Jargonaphasia as a disconnection syndrome: A study combining white matter electrical stimulation and disconnectome mapping

Background: In jargonaphasia, speech is fluent but meaningless. While neuropsychological evaluation may distinguish a neologistic component characterised by non-word production and a semantic component where pronounced words are real but speech is senseless, how this relates to the underlying white...

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Autores principales:	Davide Giampiccolo, Sylvie Moritz-Gasser, Sam Ng, Anne-Laure Lemaître, Hugues Duffau
Formato:	article
Lenguaje:	EN
Publicado:	Elsevier 2022
Materias:	Arcuate fasciculus Jargon Jargon aphasia Phonology Semantics Brain mapping Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571
Acceso en línea:	https://doaj.org/article/42d2d71d68ab48ec977d71b77a951b2b
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spelling	oai:doaj.org-article:42d2d71d68ab48ec977d71b77a951b2b2021-11-20T05:05:13ZJargonaphasia as a disconnection syndrome: A study combining white matter electrical stimulation and disconnectome mapping1935-861X10.1016/j.brs.2021.11.012https://doaj.org/article/42d2d71d68ab48ec977d71b77a951b2b2022-01-01T00:00:00Zhttp://www.sciencedirect.com/science/article/pii/S1935861X21008287https://doaj.org/toc/1935-861XBackground: In jargonaphasia, speech is fluent but meaningless. While neuropsychological evaluation may distinguish a neologistic component characterised by non-word production and a semantic component where pronounced words are real but speech is senseless, how this relates to the underlying white matter anatomy is debated. Objective: To identify white matter pathways causally involved in jargonaphasia. Methods: We retrospectively screened the intraoperative brain mapping data of 571 awake oncological resections using direct cortico-subcortical electrostimulation. Jargonaphasia was induced in 17 patients (19 sites) during a naming task. Stimulation sites were normalized to the Montreal Neurological Institute template space and used to generate individual disconnectome maps. Non-parametric voxelwise one and two sample t-tests were performed to identify the underlying white matter anatomy. Results: Jargonaphasia was induced only during stimulation of the left hemisphere. No cortical stimulation generated jargonaphasia. Subcortical sites causally associated with jargonaphasia clustered in 3 regions: in the temporal lobe (middle to inferior temporal gyri; n = 12), in the parietal lobe (supramarginal gyrus; n = 3) and in the temporal stem (n = 4). Disconnectome analysis indicated the inferior-fronto-occipital fasciculus (IFOF) was damaged in both neologistic and semantic jargonaphasia, while the involvement of the arcuate fasciculus was specific to neologistic jargonaphasia. Conclusion: For the first time, we show that jargonaphasia is induced by white matter stimulation, hinting at disconnection. As IFOF disconnection unites both variants, these may represent a continuum of disorders distinguished by semantic impairment. Conversely, damage to the arcuate fasciculus in addition to the IFOF is specific to neologistic jargonaphasia, thus suggesting a dual-disconnection syndrome.Davide GiampiccoloSylvie Moritz-GasserSam NgAnne-Laure LemaîtreHugues DuffauElsevierarticleArcuate fasciculusJargonJargon aphasiaPhonologySemanticsBrain mappingNeurosciences. Biological psychiatry. NeuropsychiatryRC321-571ENBrain Stimulation, Vol 15, Iss 1, Pp 87-95 (2022)
institution	DOAJ
collection	DOAJ
language	EN
topic	Arcuate fasciculus Jargon Jargon aphasia Phonology Semantics Brain mapping Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571
spellingShingle	Arcuate fasciculus Jargon Jargon aphasia Phonology Semantics Brain mapping Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571 Davide Giampiccolo Sylvie Moritz-Gasser Sam Ng Anne-Laure Lemaître Hugues Duffau Jargonaphasia as a disconnection syndrome: A study combining white matter electrical stimulation and disconnectome mapping
description	Background: In jargonaphasia, speech is fluent but meaningless. While neuropsychological evaluation may distinguish a neologistic component characterised by non-word production and a semantic component where pronounced words are real but speech is senseless, how this relates to the underlying white matter anatomy is debated. Objective: To identify white matter pathways causally involved in jargonaphasia. Methods: We retrospectively screened the intraoperative brain mapping data of 571 awake oncological resections using direct cortico-subcortical electrostimulation. Jargonaphasia was induced in 17 patients (19 sites) during a naming task. Stimulation sites were normalized to the Montreal Neurological Institute template space and used to generate individual disconnectome maps. Non-parametric voxelwise one and two sample t-tests were performed to identify the underlying white matter anatomy. Results: Jargonaphasia was induced only during stimulation of the left hemisphere. No cortical stimulation generated jargonaphasia. Subcortical sites causally associated with jargonaphasia clustered in 3 regions: in the temporal lobe (middle to inferior temporal gyri; n = 12), in the parietal lobe (supramarginal gyrus; n = 3) and in the temporal stem (n = 4). Disconnectome analysis indicated the inferior-fronto-occipital fasciculus (IFOF) was damaged in both neologistic and semantic jargonaphasia, while the involvement of the arcuate fasciculus was specific to neologistic jargonaphasia. Conclusion: For the first time, we show that jargonaphasia is induced by white matter stimulation, hinting at disconnection. As IFOF disconnection unites both variants, these may represent a continuum of disorders distinguished by semantic impairment. Conversely, damage to the arcuate fasciculus in addition to the IFOF is specific to neologistic jargonaphasia, thus suggesting a dual-disconnection syndrome.
format	article
author	Davide Giampiccolo Sylvie Moritz-Gasser Sam Ng Anne-Laure Lemaître Hugues Duffau
author_facet	Davide Giampiccolo Sylvie Moritz-Gasser Sam Ng Anne-Laure Lemaître Hugues Duffau
author_sort	Davide Giampiccolo
title	Jargonaphasia as a disconnection syndrome: A study combining white matter electrical stimulation and disconnectome mapping
title_short	Jargonaphasia as a disconnection syndrome: A study combining white matter electrical stimulation and disconnectome mapping
title_full	Jargonaphasia as a disconnection syndrome: A study combining white matter electrical stimulation and disconnectome mapping
title_fullStr	Jargonaphasia as a disconnection syndrome: A study combining white matter electrical stimulation and disconnectome mapping
title_full_unstemmed	Jargonaphasia as a disconnection syndrome: A study combining white matter electrical stimulation and disconnectome mapping
title_sort	jargonaphasia as a disconnection syndrome: a study combining white matter electrical stimulation and disconnectome mapping
publisher	Elsevier
publishDate	2022
url	https://doaj.org/article/42d2d71d68ab48ec977d71b77a951b2b
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Jargonaphasia as a disconnection syndrome: A study combining white matter electrical stimulation and disconnectome mapping

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