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

• Published in: Brain stimulation Vol. 15; no. 1; pp. 87 - 95
• Main Authors: Giampiccolo, Davide, Moritz-Gasser, Sylvie, Ng, Sam, Lemaître, Anne-Laure, Duffau, Hugues
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.01.2022; Elsevier
• Subjects: Arcuate fasciculus; Brain mapping; Cognitive science; Jargon; Jargon aphasia; Neuroscience; Phonology; Semantics; Jargon; Phonology; Semantics; Arcuate fasciculus; Jargon aphasia; Brain mapping; Neuropsychology
• ISSN: 1935-861X; 1876-4754
• DOI: 10.1016/j.brs.2021.11.012

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. To identify white matter pathways causally involved in jargonaphasia. 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. 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. 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. •Neural foundations underlying jargonophasia are poorly understood.•Jargonaphasia can be reliably induced by subcortical stimulation.•Semantic jargonaphasia can be generated by stimulation of the IFOF.•Neologistic jargonaphasia can be elicited by dual-stimulation of the IFOF and the AF.•Jargonophasia may be the result of a disconnection syndrome.