Neuroanatomical and cognitive correlates of visual hallucinations in Parkinson's disease and dementia with Lewy bodies: Voxel-based morphometry and neuropsychological meta-analysis

Stefania Pezzoli; Raquel Sánchez-Valle; Aleix Solanes; Matthew J. Kempton; Oliver Bandmann; Jae Il Shin; Annachiara Cagnin; Jennifer G. Goldman; Doug Merkitch; Michael J. Firbank; John Paul Taylor; Javier Pagonabarraga; Jaime Kulisevsky; Frederic Blanc; Norma Verdolini; Annalena Venneri; Joaquim Radua

doi:10.1016/j.neubiorev.2021.06.030

Neuroanatomical and cognitive correlates of visual hallucinations in Parkinson's disease and dementia with Lewy bodies: Voxel-based morphometry and neuropsychological meta-analysis

Stefania Pezzoli, Raquel Sánchez-Valle, Aleix Solanes, Matthew J. Kempton, Oliver Bandmann, Jae Il Shin, Annachiara Cagnin, Jennifer G. Goldman, Doug Merkitch, Michael J. Firbank, John Paul Taylor, Javier Pagonabarraga, Jaime Kulisevsky, Frederic Blanc, Norma Verdolini, Annalena Venneri, Joaquim Radua^*

^*Corresponding author for this work

Research output: Contribution to journal › Review article › peer-review

19 Citations (Scopus)

Abstract

Visual hallucinations (VH) are common in Parkinson's disease and dementia with Lewy bodies, two forms of Lewy body disease (LBD), but the neural substrates and mechanisms involved are still unclear. We conducted meta-analyses of voxel-based morphometry (VBM) and neuropsychological studies investigating the neuroanatomical and cognitive correlates of VH in LBD. For VBM (12 studies), we used Seed-based d Mapping with Permutation of Subject Images (SDM-PSI), including statistical parametric maps for 50% of the studies. For neuropsychology (35 studies), we used MetaNSUE to consider non-statistically significant unreported effects. VH were associated with smaller grey matter volume in occipital, frontal, occipitotemporal, and parietal areas (peak Hedges’ g -0.34 to -0.49). In patients with Parkinson's disease without dementia, VH were associated with lower verbal immediate memory performance (Hedges’ g -0.52). Both results survived correction for multiple comparisons. Abnormalities in these brain regions might reflect dysfunctions in brain networks sustaining visuoperceptive, attention, and executive abilities, with the latter also being at the basis of poor immediate memory performance.

Original language	English
Pages (from-to)	367-382
Number of pages	16
Journal	Neuroscience and Biobehavioral Reviews
Volume	128
DOIs	https://doi.org/10.1016/j.neubiorev.2021.06.030
Publication status	Published - Sept 2021

Keywords

Dementia with Lewy bodies
Grey matter volume
Lewy body disease
Memory
Meta-analysis
MRI
Neuropsychology
Parkinson's disease
VBM
Visual hallucinations

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10.1016/j.neubiorev.2021.06.030

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Pezzoli, S., Sánchez-Valle, R., Solanes, A., Kempton, M. J., Bandmann, O., Shin, J. I., Cagnin, A., Goldman, J. G., Merkitch, D., Firbank, M. J., Taylor, J. P., Pagonabarraga, J., Kulisevsky, J., Blanc, F., Verdolini, N., Venneri, A., & Radua, J. (2021). Neuroanatomical and cognitive correlates of visual hallucinations in Parkinson's disease and dementia with Lewy bodies: Voxel-based morphometry and neuropsychological meta-analysis. Neuroscience and Biobehavioral Reviews, 128, 367-382. https://doi.org/10.1016/j.neubiorev.2021.06.030

@article{5f3cdac696ce4b03926ed39f67f26c39,

title = "Neuroanatomical and cognitive correlates of visual hallucinations in Parkinson's disease and dementia with Lewy bodies: Voxel-based morphometry and neuropsychological meta-analysis",

abstract = "Visual hallucinations (VH) are common in Parkinson's disease and dementia with Lewy bodies, two forms of Lewy body disease (LBD), but the neural substrates and mechanisms involved are still unclear. We conducted meta-analyses of voxel-based morphometry (VBM) and neuropsychological studies investigating the neuroanatomical and cognitive correlates of VH in LBD. For VBM (12 studies), we used Seed-based d Mapping with Permutation of Subject Images (SDM-PSI), including statistical parametric maps for 50% of the studies. For neuropsychology (35 studies), we used MetaNSUE to consider non-statistically significant unreported effects. VH were associated with smaller grey matter volume in occipital, frontal, occipitotemporal, and parietal areas (peak Hedges{\textquoteright} g -0.34 to -0.49). In patients with Parkinson's disease without dementia, VH were associated with lower verbal immediate memory performance (Hedges{\textquoteright} g -0.52). Both results survived correction for multiple comparisons. Abnormalities in these brain regions might reflect dysfunctions in brain networks sustaining visuoperceptive, attention, and executive abilities, with the latter also being at the basis of poor immediate memory performance.",

keywords = "Dementia with Lewy bodies, Grey matter volume, Lewy body disease, Memory, Meta-analysis, MRI, Neuropsychology, Parkinson's disease, VBM, Visual hallucinations",

author = "Stefania Pezzoli and Raquel S{\'a}nchez-Valle and Aleix Solanes and Kempton, {Matthew J.} and Oliver Bandmann and Shin, {Jae Il} and Annachiara Cagnin and Goldman, {Jennifer G.} and Doug Merkitch and Firbank, {Michael J.} and Taylor, {John Paul} and Javier Pagonabarraga and Jaime Kulisevsky and Frederic Blanc and Norma Verdolini and Annalena Venneri and Joaquim Radua",

note = "Funding Information: The contribution of the Institut d'Investigacions Biom{\`e}diques August Pi i Sunyer (IDIBAPS) is acknowledged. SP was supported by a scholarship from the University of Sheffield and the Erasmus+program of the European Union . JR was supported by two grants from the Instituto de Salud Carlos III and co-funded by European Union (ERDF/ESF, {\textquoteleft}Investing in your future{\textquoteright}): Miguel Servet Research Contract CPII19/00009 and Research Project Grants PI19/00394. MJF and J-PT were supported by the National Institute for Health Research (NIHR) Newcastle Biomedical Research Centre (BRC) based at Newcastle upon Tyne Hospitals NHS Foundation Trust and Newcastle University . JP was funded by PERIS , Expedient Number SLT008/18/00088 ( Generalitat de Catalunya ); Rio Hortega CM17/00209, Instituto de Salud Carlos III (ISCIII), Spain; FIS grant PI18/01717 , Instituto de Salud Carlos III (ISCIII), Spain. Publisher Copyright: {\textcopyright} 2021 Elsevier Ltd Copyright: Copyright 2021 Elsevier B.V., All rights reserved.",

year = "2021",

month = sep,

doi = "10.1016/j.neubiorev.2021.06.030",

language = "English",

volume = "128",

pages = "367--382",

journal = "Neuroscience and Biobehavioral Reviews",

issn = "0149-7634",

}

Pezzoli, S, Sánchez-Valle, R, Solanes, A, Kempton, MJ, Bandmann, O, Shin, JI, Cagnin, A, Goldman, JG, Merkitch, D, Firbank, MJ, Taylor, JP, Pagonabarraga, J, Kulisevsky, J, Blanc, F, Verdolini, N, Venneri, A & Radua, J 2021, 'Neuroanatomical and cognitive correlates of visual hallucinations in Parkinson's disease and dementia with Lewy bodies: Voxel-based morphometry and neuropsychological meta-analysis', Neuroscience and Biobehavioral Reviews, vol. 128, pp. 367-382. https://doi.org/10.1016/j.neubiorev.2021.06.030

Neuroanatomical and cognitive correlates of visual hallucinations in Parkinson's disease and dementia with Lewy bodies: Voxel-based morphometry and neuropsychological meta-analysis. / Pezzoli, Stefania; Sánchez-Valle, Raquel; Solanes, Aleix et al.
In: Neuroscience and Biobehavioral Reviews, Vol. 128, 09.2021, p. 367-382.

Research output: Contribution to journal › Review article › peer-review

TY - JOUR

T1 - Neuroanatomical and cognitive correlates of visual hallucinations in Parkinson's disease and dementia with Lewy bodies

T2 - Voxel-based morphometry and neuropsychological meta-analysis

AU - Pezzoli, Stefania

AU - Sánchez-Valle, Raquel

AU - Solanes, Aleix

AU - Kempton, Matthew J.

AU - Bandmann, Oliver

AU - Shin, Jae Il

AU - Cagnin, Annachiara

AU - Goldman, Jennifer G.

AU - Merkitch, Doug

AU - Firbank, Michael J.

AU - Taylor, John Paul

AU - Pagonabarraga, Javier

AU - Kulisevsky, Jaime

AU - Blanc, Frederic

AU - Verdolini, Norma

AU - Venneri, Annalena

AU - Radua, Joaquim

N1 - Funding Information: The contribution of the Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS) is acknowledged. SP was supported by a scholarship from the University of Sheffield and the Erasmus+program of the European Union . JR was supported by two grants from the Instituto de Salud Carlos III and co-funded by European Union (ERDF/ESF, ‘Investing in your future’): Miguel Servet Research Contract CPII19/00009 and Research Project Grants PI19/00394. MJF and J-PT were supported by the National Institute for Health Research (NIHR) Newcastle Biomedical Research Centre (BRC) based at Newcastle upon Tyne Hospitals NHS Foundation Trust and Newcastle University . JP was funded by PERIS , Expedient Number SLT008/18/00088 ( Generalitat de Catalunya ); Rio Hortega CM17/00209, Instituto de Salud Carlos III (ISCIII), Spain; FIS grant PI18/01717 , Instituto de Salud Carlos III (ISCIII), Spain. Publisher Copyright: © 2021 Elsevier Ltd Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

PY - 2021/9

Y1 - 2021/9

N2 - Visual hallucinations (VH) are common in Parkinson's disease and dementia with Lewy bodies, two forms of Lewy body disease (LBD), but the neural substrates and mechanisms involved are still unclear. We conducted meta-analyses of voxel-based morphometry (VBM) and neuropsychological studies investigating the neuroanatomical and cognitive correlates of VH in LBD. For VBM (12 studies), we used Seed-based d Mapping with Permutation of Subject Images (SDM-PSI), including statistical parametric maps for 50% of the studies. For neuropsychology (35 studies), we used MetaNSUE to consider non-statistically significant unreported effects. VH were associated with smaller grey matter volume in occipital, frontal, occipitotemporal, and parietal areas (peak Hedges’ g -0.34 to -0.49). In patients with Parkinson's disease without dementia, VH were associated with lower verbal immediate memory performance (Hedges’ g -0.52). Both results survived correction for multiple comparisons. Abnormalities in these brain regions might reflect dysfunctions in brain networks sustaining visuoperceptive, attention, and executive abilities, with the latter also being at the basis of poor immediate memory performance.

AB - Visual hallucinations (VH) are common in Parkinson's disease and dementia with Lewy bodies, two forms of Lewy body disease (LBD), but the neural substrates and mechanisms involved are still unclear. We conducted meta-analyses of voxel-based morphometry (VBM) and neuropsychological studies investigating the neuroanatomical and cognitive correlates of VH in LBD. For VBM (12 studies), we used Seed-based d Mapping with Permutation of Subject Images (SDM-PSI), including statistical parametric maps for 50% of the studies. For neuropsychology (35 studies), we used MetaNSUE to consider non-statistically significant unreported effects. VH were associated with smaller grey matter volume in occipital, frontal, occipitotemporal, and parietal areas (peak Hedges’ g -0.34 to -0.49). In patients with Parkinson's disease without dementia, VH were associated with lower verbal immediate memory performance (Hedges’ g -0.52). Both results survived correction for multiple comparisons. Abnormalities in these brain regions might reflect dysfunctions in brain networks sustaining visuoperceptive, attention, and executive abilities, with the latter also being at the basis of poor immediate memory performance.

KW - Dementia with Lewy bodies

KW - Grey matter volume

KW - Lewy body disease

KW - Memory

KW - Meta-analysis

KW - MRI

KW - Neuropsychology

KW - Parkinson's disease

KW - VBM

KW - Visual hallucinations

UR - http://www.scopus.com/inward/record.url?scp=85108988048&partnerID=8YFLogxK

U2 - 10.1016/j.neubiorev.2021.06.030

DO - 10.1016/j.neubiorev.2021.06.030

M3 - Review article

AN - SCOPUS:85108988048

SN - 0149-7634

VL - 128

SP - 367

EP - 382

JO - Neuroscience and Biobehavioral Reviews

JF - Neuroscience and Biobehavioral Reviews

ER -

Neuroanatomical and cognitive correlates of visual hallucinations in Parkinson's disease and dementia with Lewy bodies: Voxel-based morphometry and neuropsychological meta-analysis

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Keywords

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