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Visual cortical activity in Charles Bonnet syndrome: testing the deafferentation hypothesis

Lookup NU author(s): Dr Kat Da Silva MorganORCiD, Daniel Collerton, Dr Michael FirbankORCiD, Julia SchumacherORCiD, Professor John-Paul TaylorORCiD

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This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0).


Abstract

Visual hallucinations in individuals following sight loss (Charles Bonnet syndrome; CBS) have been posited to arise because of spontaneous, compensatory, neural activity in the visual cortex following sensory input loss from the eyes—known as deafferentation. However, neurophysiological investigations of CBS remain limited. We performed a multi-modal investigation comparing visual cortical activity in 19 people with eye disease who experience visual hallucinations (CBS) with 18 people with eye disease without hallucinations (ED-Controls; matched for age and visual acuity) utilising functional MRI, EEG, and transcranial magnetic stimulation (TMS). A pattern of altered visual cortical activity in people with CBS was noted across investigations. Reduced BOLD activation in ventral extrastriate and primary visual cortex, and reduced EEG alpha-reactivity in response to visual stimulation was observed in CBS compared to ED-Controls. The CBS group also demonstrated a shift towards lower frequency band oscillations in the EEG, indicative of cortical slowing, with significantly greater occipital theta power compared to ED-controls. Furthermore, a significant association between reduced activation in response to visual stimulation and increased excitability (in the form of reduced TMS phosphene thresholds) was observed in CBS, indicating persistent visual cortical activation consistent with hyperexcitability, which was found to be significantly associated with increased hallucination severity. These results provide converging lines of evidence to support the role of increased visual cortical excitability in the formation of visual hallucinations in some people following sight loss, consistent with the deafferentation hypothesis.


Publication metadata

Author(s): daSilva Morgan K, Collerton D, Firbank MJ, Schumacher J, ffytche DH, Taylor JP

Publication type: Article

Publication status: Published

Journal: Journal of Neuology

Year: 2025

Volume: 272

Print publication date: 11/02/2025

Online publication date: 11/02/2025

Acceptance date: 08/11/2024

Date deposited: 18/02/2025

ISSN (print): 0340-5354

ISSN (electronic): 1432-1459

Publisher: Springer

URL: https://doi.org/10.1007/s00415-024-12741-2

DOI: 10.1007/s00415-024-12741-2

Data Access Statement: The data supporting the findings presented in this paper are available on the basis of a formal data-sharing agreement and, depending on data usage, agreement for formal collaboration, and co-authorship where appropriate.


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Funding

Funder referenceFunder name
Fight for Sight, 24TP172
Macular Society, BH152932
Thomas Pocklington Trust, 24TP172

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