Maximilian U. Friedrich MD, Elijah C. Baughan BS, Isaiah Kletenik MD, Ellen Younger MS, Charlie W. Zhao MD, Calvin Howard MD, Michael A. Ferguson PhD, Frederic L.W.V.J. Schaper MD, PhD, Amalie Chen MD, Daniel Zeller MD, Claudia Piervincenzi PhD, Silvia Tommasin PhD, Patrizia Pantano MD, Olaf Blanke MD, PhD, Sashank Prasad MD, Jared A. Nielsen PhD, Michael D. Fox MD, PhD
{"title":"Lesions Causing Alice in Wonderland Syndrome Map to a Common Brain Network Linking Body and Size Perception","authors":"Maximilian U. Friedrich MD, Elijah C. Baughan BS, Isaiah Kletenik MD, Ellen Younger MS, Charlie W. Zhao MD, Calvin Howard MD, Michael A. Ferguson PhD, Frederic L.W.V.J. Schaper MD, PhD, Amalie Chen MD, Daniel Zeller MD, Claudia Piervincenzi PhD, Silvia Tommasin PhD, Patrizia Pantano MD, Olaf Blanke MD, PhD, Sashank Prasad MD, Jared A. Nielsen PhD, Michael D. Fox MD, PhD","doi":"10.1002/ana.27015","DOIUrl":null,"url":null,"abstract":"<div>\n \n <section>\n \n <h3> Objective</h3>\n \n <p>Alice in Wonderland syndrome (AIWS) profoundly affects human perception of size and scale, particularly regarding one's own body and the environment. Its neuroanatomical basis has remained elusive, partly because brain lesions causing AIWS can occur in different brain regions. Here, we aimed to determine if brain lesions causing AIWS map to a distributed brain network.</p>\n </section>\n \n <section>\n \n <h3> Methods</h3>\n \n <p>A retrospective case–control study analyzing 37 cases of lesion-induced AIWS identified through systematic literature review was conducted. Using resting-state functional connectome data from 1,000 healthy individuals, the whole-brain connections of each lesion were estimated and contrasted with those from a control dataset comprising 1,073 lesions associated with 25 other neuropsychiatric syndromes. Additionally, connectivity findings from lesion-induced AIWS cases were compared with functional neuroimaging results from 5 non-lesional AIWS cases.</p>\n </section>\n \n <section>\n \n <h3> Results</h3>\n \n <p>AIWS-associated lesions were located in various brain regions with minimal overlap (≤33%). However, the majority of lesions (≥85%) demonstrated shared connectivity to the right extrastriate body area, known to be selectively activated by viewing body part images, and the inferior parietal cortex, involved in size and scale judgements. This pattern was uniquely characteristic of AIWS when compared with other neuropsychiatric disorders (family-wise error-corrected <i>p <</i> 0.05) and consistent with functional neuroimaging observations in AIWS due to nonlesional causes (median correlation <i>r =</i> 0.56, interquartile range 0.24).</p>\n </section>\n \n <section>\n \n <h3> Interpretation</h3>\n \n <p>AIWS-related perceptual distortions map to one common brain network, encompassing regions critical for body representation and size-scale processing. These findings lend insight into the neuroanatomical localization of higher-order perceptual functions, and may inform future therapeutic strategies for perceptual disorders. ANN NEUROL 2024;96:662–674</p>\n </section>\n </div>","PeriodicalId":127,"journal":{"name":"Annals of Neurology","volume":null,"pages":null},"PeriodicalIF":8.1000,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Annals of Neurology","FirstCategoryId":"3","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1002/ana.27015","RegionNum":1,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"CLINICAL NEUROLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Objective
Alice in Wonderland syndrome (AIWS) profoundly affects human perception of size and scale, particularly regarding one's own body and the environment. Its neuroanatomical basis has remained elusive, partly because brain lesions causing AIWS can occur in different brain regions. Here, we aimed to determine if brain lesions causing AIWS map to a distributed brain network.
Methods
A retrospective case–control study analyzing 37 cases of lesion-induced AIWS identified through systematic literature review was conducted. Using resting-state functional connectome data from 1,000 healthy individuals, the whole-brain connections of each lesion were estimated and contrasted with those from a control dataset comprising 1,073 lesions associated with 25 other neuropsychiatric syndromes. Additionally, connectivity findings from lesion-induced AIWS cases were compared with functional neuroimaging results from 5 non-lesional AIWS cases.
Results
AIWS-associated lesions were located in various brain regions with minimal overlap (≤33%). However, the majority of lesions (≥85%) demonstrated shared connectivity to the right extrastriate body area, known to be selectively activated by viewing body part images, and the inferior parietal cortex, involved in size and scale judgements. This pattern was uniquely characteristic of AIWS when compared with other neuropsychiatric disorders (family-wise error-corrected p < 0.05) and consistent with functional neuroimaging observations in AIWS due to nonlesional causes (median correlation r = 0.56, interquartile range 0.24).
Interpretation
AIWS-related perceptual distortions map to one common brain network, encompassing regions critical for body representation and size-scale processing. These findings lend insight into the neuroanatomical localization of higher-order perceptual functions, and may inform future therapeutic strategies for perceptual disorders. ANN NEUROL 2024;96:662–674
期刊介绍:
Annals of Neurology publishes original articles with potential for high impact in understanding the pathogenesis, clinical and laboratory features, diagnosis, treatment, outcomes and science underlying diseases of the human nervous system. Articles should ideally be of broad interest to the academic neurological community rather than solely to subspecialists in a particular field. Studies involving experimental model system, including those in cell and organ cultures and animals, of direct translational relevance to the understanding of neurological disease are also encouraged.