Abstract
ObjectivesWe investigated the neural basis of hallucinations Alzheimer's disease (AD) by applying voxel-based morphometry (VBM) to anatomical and functional data from the AD Neuroimaging Initiative.MethodsAD patients with hallucinations, based on the Neuropsychiatric Inventory (NPI-Q) (AD-hallu group; n = 39), were compared to AD patients without hallucinations matched for age, sex, educational level, handedness and MMSE (AD-c group; n = 39). Focal brain volume on MRI was analyzed and compared between the two groups according to the VBM method. We also performed voxel-level correlations between brain volume and hallucinations intensity. A similar paradigm was used for the PET analysis. “Core regions” (i.e. regions identified in both MRI and PET analyses, simply done by retaining the clusters obtained from the two analyses that are overlapping) were then determined.ResultsRegions with relative atrophy in association with hallucinations were: anterior part of the right insula, left superior frontal gyrus and lingual gyri. Regions with relative hypometabolism in association with hallucinations were a large right ventral and dorsolateral prefrontal area. "Core region" in association with hallucinations was the right anterior part of the insula. Correlations between intensity of hallucinations and brain volume were found in the right anterior insula, precentral gyrus, superior temporal gyrus, and left precuneus. Correlations between intensity of hallucinations and brain hypometabolism were found in the left midcingulate gyrus. We checked the neuropathological status and we found that the 4 patients autopsied in the AD-hallu group had the mixed pathology AD and Dementia with Lewy bodies (DLB).ConclusionNeural basis of hallucinations in cognitive neurodegenerative diseases (AD or AD and DLB) include a right predominant anterior-posterior network, and the anterior insula as the core region. This study is coherent with the top-down/bottom-up hypotheses on hallucinations but also hypotheses of the key involvement of the anterior insula in hallucinations in cognitive neurodegenerative diseases.
Highlights
The reported prevalence of hallucinations in Alzheimer’s disease (AD) patients varies from 0 to 25% depending on the study [1]
The protocol was submitted to appropriate Boards and their written unconditional approval obtained and submitted to Regulatory Affairs at the Alzheimer’s Disease Neuroimaging Initiative Coordinating Center (ADNICC) prior to commencement of the study
We define as "core regions" the regions that were identified in both magnetic resonance imaging (MRI) and positron emission tomography (PET) analyses. This is done by retaining the clusters obtained from the two analyses that are overlapping. We looked for these "core regions" either for the comparison between AD-hallu and AD-cor for the correlation analyses with the intensity of hallucinations
Summary
The reported prevalence of hallucinations in Alzheimer’s disease (AD) patients varies from 0 to 25% depending on the study [1]. Taylor et al started hallucinations in DLB patients in one third of the cases using transcranial magnetic stimulation of the occipital lobe [10]. They found that the severity of visual hallucinations were strongly correlated with occipital lobe excitability [10]. PD patients with hallucinations compared to Parkinson’s disease (PD) patients without, matched for cognitive status, exhibited grey matter atrophy in the cuneus, lingual and fusiform gyri, middle occipital lobe, inferior parietal lobule, and cingulate, paracentral and precentral gyri [12]
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