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Changes in both top-down and bottom-up effective connectivity drive visual hallucinations in Parkinson’s disease

Visual hallucinations are common in Parkinson’s disease and are associated with a poorer quality of life and a higher risk of dementia. An important and influential model that is widely accepted as an explanation for the mechanism of visual hallucinations in Parkinson’s disease and other Lewy body d...

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Autores principales: Thomas, George E C, Zeidman, Peter, Sultana, Tajwar, Zarkali, Angeliki, Razi, Adeel, Weil, Rimona S
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9798302/
https://www.ncbi.nlm.nih.gov/pubmed/36601626
http://dx.doi.org/10.1093/braincomms/fcac329
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author Thomas, George E C
Zeidman, Peter
Sultana, Tajwar
Zarkali, Angeliki
Razi, Adeel
Weil, Rimona S
author_facet Thomas, George E C
Zeidman, Peter
Sultana, Tajwar
Zarkali, Angeliki
Razi, Adeel
Weil, Rimona S
author_sort Thomas, George E C
collection PubMed
description Visual hallucinations are common in Parkinson’s disease and are associated with a poorer quality of life and a higher risk of dementia. An important and influential model that is widely accepted as an explanation for the mechanism of visual hallucinations in Parkinson’s disease and other Lewy body diseases is that these arise due to aberrant hierarchical processing, with impaired bottom-up integration of sensory information and overweighting of top-down perceptual priors within the visual system. This hypothesis has been driven by behavioural data and supported indirectly by observations derived from regional activation and correlational measures using neuroimaging. However, until now, there was no evidence from neuroimaging for differences in causal influences between brain regions measured in patients with Parkinson’s hallucinations. This is in part because previous resting-state studies focused on functional connectivity, which is inherently undirected in nature and cannot test hypotheses about the directionality of connectivity. Spectral dynamic causal modelling is a Bayesian framework that allows the inference of effective connectivity—defined as the directed (causal) influence that one region exerts on another region—from resting-state functional MRI data. In the current study, we utilize spectral dynamic causal modelling to estimate effective connectivity within the resting-state visual network in our cohort of 15 Parkinson’s disease visual hallucinators and 75 Parkinson’s disease non-visual hallucinators. We find that visual hallucinators display decreased bottom-up effective connectivity from the lateral geniculate nucleus to primary visual cortex and increased top-down effective connectivity from the left prefrontal cortex to primary visual cortex and the medial thalamus, as compared with non-visual hallucinators. Importantly, we find that the pattern of effective connectivity is predictive of the presence of visual hallucinations and associated with their severity within the hallucinating group. This is the first study to provide evidence, using resting-state effective connectivity, to support a model of aberrant hierarchical predictive processing as the mechanism for visual hallucinations in Parkinson’s disease.
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spelling pubmed-97983022023-01-03 Changes in both top-down and bottom-up effective connectivity drive visual hallucinations in Parkinson’s disease Thomas, George E C Zeidman, Peter Sultana, Tajwar Zarkali, Angeliki Razi, Adeel Weil, Rimona S Brain Commun Original Article Visual hallucinations are common in Parkinson’s disease and are associated with a poorer quality of life and a higher risk of dementia. An important and influential model that is widely accepted as an explanation for the mechanism of visual hallucinations in Parkinson’s disease and other Lewy body diseases is that these arise due to aberrant hierarchical processing, with impaired bottom-up integration of sensory information and overweighting of top-down perceptual priors within the visual system. This hypothesis has been driven by behavioural data and supported indirectly by observations derived from regional activation and correlational measures using neuroimaging. However, until now, there was no evidence from neuroimaging for differences in causal influences between brain regions measured in patients with Parkinson’s hallucinations. This is in part because previous resting-state studies focused on functional connectivity, which is inherently undirected in nature and cannot test hypotheses about the directionality of connectivity. Spectral dynamic causal modelling is a Bayesian framework that allows the inference of effective connectivity—defined as the directed (causal) influence that one region exerts on another region—from resting-state functional MRI data. In the current study, we utilize spectral dynamic causal modelling to estimate effective connectivity within the resting-state visual network in our cohort of 15 Parkinson’s disease visual hallucinators and 75 Parkinson’s disease non-visual hallucinators. We find that visual hallucinators display decreased bottom-up effective connectivity from the lateral geniculate nucleus to primary visual cortex and increased top-down effective connectivity from the left prefrontal cortex to primary visual cortex and the medial thalamus, as compared with non-visual hallucinators. Importantly, we find that the pattern of effective connectivity is predictive of the presence of visual hallucinations and associated with their severity within the hallucinating group. This is the first study to provide evidence, using resting-state effective connectivity, to support a model of aberrant hierarchical predictive processing as the mechanism for visual hallucinations in Parkinson’s disease. Oxford University Press 2022-12-14 /pmc/articles/PMC9798302/ /pubmed/36601626 http://dx.doi.org/10.1093/braincomms/fcac329 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of the Guarantors of Brain. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Article
Thomas, George E C
Zeidman, Peter
Sultana, Tajwar
Zarkali, Angeliki
Razi, Adeel
Weil, Rimona S
Changes in both top-down and bottom-up effective connectivity drive visual hallucinations in Parkinson’s disease
title Changes in both top-down and bottom-up effective connectivity drive visual hallucinations in Parkinson’s disease
title_full Changes in both top-down and bottom-up effective connectivity drive visual hallucinations in Parkinson’s disease
title_fullStr Changes in both top-down and bottom-up effective connectivity drive visual hallucinations in Parkinson’s disease
title_full_unstemmed Changes in both top-down and bottom-up effective connectivity drive visual hallucinations in Parkinson’s disease
title_short Changes in both top-down and bottom-up effective connectivity drive visual hallucinations in Parkinson’s disease
title_sort changes in both top-down and bottom-up effective connectivity drive visual hallucinations in parkinson’s disease
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9798302/
https://www.ncbi.nlm.nih.gov/pubmed/36601626
http://dx.doi.org/10.1093/braincomms/fcac329
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