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The role of dysfunctional attentional control networks in visual misperceptions in Parkinson's disease

Authors

  • James M. Shine,

    1. Parkinson's Disease Research Clinic, Brain and Mind Research Institute, The University of Sydney, New South Wales, Australia
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  • Glenda M. Halliday,

    1. Neuroscience Research Australia, Sydney, New South Wales, Australia
    2. The University of New South Wales, Sydney, New South Wales, Australia
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  • Moran Gilat,

    1. Parkinson's Disease Research Clinic, Brain and Mind Research Institute, The University of Sydney, New South Wales, Australia
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  • Elie Matar,

    1. Parkinson's Disease Research Clinic, Brain and Mind Research Institute, The University of Sydney, New South Wales, Australia
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  • Samuel J. Bolitho,

    1. Parkinson's Disease Research Clinic, Brain and Mind Research Institute, The University of Sydney, New South Wales, Australia
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  • Maria Carlos,

    1. Parkinson's Disease Research Clinic, Brain and Mind Research Institute, The University of Sydney, New South Wales, Australia
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  • Sharon L. Naismith,

    1. Parkinson's Disease Research Clinic, Brain and Mind Research Institute, The University of Sydney, New South Wales, Australia
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  • Simon J.G. Lewis

    Corresponding author
    1. Parkinson's Disease Research Clinic, Brain and Mind Research Institute, The University of Sydney, New South Wales, Australia
    • Correspondence to: Simon J.G. Lewis, Parkinson's Disease Research Clinic, 94 Mallett Street, Camperdown, Sydney, New South Wales 2050, Australia. E-mail: simonl@med.usyd.edu.au

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Abstract

Visual misperceptions and hallucinations represent a problematic symptom of Parkinson's disease. The pathophysiological mechanisms underlying these symptoms remain poorly understood, however, a recent hypothesis has suggested that visual misperceptions and hallucinations may arise from disrupted processing across attentional networks. To test the specific predictions of this hypothesis, 22 patients with Parkinson's disease underwent 3T fMRI while performing the Bistable Percept Paradigm, a task that has previously been shown to identify patients with hallucinations. Subjects are required to study a battery of randomly assigned “monostable” and “bistable” monochromatic images for the presence or absence of a bistable percept. Those patients who scored a high percentage of misperceptions and missed images on the task were less able to activate frontal and parietal hubs of the putative Dorsal Attention Network. Furthermore, poor performance on the task was significantly correlated with the degree of decreased activation in a number of these hubs. At the group level, the difference between processing a bistable versus a monostable cue was associated with increased recruitment of the anterior insula. In addition, those patients with impaired performance on the paradigm displayed decreased resting state functional connectivity between hubs of the Ventral and Dorsal Attention Networks. These same patients had significantly decreased gray matter in the insula bilaterally. In addition, a combined analysis of the separate neuroimaging approaches revealed significant relationships across the impaired networks. These findings are consistent with specific predictions from a recently proposed hypothesis that implicates dysfunction within attentional networks in Parkinsonian hallucinations. Hum Brain Mapp 35:2206–2219, 2014. © 2013 Wiley Periodicals, Inc.

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