Stimulus-Driven Cortical Hyperexcitability in Individuals with Charles Bonnet Hallucinations
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Dwyer, Michael F
Kamke, Marc R
Mattingley, Jason B
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Abstract
Throughout the lifespan, the cerebral cortex adapts its structure and function in response to changing sensory input [1, 2]. Whilst such changes are typically adaptive, they can be maladaptive when they follow damage to the peripheral nervous system, including phantom limb pain and tinnitus [3, 4]. An intriguing example occurs in individuals with acquired ocular pathologies—most commonly age-related macular degeneration (MD) [5]—who lose their foveal vision but retain intact acuity in the peripheral visual field. Up to 40% of ocular pathology patients develop long-term hallucinations involving flashes of light, shapes, or geometric patterns and/or complex hallucinations, including faces, animals, or entire scenes, a condition known as Charles Bonnet Syndrome (CBS) [6, 7, 8]. Though CBS was first described over 250 years ago [9, 10], the neural basis for the hallucinations remains unclear, with no satisfactory explanation as to why some individuals develop hallucinations, while many do not. An influential but untested hypothesis for the visual hallucinations in CBS is that retinal deafferentation causes hyperexcitability in early visual cortex. To assess this, we investigated electrophysiological responses to peripheral visual field stimulation in MD patients with and without hallucinations and in matched controls without ocular pathology. Participants performed a concurrent attention task within intact portions of their peripheral visual field, while ignoring flickering checkerboards that drove periodic electrophysiological responses. CBS individuals showed strikingly elevated visual cortical responses to peripheral field stimulation compared with patients without hallucinations and controls, providing direct support for the hypothesis of visual cortical hyperexcitability in CBS. Visual hallucinations often result from age-related degeneration of the retina. Painter et al. show that these hallucinations are associated with stimulus-driven hyperexcitability within early visual cortex, providing the first evidence for an influential but untested hypothesis.
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Current Biology
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28
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21
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Biological sciences
Biomedical and clinical sciences
Psychology
Science & Technology
Life Sciences & Biomedicine
Biochemistry & Molecular Biology
Biology
Cell Biology
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Painter, DR; Dwyer, MF; Kamke, MR; Mattingley, JB, Stimulus-Driven Cortical Hyperexcitability in Individuals with Charles Bonnet Hallucinations, Current Biology, 2018, 28 (21), pp. 3475-3480.e3