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

Davide Giampiccolo; Sylvie Moritz-Gasser; Sam Ng; Anne-Laure Lemaître; Hugues Duffau

doi:10.1016/j.brs.2021.11.012

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

Brain Stimul. 2022 Jan-Feb;15(1):87-95. doi: 10.1016/j.brs.2021.11.012. Epub 2021 Nov 18.

Authors

Davide Giampiccolo¹, Sylvie Moritz-Gasser², Sam Ng³, Anne-Laure Lemaître³, Hugues Duffau⁴

Affiliations

¹ Section of Neurosurgery, Department of Neurosciences, Biomedicine and Movement Sciences, University Hospital, Verona, Italy; Department of Neurosurgery, Gui de Chauliac Hospital, Montpellier University Medical Center, Montpellier, France.
² Department of Neurosurgery, Gui de Chauliac Hospital, Montpellier University Medical Center, Montpellier, France; Team "Neuroplasticity, Stem Cells and Low-grade Gliomas," INSERM U1191, Institute of Genomics of Montpellier, University of Montpellier, Montpellier, France; Department of Speech-Language Pathology, University of Montpellier, Montpellier, France.
³ Department of Neurosurgery, Gui de Chauliac Hospital, Montpellier University Medical Center, Montpellier, France; Team "Neuroplasticity, Stem Cells and Low-grade Gliomas," INSERM U1191, Institute of Genomics of Montpellier, University of Montpellier, Montpellier, France.
⁴ Department of Neurosurgery, Gui de Chauliac Hospital, Montpellier University Medical Center, Montpellier, France; Team "Neuroplasticity, Stem Cells and Low-grade Gliomas," INSERM U1191, Institute of Genomics of Montpellier, University of Montpellier, Montpellier, France. Electronic address: h-duffau@chu-montpellier.fr.

PMID: 34801750
DOI: 10.1016/j.brs.2021.11.012

Abstract

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.

Keywords: Arcuate fasciculus; Brain mapping; Jargon; Jargon aphasia; Phonology; Semantics.

MeSH terms

Brain Mapping
Electric Stimulation
Humans
Nerve Net
Neural Pathways / physiology
Retrospective Studies
White Matter* / diagnostic imaging
White Matter* / physiology