Lesions Causing Alice in Wonderland Syndrome Map to a Common Brain Network Linking Body and Size Perception.


Journal

Annals of neurology
ISSN: 1531-8249
Titre abrégé: Ann Neurol
Pays: United States
ID NLM: 7707449

Informations de publication

Date de publication:
01 Jul 2024
Historique:
revised: 28 05 2024
received: 13 04 2024
accepted: 06 06 2024
medline: 1 7 2024
pubmed: 1 7 2024
entrez: 1 7 2024
Statut: aheadofprint

Résumé

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. 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. 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). 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.

Identifiants

pubmed: 38949221
doi: 10.1002/ana.27015
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024 American Neurological Association.

Références

Lippman CW. Certain hallucinations peculiar to migraine. J Nerv Ment Dis 1952;116:346–351.
Lanska DJ, Lanska JR. The Alice‐in‐Wonderland syndrome. Front Neurol Neurosci 2018;42:142–150.
Blom JD. Alice in wonderland syndrome: a systematic review. Neurol Clin Pract 2016;6:259–270.
Todd J. The syndrome of Alice in Wonderland. Can Med Assoc J 1955;73:701–704.
Mastria G, Mancini V, Viganò A, Di Piero V. Alice in wonderland syndrome: a clinical and pathophysiological review. Biomed Res Int 2016;2016:8243145.
ElTarhouni AH, Beer L, Mouthon M, et al. The right thalamic ventral posterolateral nucleus seems to be determinant for macrosomatognosia: a case report. BMC Neurol 2020;20:393.
Lanska JR, Lanska DJ. Alice in wonderland syndrome: Somesthetic vs visual perceptual disturbance. Neurology 2013;80:1262–1264.
Weijers NR, Rietveld A, Meijer FJA, deLeeuw FE. Macrosomatognosia in frontal lobe infarct—a case report. J Neurol 2013;260:925–926.
Brumm K, Walenski M, Haist F, et al. Functional magnetic resonance imaging of a child with Alice in wonderland syndrome during an episode of micropsia. J Am Assoc Pediatr Ophthalmol Strabismus 2010;14:317–322.
Gencoglu EA, Alehan F, Erol I, et al. Brain SPECT findings in a patient with Alice in wonderland syndrome. Clin Nucl Med 2005;30:758–759.
Morland D, Wolff V, Dietemann J‐L, et al. Robin Hood caught in wonderland: brain SPECT findings. Clin Nucl Med 2013;38:979–981.
Mancini V, Mastria G, Frantellizzi V, et al. Aripiprazole‐triggered Alice in wonderland syndrome episodes studied with 99mTc‐HMPAO brain SPECT. Eur Neurol 2018;79:333–334.
Oliván‐Sasot P, Ipiens‐Escuer C, Orozco‐Molano AC, et al. Brain perfusion SPECT in Alice in wonderland syndrome. Rev Esp Med Nucl E Imagen Mol Engl Ed 2022;41:S62–S63.
Siddiqi SH, Kording KP, Parvizi J, Fox MD. Causal mapping of human brain function. Nat Rev Neurosci 2022;23:361–375.
Piervincenzi C, Petsas N, Giannì C, et al. Alice in wonderland syndrome: a lesion mapping study. Neurol Sci 2022;43:3321–3332.
Fox MD. Mapping symptoms to brain networks with the human connectome. N Engl J Med 2018;379:2237–2245.
Joutsa J, Corp DT, Fox MD. Lesion network mapping for symptom localization: recent developments and future directions. Curr Opin Neurol 2022;35:453–459.
Li Y, Qi L, Schaper FLWVJ, et al. A vertigo network derived from human brain lesions and brain stimulation. Brain Commun 2023;5:fcad071.
Kim NY, Hsu J, Talmasov D, et al. Lesions causing hallucinations localize to one common brain network. Mol Psychiatry 2021;26:1299–1309.
Darby RR, Joutsa J, Burke MJ, Fox MD. Lesion network localization of free will. Proc Natl Acad Sci U S A 2018;115:10792–10797.
Cohen AL, Soussand L, Corrow SL, et al. Looking beyond the face area: lesion network mapping of prosopagnosia. Brain 2019;142:3975–3990.
Darby RR, Laganiere S, Pascual‐Leone A, et al. Finding the imposter: brain connectivity of lesions causing delusional misidentifications. Brain J Neurol 2017;140:497–507.
Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021;372:n71.
Liu AM, Liu JG, Liu GW, Liu GT. ‘Alice in wonderland’ syndrome: presenting and follow‐up characteristics. Pediatr Neurol 2014;51:317–320.
Holmes AJ, Hollinshead MO, O'Keefe TM, et al. Brain genomics superstruct project initial data release with structural, functional, and behavioral measures. Sci Data 2015;2:150031.
Thomas Yeo BT, Krienen FM, Sepulcre J, et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol 2011;106:1125–1165.
Fox MD, Snyder AZ, Vincent JL, et al. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci U S A 2005;102:9673–9678.
Kletenik I, Ferguson MA, Bateman JR, et al. Network localization of unconscious visual perception in Blindsight. Ann Neurol 2022;91:217–224.
Winkler AM, Ridgway GR, Webster MA, et al. Permutation inference for the general linear model. Neuroimage 2014;92:381–397.
Rosenke M, vanHoof R, van denHurk J, et al. A probabilistic functional atlas of human Occipito‐temporal visual cortex. Cereb Cortex 2021;31:603–619.
Amunts K, Mohlberg H, Bludau S, Zilles K. Julich‐brain: a 3D probabilistic atlas of the human brain's cytoarchitecture. Science 2020;369:988–992.
Fan L, Li H, Zhuo J, et al. The human Brainnetome atlas: a new brain atlas based on connectional architecture. Cereb Cortex N Y 2016;26:3508–3526.
Jenkinson M, Beckmann CF, Behrens TEJ, et al. FSL. NeuroImage 2012;62:782–790.
Mastria G, Mancini V, Cesare MD, et al. Prevalence and characteristics of Alice in wonderland syndrome in adult migraineurs: perspectives from a tertiary referral headache unit. Cephalalgia 2021;41:515–524.
Hadjikhani N, Sanchez del Rio M, Wu O, et al. Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc Natl Acad Sci U S A 2001;98:4687–4692.
Silvestro M, Tessitore A, di Nardo F, et al. Functional connectivity changes in complex migraine aura: beyond the visual network. Eur J Neurol 2022;29:295–304.
The Project Gutenberg e‐book of Tenniel Illustrations for Alice in Wonderland, By Sir John Tenniel, https://www.gutenberg.org/files/114/114-h/114-h.htm.
Downing PE, Jiang Y, Shuman M, Kanwisher N. A cortical area selective for visual processing of the human body. Science 2001;293:2470–2473.
Myers A, Sowden PT. Your hand or mine? The extrastriate body area. NeuroImage 2008;42:1669–1677.
Arzy S, Thut G, Mohr C, et al. Neural basis of embodiment: distinct contributions of temporoparietal junction and extrastriate body area. J Neurosci 2006;26:8074–8081.
Harvey BM, Fracasso A, Petridou N, Dumoulin SO. Topographic representations of object size and relationships with numerosity reveal generalized quantity processing in human parietal cortex. Proc Natl Acad Sci 2015;112:13525–13530.
Welbourne LE, Jonnalagadda A, Giesbrecht B, Eckstein MP. The transverse occipital sulcus and intraparietal sulcus show neural selectivity to object‐scene size relationships. Commun Biol 2021;4:1–14.
Bueti D, Walsh V. The parietal cortex and the representation of time, space, number and other magnitudes. Philos Trans R Soc B Biol Sci 2009;364:1831–1840.
Mock J, Huber S, Bloechle J, et al. Magnitude processing of symbolic and non‐symbolic proportions: an fMRI study. Behav Brain Funct BBF 2018;14:9.
Burke MJ, Joutsa J, Cohen AL, et al. Mapping migraine to a common brain network. Brain 2020;143:541–553.
Charles A. Advances in the basic and clinical science of migraine. Ann Neurol 2009;65:491–498.
Mastria G, Mancini V, Viganò A, et al. Neuroimaging markers of Alice in wonderland syndrome in patients with migraine with aura. Front Neurol 2023;14:1210811.
Herbet G, Zemmoura I, Duffau H. Functional anatomy of the inferior longitudinal fasciculus: from historical reports to current hypotheses. Front Neuroanat 2018;12:77.
Taylor JC, Wiggett AJ, Downing PE. Functional MRI analysis of body and body part representations in the extrastriate and fusiform body areas. J Neurophysiol 2007;98:1626–1633.
Limanowski J, Blankenburg F. Integration of visual and proprioceptive limb position information in human posterior parietal, premotor, and Extrastriate cortex. J Neurosci 2016;36:2582–2589.
Astafiev SV, Stanley CM, Shulman GL, Corbetta M. Extrastriate body area in human occipital cortex responds to the performance of motor actions. Nat Neurosci 2004;7:542–548.
Vocks S, Busch M, Grönemeyer D, et al. Differential neuronal responses to the self and others in the extrastriate body area and the fusiform body area. Cogn Affect Behav Neurosci 2010;10:422–429.
Barton JJS. Chapter 9—Disorders of higher visual processing. In: Kennard C, Leigh RJ, eds. Handbook of Clinical Neurology. Vol 102. Elsevier, 2011:223‐261.
Kristensen S, Fracasso A, Dumoulin SO, et al. Size constancy affects the perception and parietal neural representation of object size. Neuroimage 2021;232:117909.
Hashimoto T, Iriki A. Dissociations between the horizontal and dorsoventral axes in body‐size perception. Eur J Neurosci 2013;37:1747–1753.
Holmes G. The Montgomery lectures in OPHTHALMOLOGY. Br Med J 1919;2:230–233.
Wyke M. Alterations of size constancy associated with brain lesions in man. J Neurol Neurosurg Psychiatry 1960;23:253–261.
Kassubek J, Otte M, Wolter T, et al. Brain imaging in a patient with hemimicropsia. Neuropsychologia 1999;37:1327–1334.
Cohen L, Gray F, Meyrignac C, et al. Selective deficit of visual size perception: two cases of hemimicropsia. J Neurol Neurosurg Psychiatry 1994;57:73–78.
Boes AD, Prasad S, Liu H, et al. Network localization of neurological symptoms from focal brain lesions. Brain 2015;138:3061–3075.
Cavanna AE, Trimble MR. The precuneus: a review of its functional anatomy and behavioural correlates. Brain 2006;129:564–583.
Dary Z, Lenggenhager B, Lagarde S, et al. Neural bases of the bodily self as revealed by electrical brain stimulation: a systematic review. Hum Brain Mapp 2023;44:2936–2959.
Frassinetti F, Nichelli P, Di Pellegrino G. Selective horizontal dysmetropsia following prestriate lesion. Brain 1999;122:339–350.
Joutsa J, Shih LC, Horn A, et al. Identifying therapeutic targets from spontaneous beneficial brain lesions. Ann Neurol 2018;84:153–157.
Joutsa J, Moussawi K, Siddiqi SH, et al. Brain lesions disrupting addiction map to a common human brain circuit. Nat Med 2022;28:1249–1255.
Siddiqi SH, Schaper FLWVJ, Horn A, et al. Brain stimulation and brain lesions converge on common causal circuits in neuropsychiatric disease. Nat Hum Behav 2021;5:1707–1716.
Blom JD, Looijestijn J, Goekoop R, et al. Treatment of Alice in wonderland syndrome and verbal auditory hallucinations using repetitive transcranial magnetic stimulation: a case report with fMRI findings. Psychopathology 2011;44:337–344.

Auteurs

Maximilian U Friedrich (MU)

Center for Brain Circuit Therapeutics, Brigham & Women's Hospital, Boston, MA.
Harvard Medical School, Boston, MA.

Elijah C Baughan (EC)

Department of Psychology, Brigham Young University, Provo, UT.

Isaiah Kletenik (I)

Center for Brain Circuit Therapeutics, Brigham & Women's Hospital, Boston, MA.
Harvard Medical School, Boston, MA.

Ellen Younger (E)

School of Psychology, Faculty of Health, Deakin University, Geelong, Victoria, Australia.

Charlie W Zhao (CW)

Center for Brain Circuit Therapeutics, Brigham & Women's Hospital, Boston, MA.

Calvin Howard (C)

Center for Brain Circuit Therapeutics, Brigham & Women's Hospital, Boston, MA.

Michael A Ferguson (MA)

Center for Brain Circuit Therapeutics, Brigham & Women's Hospital, Boston, MA.

Frederic L W V J Schaper (FLWVJ)

Center for Brain Circuit Therapeutics, Brigham & Women's Hospital, Boston, MA.
Harvard Medical School, Boston, MA.

Amalie Chen (A)

Department of Neurology, Massachusetts General Hospital, Boston, MA.

Daniel Zeller (D)

Department of Neurology, University Hospital Wuerzburg, Würzburg, Germany.

Claudia Piervincenzi (C)

Department of Human Neurosciences, Sapienza University of Rome, Rome, Italy.

Silvia Tommasin (S)

Department of Human Neurosciences, Sapienza University of Rome, Rome, Italy.

Patrizia Pantano (P)

Department of Human Neurosciences, Sapienza University of Rome, Rome, Italy.
IRCCS Neuromed, Pozzilli, Isernia, Italy.

Olaf Blanke (O)

Laboratory of Cognitive Neuroscience, Neuro-X Institute, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland.

Sashank Prasad (S)

Department of Neurology, University of Pennsylvania Perelman School of Medicine, Pennsylvania, PA.

Jared A Nielsen (JA)

Department of Psychology, Brigham Young University, Provo, UT.
Neuroscience Center, Brigham Young University, Provo, UT.

Michael D Fox (MD)

Center for Brain Circuit Therapeutics, Brigham & Women's Hospital, Boston, MA.
Harvard Medical School, Boston, MA.

Classifications MeSH