Skip to main content

Advertisement

SpringerLink
Log in

What can we learn from fMRI capture of visual hallucinations in Parkinson’s disease?

  • Brief Communication
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

With disease progression, patients with Parkinson’s disease (PD) may have chronic visual hallucinations (VH). The mechanisms behind this invalidating non-motor symptom remain largely unknown, namely because it is extremely difficult to capture hallucination events. This study aimed to describe the patterns of brain functional changes when VH occur in PD patients. Nine PD patients were enrolled because of their frequent and chronic VH (> 10/day). Patients with severe cognitive decline (MMSE<18) were excluded. Patients were scanned during ON/OFF hallucinatory states and resting-state functional imaging (rs-fMRI) was performed. Data were analyzed in reference to the two-step method, which consists in: (i) a data-driven analysis of per-hallucinatory fMRI data, and (ii) selection of the components of interest based on a post-fMRI interview. The phenomenology of VH ranged from visual spots to distorting faces. First, at the individual level, several VH-related components of interest were identified and integrated in a second-level analysis. Using a random-effects self-organizing-group ICA, we evidenced increased connectivity in visual networks concomitant to VH, encompassing V2, V3 and the fusiform gyri bilaterally. Interestingly, the stability of the default-mode network (DMN) was found positively correlated with VH severity (Spearman’s rho = 0.77, p = 0.05). By using a method that does not need online self-report, we showed that VH in PD patients were associated with functional changes in associative visual cortices, possibly linked with strengthened stability of resting-state networks.

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

References

  • Burn, D., Emre, M., McKeith, I., De Deyn, P. P., Aarsland, D., Hsu, C., & Lane, R. (2006). Effects of rivastigmine in patients with and without visual hallucinations in dementia associated with Parkinson's disease. Movement Disorders, 21, 1899–1907.

    Article  Google Scholar 

  • De Martino, F., Gentile, F., Esposito, F., Balsi, M., Di Salle, F., Goebel, R., & Formisano, E. (2007). Classification of fMRI independent components using IC-fingerprints and support vector machine classifiers. Neuroimage, 34, 177–194.

    Article  Google Scholar 

  • de Medeiros, K., Robert, P., Gauthier, S., Stella, F., Politis, A., Leoutsakos, J., Taragano, F., Kremer, J., Brugnolo, A., Porsteinsson, A. P., Geda, Y. E., Brodaty, H., Gazdag, G., Cummings, J., & Lyketsos, C. (2010). The neuropsychiatric inventory-clinician rating scale (NPI-C): Reliability and validity of a revised assessment of neuropsychiatric symptoms in dementia. International Psychogeriatrics, 22, 984–994.

    Article  Google Scholar 

  • Diederich, N. J., Goetz, C. G., & Stebbins, G. T. (2005). Repeated visual hallucinations in Parkinson's disease as disturbed external/internal perceptions: Focused review and a new integrative model. Movement Disorders, 20, 130–140.

    Article  Google Scholar 

  • Diederich, N. J., Fenelon, G., Stebbins, G., & Goetz, C. G. (2009). Hallucinations in Parkinson disease. Nature Reviews. Neurology, 5, 331–342.

    Article  CAS  Google Scholar 

  • Esposito, F., Scarabino, T., Hyvarinen, A., Himberg, J., Formisano, E., Comani, S., Tedeschi, G., Goebel, R., Seifritz, E., & Di Salle, F. (2005). Independent component analysis of fMRI group studies by self-organizing clustering. Neuroimage, 25, 193–205.

    Article  Google Scholar 

  • Fenelon, G., & Alves, G. (2010). Epidemiology of psychosis in Parkinson's disease. Journal of the Neurological Sciences, 289, 12–17.

    Article  Google Scholar 

  • Fénelon, G., Mahieux, F., Huon, R., & Ziégler, M. (2000). Hallucinations in Parkinson's disease: Prevalence, phenomenology and risk factors. Brain, 123(Pt 4), 733–745.

    Article  Google Scholar 

  • Ffytche, D. H., & Aarsland, D. (2017). Psychosis in Parkinson's disease. International Review of Neurobiology, 133, 585–622.

    Article  Google Scholar 

  • Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198.

    Article  CAS  Google Scholar 

  • Formisano, E., Esposito, F., Di Salle, F., & Goebel, R. (2004). Cortex-based independent component analysis of fMRI time series. Magnetic Resonance Imaging, 22, 1493–1504.

    Article  Google Scholar 

  • Friedman, J. H. (2010). Parkinson's disease psychosis 2010: A review article. Parkinsonism & Related Disorders, 16, 553–560.

    Article  Google Scholar 

  • Gibb, W. R., & Lees, A. J. (1988). The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson's disease. Journal of Neurology, Neurosurgery, and Psychiatry, 51, 745–752.

    Article  CAS  Google Scholar 

  • Goetz, C. G., Tilley, B. C., Shaftman, S. R., Stebbins, G. T., Fahn, S., Martinez-Martin, P., Poewe, W., Sampaio, C., Stern, M. B., Dodel, R., Dubois, B., Holloway, R., Jankovic, J., Kulisevsky, J., Lang, A. E., Lees, A., Leurgans, S., LeWitt, P. A., Nyenhuis, D., Olanow, C. W., Rascol, O., Schrag, A., Teresi, J. A., van Hilten, J. J., LaPelle, N., & Movement Disorder Society UPDRS Revision Task Force. (2008). Movement Disorder Society-sponsored revision of the unified Parkinson's disease rating scale (MDS-UPDRS): Scale presentation and clinimetric testing results. Movement Disorders, 23, 2129–2170.

    Article  Google Scholar 

  • Goetz, C. G., Vaughan, C. L., Goldman, J. G., & Stebbins, G. T. (2014). I finally see what you see: Parkinson's disease visual hallucinations captured with functional neuroimaging. Movement Disorders, 29, 115–117.

    Article  Google Scholar 

  • Jardri, R., Thomas, P., Delmaire, C., Delion, P., & Pins, D. (2013). The neurodynamic organization of modality-dependent hallucinations. Cerebral Cortex, 23, 1108–1117.

    Article  Google Scholar 

  • Lee, J.-Y., Kim, J. M., Ahn, J., Kim, H.-J., Jeon, B. S., & Kim, T. W. (2014). Retinal nerve fiber layer thickness and visual hallucinations in Parkinson's disease. Movement Disorders, 29, 61–67.

    Article  Google Scholar 

  • Lefebvre, S., Demeulemeester, M., Leroy, A., Delmaire, C., Lopes, R., Pins, D., Thomas, P., & Jardri, R. (2016). Network dynamics during the different stages of hallucinations in schizophrenia. Human Brain Mapping, 37, 2571–2586.

    Article  Google Scholar 

  • Lenka, A., Jhunjhunwala, K. R., Saini, J., & Pal, P. K. (2015). Structural and functional neuroimaging in patients with Parkinson's disease and visual hallucinations: A critical review. Parkinsonism & Related Disorders, 21, 683–691.

    Article  Google Scholar 

  • Leroy, A., Foucher, J. R., Pins, D., Delmaire, C., Thomas, P., Roser, M. M., Lefebvre, S., Amad, A., Fovet, T., Jaafari, N., & Jardri, R. (2017). fMRI capture of auditory hallucinations: Validation of the two-steps method. Human Brain Mapping, 38, 4966–4979.

    Article  Google Scholar 

  • Martinez-Martin, P., Schapira, A. H. V., Stocchi, F., Sethi, K., Odin, P., MacPhee, G., Brown, R. G., Naidu, Y., Clayton, L., Abe, K., Tsuboi, Y., MacMahon, D., Barone, P., Rabey, M., Bonuccelli, U., Forbes, A., Breen, K., Tluk, S., Olanow, C. W., Thomas, S., Rye, D., Hand, A., Williams, A. J., Ondo, W., & Chaudhuri, K. R. (2007). Prevalence of nonmotor symptoms in Parkinson's disease in an international setting; study using nonmotor symptoms questionnaire in 545 patients. Movement Disorders, 22, 1623–1629.

    Article  Google Scholar 

  • Mattis, S. (1976). Mental status examination for organic mental syndrome in the elderly patient. In L. T. K. Bellak (Ed.), Geriatric psychiatry (pp. 77–121). New York: Grune and Stratton.

    Google Scholar 

  • Milner, A. D. (2017). How do the two visual streams interact with each other? Experimental Brain Research, 235, 1297–1308.

    Article  CAS  Google Scholar 

  • Montgomery SA, Asberg M (1979) A new depression scale designed to be sensitive to change. The British journal of psychiatry.

  • Muller, A. J., Shine, J. M., Halliday, G. M., & Lewis, S. J. G. (2014). Visual hallucinations in Parkinson's disease: Theoretical models. Movement Disorders, 29, 1591–1598.

    Article  Google Scholar 

  • Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97–113.

    Article  CAS  Google Scholar 

  • Papapetropoulos, S., Katzen, H., Schrag, A., Singer, C., Scanlon, B. K., Nation, D., Guevara, A., & Levin, B. (2008). A questionnaire-based (UM-PDHQ) study of hallucinations in Parkinson's disease. BMC Neurology, 8, 21.

    Article  Google Scholar 

  • Pieri, V., Diederich, N. J., Raman, R., & Goetz, C. G. (2000). Decreased color discrimination and contrast sensitivity in Parkinson's disease. Journal of the Neurological Sciences, 172, 7–11.

    Article  CAS  Google Scholar 

  • Shine, J. M., Halliday, G. M., Gilat, M., Matar, E., Bolitho, S. J., Carlos, M., Naismith, S. L., & Lewis, S. J. G. (2014). The role of dysfunctional attentional control networks in visual misperceptions in Parkinson's disease. Human Brain Mapping, 35, 2206–2219.

    Article  Google Scholar 

  • Shine, J. M., Muller, A. J., O'Callaghan, C., Hornberger, M., Halliday, G. M., & Lewis, S. J. (2015). Abnormal connectivity between the default mode and the visual system underlies the manifestation of visual hallucinations in Parkinson's disease: A task-based fMRI study. NPJ Parkinsons Dis, 1, 15003.

    Article  Google Scholar 

  • Swann, P., & O'Brien, J. T. (2018). Management of visual hallucinations in dementia and Parkinson's disease. International Psychogeriatrics, 1–22.

  • Tomlinson, C. L., Stowe, R., Patel, S., Rick, C., Gray, R., & Clarke, C. E. (2010). Systematic review of levodopa dose equivalency reporting in Parkinson's disease. Movement Disorders, 25, 2649–2653.

    Article  Google Scholar 

  • Weil, R. S., Schrag, A. E., Warren, J. D., Crutch, S. J., Lees, A. J., & Morris, H. R. (2016). Visual dysfunction in Parkinson's disease. Brain, 139, 2827–2843.

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank Anne-Sophie Carette and Lucie Plomhause for their help in neuropsychological assessment.

Funding

This study was funded by the Structure Fédérative de Recherche Démence des Maladies Neurologiques et Mentales (DN2M), Lille, France, the European Regional Development Fund (FEDER-Région Nord-Pas-de-Calais, France) and the France Parkinson charity. The sponsors were not involved in the study design or in data interpretation, writing of the report or decision to submit the article for publication.

Author information

Authors and Affiliations

  1. Inserm, U1171 - Degenerative & Vascular Cognitive Disorders, University of Lille, F-59000, Lille, France

    Kathy Dujardin, Guillaume Baille & Luc Defebvre

  2. Neurology and Movement Disorders Department, CHU Lille, F-59000, Lille, France

    Kathy Dujardin, Guillaume Baille & Luc Defebvre

  3. Psychiatry Department, CHU Lille, F-59000, Lille, France

    David Roman & Renaud Jardri

  4. CNRS, UMR 9193 - Cognitive and Affective Sciences - SCALab, University of Lille, F-59000, Lille, France

    Delphine Pins, Stéphanie Lefebvre & Renaud Jardri

  5. Neuroimaging Department, CHU Lille, F-59000, Lille, France

    Christine Delmaire

Authors
  1. Kathy Dujardin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David Roman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guillaume Baille
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Delphine Pins
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stéphanie Lefebvre
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Christine Delmaire
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luc Defebvre
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Renaud Jardri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kathy Dujardin.

Ethics declarations

Conflict of interest

The authors have no conflict of interest to declare.

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 1964 Helsinki declaration 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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dujardin, K., Roman, D., Baille, G. et al. What can we learn from fMRI capture of visual hallucinations in Parkinson’s disease?. Brain Imaging and Behavior 14, 329–335 (2020). https://doi.org/10.1007/s11682-019-00185-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-019-00185-6

Keywords

Search

Navigation