Functional and structural brain network correlates of visual hallucinations in Lewy body dementia.
| Title: | Functional and structural brain network correlates of visual hallucinations in Lewy body dementia. |
|---|---|
| Authors: | Mehraram R; Experimental Oto-rhino-laryngology (ExpORL) Research Group, Department of Neurosciences, KU Leuven, Leuven, Belgium.; NIHR Newcastle Biomedical Research Centre, Campus for Ageing and Vitality, Newcastle upon Tyne, UK.; Translational and Clinical Research Institute, Newcastle University, Campus for Ageing and Vitality, Newcastle upon Tyne, UK.; Interdisciplinary Computing and Complex BioSystems (ICOS) research group, School of Computing, Newcastle University, Newcastle upon Tyne, UK.; Peraza LR; IXICO Plc, London, UK.; Murphy NRE; Baylor College of Medicine, Menninger Department of Psychiatry and Behavioral Sciences, Houston, TX 77030, USA.; The Menninger Clinic, Houston, TX 77035, USA.; Michael E. DeBakey VA Medical Center, 2002 Holcombe Boulevard, Houston, TX 77030, USA.; Cromarty RA; Translational and Clinical Research Institute, Newcastle University, Campus for Ageing and Vitality, Newcastle upon Tyne, UK.; Graziadio S; NIHR Newcastle in vitro Diagnostics Cooperative, Newcastle upon Tyne Hospitals NHS Foundation Trust, Newcastle upon Tyne, UK.; O'Brien JT; Department of Psychiatry, University of Cambridge School of Medicine, Cambridge, UK.; Killen A; Translational and Clinical Research Institute, Newcastle University, Campus for Ageing and Vitality, Newcastle upon Tyne, UK.; Colloby SJ; Translational and Clinical Research Institute, Newcastle University, Campus for Ageing and Vitality, Newcastle upon Tyne, UK.; Firbank M; Translational and Clinical Research Institute, Newcastle University, Campus for Ageing and Vitality, Newcastle upon Tyne, UK.; Su L; Department of Psychiatry, University of Cambridge School of Medicine, Cambridge, UK.; Department of Neuroscience, The University of Sheffield, Sheffield, UK.; Collerton D; Translational and Clinical Research Institute, Newcastle University, Campus for Ageing and Vitality, Newcastle upon Tyne, UK.; Taylor JP; Translational and Clinical Research Institute, Newcastle University, Campus for Ageing and Vitality, Newcastle upon Tyne, UK.; Kaiser M; Interdisciplinary Computing and Complex BioSystems (ICOS) research group, School of Computing, Newcastle University, Newcastle upon Tyne, UK.; NIHR Nottingham Biomedical Research Centre, School of Medicine, University of Nottingham, Nottingham, UK.; Sir Peter Mansfield Imaging Centre, School of Medicine, University of Nottingham, Nottingham, UK.; Department of Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China. |
| Source: | Brain : a journal of neurology [Brain] 2022 Jun 30; Vol. 145 (6), pp. 2190-2205. |
| Publication Type: | Journal Article; Research Support, Non-U.S. Gov't; Comment |
| Language: | English |
| Journal Info: | Publisher: Oxford University Press Country of Publication: England NLM ID: 0372537 Publication Model: Print Cited Medium: Internet ISSN: 1460-2156 (Electronic) Linking ISSN: 00068950 NLM ISO Abbreviation: Brain Subsets: MEDLINE |
| Imprint Name(s): | Publication: Oxford : Oxford University Press; Original Publication: London. |
| MeSH Terms: | Alzheimer Disease*/pathology ; Lewy Body Disease*/complications ; Lewy Body Disease*/diagnostic imaging ; Lewy Body Disease*/pathology; Brain/pathology ; Hallucinations/etiology ; Diffusion Tensor Imaging ; Humans |
| Abstract: | Visual hallucinations are a common feature of Lewy body dementia. Previous studies have shown that visual hallucinations are highly specific in differentiating Lewy body dementia from Alzheimer's disease dementia and Alzheimer-Lewy body mixed pathology cases. Computational models propose that impairment of visual and attentional networks is aetiologically key to the manifestation of visual hallucinations symptomatology. However, there is still a lack of experimental evidence on functional and structural brain network abnormalities associated with visual hallucinations in Lewy body dementia. We used EEG source localization and network based statistics to assess differential topographical patterns in Lewy body dementia between 25 participants with visual hallucinations and 17 participants without hallucinations. Diffusion tensor imaging was used to assess structural connectivity between thalamus, basal forebrain and cortical regions belonging to the functionally affected network component in the hallucinating group, as assessed with network based statistics. The number of white matter streamlines within the cortex and between subcortical and cortical regions was compared between hallucinating and not hallucinating groups and correlated with average EEG source connectivity of the affected subnetwork. Moreover, modular organization of the EEG source network was obtained, compared between groups and tested for correlation with structural connectivity. Network analysis showed that compared to non-hallucinating patients, those with hallucinations feature consistent weakened connectivity within the visual ventral network, and between this network and default mode and ventral attentional networks, but not between or within attentional networks. The occipital lobe was the most functionally disconnected region. Structural analysis yielded significantly affected white matter streamlines connecting the cortical regions to the nucleus basalis of Meynert and the thalamus in hallucinating compared to not hallucinating patients. The number of streamlines in the tract between the basal forebrain and the cortex correlated with cortical functional connectivity in non-hallucinating patients, while a correlation emerged for the white matter streamlines connecting the functionally affected cortical regions in the hallucinating group. This study proposes, for the first time, differential functional networks between hallucinating and not hallucinating Lewy body dementia patients, and provides empirical evidence for existing models of visual hallucinations. Specifically, the outcome of the present study shows that the hallucinating condition is associated with functional network segregation in Lewy body dementia and supports the involvement of the cholinergic system as proposed in the current literature.; (© The Author(s) 2022. Published by Oxford University Press on behalf of the Guarantors of Brain.) |
| Comments: | Comment on: Brain. 2016 Nov 1;139(11):2827-2843. doi: 10.1093/brain/aww175.. (PMID: 27412389); Comment in: Brain. 2022 Jun 30;145(6):1883-1885. doi: 10.1093/brain/awac170.. (PMID: 35642563) |
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| Grant Information: | MR/T004347/1 United Kingdom MRC_ Medical Research Council; MR/T004347/2 United Kingdom MRC_ Medical Research Council; United Kingdom WT_ Wellcome Trust; United Kingdom DH_ Department of Health |
| Contributed Indexing: | Keywords: EEG; MRI; Parkinson; diffusion; graph |
| Entry Date(s): | Date Created: 20220309 Date Completed: 20220704 Latest Revision: 20250530 |
| Update Code: | 20260130 |
| PubMed Central ID: | PMC9246710 |
| DOI: | 10.1093/brain/awac094 |
| PMID: | 35262667 |
| Database: | MEDLINE |
Journal Article; Research Support, Non-U.S. Gov't; Comment