease: a comparison. Neurology. 2004;62(9):1568–72.

    Article  CAS  PubMed  Google Scholar 

  11. Colloby SJ, O’Brien JT, Fenwick JD, Firbank MJ, Burn DJ, McKeith IG, et al. The application of statistical parametric mapping to 123I-FP-CIT SPECT in dementia with Lewy bodies, Alzheimer’s disease and Parkinson’s disease. Neuroimage. 2004;23:956–66.

    Article  PubMed  Google Scholar 

  12. McKeith IG, Dickson DW, Lowe J, Emre M, O’Brien JT, Feldman H, et al. Diagnosis and management of dementia with Lewy bodies: third report of the DLB consortium. Neurology. 2005;65:1863–72. https://doi.org/10.1212/01.wnl.0000187889.17253.b1.

    Article  CAS  PubMed  Google Scholar 

  13. Pilotto A, Turrone R, Liepelt-Scarfone I, Bianchi M, Poli L, Borroni B, et al. Vascular risk factors and cognition in Parkinson’s disease. J Alzheimers Dis. 2016;51:563–70. https://doi.org/10.3233/JAD-150610.

    Article  CAS  PubMed  Google Scholar 

  14. Premi E, Pilotto A, Garibotto V, Bigni B, Turrone R, Alberici A, et al. Impulse control disorder in PD: a lateralized monoaminergic frontostriatal disconnection syndrome? Parkinsonism Relat Disord. 2016;30:62–6. https://doi.org/10.1016/j.parkreldis.2016.05.028.

    Article  CAS  PubMed  Google Scholar 

  15. Emre M, Aarsland D, Brown R, Burn DJ, Duyckaerts C, Mizuno Y, et al. Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord. 2007;22:1689–707. https://doi.org/10.1002/mds.21507.

    Article  Google Scholar 

  16. Bhatia KP, Bain P, Bajaj N, Elble RJ, Hallett M, Louis ED, et al. Consensus statement on the classification of tremors. From the task force on tremor of the International Parkinson and Movement Disorder Society. Mov Disord. 2018;33:75–87. https://doi.org/10.1002/mds.27121.

    Article  PubMed  Google Scholar 

  17. Premi E, Calhoun VD, Garibotto V, Turrone R, Alberici A, Cottini E, et al. Source-based morphometry multivariate approach to analyze [123I]FP-CIT SPECT imaging. Mol Imaging Biol. 2017;19(5):772–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Lancaster JL, Woldorff MG, Parsons LM, Liotti M, Freitas CS, Rainey L, et al. Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp. 2000;10:120–31.

    Article  CAS  PubMed  Google Scholar 

  19. Darcourt J, Booij J, Tatsch K, Varrone A, Vander Borght T, Kapucu ÖL, et al. EANM procedure guidelines for brain neurotransmission SPECT using 123I-labelled dopamine transporter ligands, version 2. Eur J Nucl Med Mol Imaging. 2010;37:443–50.

    Article  CAS  PubMed  Google Scholar 

  20. Calvini P, Rodriguez G, Inguglia F, Mignone A, Guerra UP, Nobili F. The basal ganglia matching tools package for striatal uptake semi-quantification: description and validation. Eur J Nucl Med Mol Imaging. 2007;34:1240–53.

    Article  PubMed  Google Scholar 

  21. Paternicó D, Premi E, Alberici A, Archetti S, Bonomi E, Gualeni V, et al. Dyslexia susceptibility genes influence brain atrophy in frontotemporal dementia. Neurol Genet. 2015;1:e24. https://doi.org/10.1212/NXG.0000000000000024.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Marquie M, Locascio JJ, Rentz DM, Becker JA, Hedden T, Johnson KA, et al. Striatal and extrastriatal dopamine transporter levels relate to cognition in Lewy body diseases: an 11C altropane positron emission tomography study. Alzheimers Res Ther. 2014;6:52. https://doi.org/10.1186/s13195-014-0052-7.

  23. Politis M, Wu K, Loane C, Kiferle L, Molloy S, Brooks DJ, et al. Staging of serotonergic dysfunction in Parkinson’s disease: an in vivo 11C-DASB PET study. Neurobiol Dis. 2010;40:216–21. https://doi.org/10.1016/j.nbd.2010.05.028.

    Article  CAS  PubMed  Google Scholar 

  24. Lewis DA, Melchitzky DS, Sesack SR, Whitehead RE, Auh S, Sampson A. Dopamine transporter immunoreactivity in monkey cerebral cortex: regional, laminar, and ultrastructural localization. J Comp Neurol. 2001;136:119–36.

    Article  Google Scholar 

  25. Papapetropoulos S, Mash DC. Insular pathology in Parkinson’s disease patients with orthostatic hypotension. Parkinsonism Relat Disord. 2007;13:308–11.

    Article  PubMed  Google Scholar 

  26. Christopher L, Koshimori Y, Lang AE, Criaud M, Strafella AP. Uncovering the role of the insula in non-motor symptoms of Parkinson’s disease. Brain. 2014;137:2143–54.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Fathy YY, Jonker AJ, Oudejans E, de Jong FJJ, van Dam AW, Rozemuller AJM, et al. Differential insular cortex subregional vulnerability to α-synuclein pathology in Parkinson’s disease and dementia with Lewy bodies. Neuropathol Appl Neurobiol. 2019;45:262–7. https://doi.org/10.1111/nan.12501.

    Article  CAS  PubMed  Google Scholar 

  28. Roquet D, Noblet V, Anthony P, Philippi N, Cretin B, Martin-Hunyadi C, et al. Insular atrophy at the prodromal stage of dementia with Lewy bodies: a VBM DARTEL study. Sci Rep. 2017;7:9437. https://doi.org/10.1038/s41598-017-08667-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Liepelt-Scarfone I, Pilotto A, Müller K, Bormann C, Gauss K, Wurster I, et al. Autonomic dysfunction in subjects at high risk for Parkinson’s disease. J Neurol. 2015;262(12):2643–52.

    Article  CAS  PubMed  Google Scholar 

  30. Coon EA, Cutsforth-Gregory JK, Benarroch EE. Neuropathology of autonomic dysfunction in synucleinopathies. Mov Disord. 2018;33(3):349–58. https://doi.org/10.1002/mds.27186.

    Article  PubMed  Google Scholar 

  31. Shennhav A, Botvinick M, Cohen JD. The expected value of control: an integrative theory of anterior cingulate cortex function. Neuron. 2013;79:217–40.

    Article  CAS  Google Scholar 

  32. Leech R, Sharp DJ. The role of the posterior cingulate cortex in cognition and disease. Brain. 2014;137:12–32.

    Article  Google Scholar 

  33. Haber SN, Calzavara R. The cortico-basal ganglia integrative network: the role of the thalamus. Brain Res Bull. 2009;78(2-3):69–74.

    Article  PubMed  Google Scholar 

  34. Mitchell AS, Sherman SM, Sommer MA, Mair RG, Vertes RP, Chudasama Y. Advances in understanding mechanisms of thalamic relays in cognition and behavior. J Neurosci. 2014;34:15340–6. https://doi.org/10.1523/JNEUROSCI.3289-14.2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Delli Pizzi S, Franciotti R, Taylor JP, Thomas A, Tartaro A, Onofrj M, et al. Thalamic involvement in fluctuating cognition in dementia with Lewy bodies: magnetic resonance evidences. Cereb Cortex. 2015;25:3682–9.

  36. Watson R, Colloby SJ, Blamire AM, Wesnes KA, Wood J, O’Brien JT. Does attentional dysfunction and thalamic atrophy predict decline in dementia with Lewy bodies? Parkinsonism Relat Disord. 2017;45:69–74. https://doi.org/10.1016/j.parkreldis.2017.10.006.

    Article  PubMed  Google Scholar 

  37. Gazzina S, Premi E, Turrone R, Acosta-Cabronero J, Rizzetti MC, Cotelli MS, et al. Subcortical matter in the α-synucleinopathies spectrum: an MRI pilot study. J Neurol. 2016;263:1575–82. https://doi.org/10.1007/s00415-016-8173-5.

    Article  CAS  PubMed  Google Scholar 

  38. Jellinger KA, Attems J. Does striatal pathology distinguish Parkinson disease with dementia and dementia with Lewy bodies? Acta Neuropathol. 2006;112:253–60.

    Article  PubMed  Google Scholar 

  39. Erskine D, Ding J, Thomas AJ, Kaganovich A, Khundakar AA, Hanson PS, et al. Molecular changes in the absence of severe pathology in the pulvinar in dementia with Lewy bodies. Mov Disord. 2018;33:982–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Stokholm MG, Iranzo A, Østergaard K, Serradell M, Otto M, Bacher Svendsen K, et al. Extrastriatal monoaminergic dysfunction and enhanced microglial activation in idiopathic rapid eye movement sleep behaviour disorder. Neurobiol Dis. 2018;115:9–16. https://doi.org/10.1016/j.nbd.2018.02.017.

    Article  CAS  PubMed  Google Scholar 

  41. Pilotto A, Heinzel S, Suenkel U, Lerche S, Brockmann K, Roeben B, et al. Application of the Movement Disorder Society prodromal Parkinson’s disease research criteria in 2 independent prospective cohorts. Mov Disord. 2017;2:1025–34. https://doi.org/10.1002/mds.27035.

    Article  CAS  Google Scholar 

  42. Moore RY, Whone AL, Brooks DJ. Extrastriatal monoamine neuron function in Parkinson’s disease: an 18F-dopa PET study. Neurobiol Dis. 2008;29:381–90.

    Article  CAS  PubMed  Google Scholar 

  43. Pavese N, Rivero-Bosch M, Lewis SJ, Whone AL, Brooks DJ. Progression of monoaminergic dysfunction in Parkinson’s disease: a longitudinal 18F-dopa PET study. Neuroimage. 2011;56:1463–8.

    Article  CAS  PubMed  Google Scholar 

  44. Albin RL, Koeppe RA, Bohnen NI, Wernette K, Kilbourn MA, Frey KA. Spared caudal brainstem SERT binding in early Parkinson’s disease. J Cereb Blood Flow Metab. 2008;28:441–4.

    Article  CAS  PubMed  Google Scholar 

  45. Pilotto A, Premi E, Paola Caminiti S, Presotto L, Turrone R, Alberici A, et al. Single-subject SPM FDG-PET patterns predict risk of dementia progression in Parkinson disease. Neurology. 2018;90(12):e1029–37. https://doi.org/10.1212/WNL.0000000000005161.

    Article  PubMed  Google Scholar 

  46. Booij J, de Jong J, de Bruin K, Knol R, de Win MM, van Eck-Smit BL. Quantification of striatal dopamine transporters with 123I-FP-CIT SPECT is influenced by the selective serotonin reuptake inhibitor paroxetine: a double-blind, placebo-controlled, crossover study in healthy control subjects. J Nucl Med. 2007;48:359–66.

    CAS  PubMed  Google Scholar 

  47. Koopman KE, la Fleur SE, Fliers E, Serlie MJ, Booij J. Assessing the optimal time point for the measurement of extrastriatal serotonin transporter binding with 123I-FP-CIT SPECT in healthy, male subjects. J Nucl Med. 2012;53:1087–90. https://doi.org/10.2967/jnumed.111.102277.

    Article  CAS  PubMed  Google Scholar 

  48. Matsuoka K, Yasuno F, Shinkai T, Miyasaka T, Takahashi M, Kiuchi K, et al. Test-retest reproducibility of extrastriatal binding with 7#I-FP-CIT SPECT in healthy male subjects. Psychiatry Res Neuroimaging. 2016;258:10–5. https://doi.org/10.1016/j.pscychresns.2016.10.007.

  49. Walker Z, Moreno E, Thomas A, Inglis F, Tabet N, Stevens T, et al. Evolution of clinical features in possible DLB depending on FP-CIT SPECT result. Neurology. 2016;87:1045–51.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Iranzo A, Valldeoriola F, Lomeña F, Molinuevo JL, Serradell M, Salamero M, et al. Serial dopamine transporter imaging of nigrostriatal function in patients with idiopathic rapid-eye-movement sleep behaviour disorder: a prospective study. Lancet Neurol. 2011;10:797–805. https://doi.org/10.1016/S1474-4422(11)70152-1.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Neurology Unit, Department of Clinical and Experimental Sciences, University of Brescia, P.zzale Spedali Civili, 1, 25123, Brescia, Italy

    Andrea Pilotto, Francesca Schiano di Cola, Enrico Premi, Roberto Grasso, Rosanna Turrone, Stefano Gipponi, Andrea Scalvini, Elisabetta Cottini, Barbara Borroni & Alessandro Padovani

  2. Parkinson’s Disease Rehabilitation Centre, FERB ONLUS – S. Isidoro Hospital, Trescore Balneario, BG, Italy

    Andrea Pilotto & Maria Cristina Rizzetti

  3. Stroke Unit, Azienda Socio Sanitaria Territoriale Spedali Civili, Spedali Civili Hospital, Brescia, Italy

    Enrico Premi

  4. Nuclear Medicine Unit, University of Brescia, Brescia, Italy

    Barbara Paghera

  5. Department of Medical Imaging, Geneva University Hospital, Geneva, Switzerland

    Valentina Garibotto

  6. Department of Neuroscience Imaging and Clinical Sciences, University G. d’Annunzio of Chieti-Pescara, Chieti, Italy

    Laura Bonanni

  7. Nuclear Medicine Unit, Department of Health Sciences, University of Genoa, Genoa, Italy

    Silvia Morbelli

  8. IRCCS ospedale Policlinico San Martino, Genoa, Italy

    Silvia Morbelli & Flavio Nobili

  9. Department of Neuroscience (DINOGMI), University of Genoa, Genoa, Italy

    Flavio Nobili

  10. Nuclear Medicine Unit, Poliambulanza Hospital, Brescia, Italy

    Ugo Paolo Guerra

  11. Nuclear Medicine Unit San Raffaele Hospital, Division of Neuroscience San Raffaele Scientific Institute, Milan, Italy

    Daniela Perani

Authors
  1. Andrea Pilotto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Francesca Schiano di Cola
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Enrico Premi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Roberto Grasso
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rosanna Turrone
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stefano Gipponi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Andrea Scalvini
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Elisabetta Cottini
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Barbara Paghera
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Valentina Garibotto
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Maria Cristina Rizzetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Laura Bonanni
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Barbara Borroni
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Silvia Morbelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Flavio Nobili
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Ugo Paolo Guerra
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Daniela Perani
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Alessandro Padovani
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Andrea Pilotto: study concept and design, acquisition of data, statistical analysis design and execution, interpretation of data, drafting/revising the manuscript for content.

Francesca Schiano di Cola: acquisition of data, statistical analysis execution, interpretation of data, drafting/revising the manuscript for content.

Enrico Premi: statistical analysis design and interpretation of data, revising the manuscript for content.

Roberto Grasso: acquisition of data, revising the manuscript for content.

Rosanna Turrone: acquisition of data, revising the manuscript for content.

Stefano Gipponi: acquisition of data, revising the manuscript for content.

Andrea Scalvini acquisition of data, revising the manuscript for content.

Elisabetta Cottini: acquisition of data, revising the manuscript for content.

Barbara Paghera: acquisition of data, revising the manuscript for content.

Valentina Garibotto: revising the manuscript for content.

Maria Cristina Rizzetti: revising the manuscript for content.

Laura Bonanni: revising the manuscript for content.

Barbara Borroni: revising the manuscript for content.

Silvia Morbelli: revising the manuscript for content.

Flavio Nobili: revising the manuscript for content.

Ugo Paolo Guerra: revising the manuscript for content.

Daniela Perani: revising the manuscript for content.

Alessandro Padovani: study concept and design, acquisition of data, analysis and interpretation of data, drafting/revising the manuscript for content.

Corresponding author

Correspondence to Andrea Pilotto.

Ethics declarations

Conflicts of interest

Andrea Pilotto received speaker honoraria from BioMarin Pharmaceutical, Chiesi Pharmaceuticals, Nutricia Pharmaceuticals, UCB Pharma and Zambon Pharmaceuticals. He received travel grants from AbbVie Pharmaceuticals, BioMarin Pharmaceutical, Nutricia Pharmaceuticals, Zambon Pharmaceuticals and the Italian Movement Disorder Society.

Valentina Garibotto is funded by a grant from the Swiss National Science Foundation (SNF 320030_169876) and from the Velux Foundation (project 1123).

Silvia Morbelli acted as consultant for Eli Lilly in 2014 and for Avid Radiopharmaceuticals in 2016. She received speaker honoraria from General Electric Healthcare in 2017.

Daniela Perani is funded by a grant from Fondazione Cariplo, Bando Ricerca 2014 Malattie Invecchiamento, project title “Evaluation of autonomic, genetic, imaging and biochemical markers for Parkinson-related dementia,” 2015–2017, and the EU FP7 INMIND project (FP7-HEALTH-2013, grant agreement 278,850).

Alessandro Padovani is a consultant for and served on the scientific advisory board of GE Healthcare, Eli Lilly, and Actelion Ltd. Pharmaceuticals, received speaker honoraria from Nutricia, PIAM, Langstone Technology, GE Healthcare, Lilly, UCB Pharma, Zambon and Chiesi Pharmaceuticals. He is funded by a grant from the Ministry of University and Research (MURST).

All other authors declare no conflicts of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the principles of the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pilotto, A., Schiano di Cola, F., Premi, E. et al. Extrastriatal dopaminergic and serotonergic pathways in Parkinson’s disease and in dementia with Lewy bodies: a 123I-FP-CIT SPECT study. Eur J Nucl Med Mol Imaging 46, 1642–1651 (2019). https://doi.org/10.1007/s00259-019-04324-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00259-019-04324-5

Keywords

Search

Navigation