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Written word-level semantic representation in the left ventromedial temporal lobe: converging evidence from intracerebral recordings and electrical stimulation

Poster Session E, Friday, October 2, 11:00 am - 1:00 pm, Wangari Maathai

Bruno Rossion1, Luna Angelini1, Angélique Volfart2, Jacques Jonas3, Antonietta Gabriella Liuzzi4; 1Université de Lorraine, CNRS, IMoPA, 2University of Luxembourg, Department of Behavioural and Cognitive Sciences, 3Université de Lorraine, CHRU-Nancy, Service de Neurologie, 4KUleuven, Laboratory for Cognitive Neurology, Department of Neurosciences

A sensitive and objective electrophysiological measure of (written) word semantic categorization, relying on the principle of ‘frequency-tagging’ or fast periodic visual stimulation (FPVS), has been recently developed (Volfart et al., 2021). In this paradigm, a sequence of written words belonging to the same semantic category (e.g., cities) is presented at 4Hz (4 stimuli / second) and alternated - every 4 stimuli - with a written word from a different semantic category (e.g., animals). In healthy individuals, a significant response is objectively identified in the frequency spectrum at the semantic category change frequency (i.e., 1 Hz harmonics) after a few minutes of stimulation only, reflecting participants’ (automatic) semantic categorisation function. Unlike typical N400 (effects), this periodic EEG response is localized mainly over left posterior occipito-temporal regions. While this scalp topography is compatible with neural generators in the left posterior middle temporal gyrus, which is reliably activated in functional neuroimaging studies of semantic processing, this novel FPVS paradigm could (also) elicit neural activity in anterior regions of the ventromedial temporal lobe thought to be involved in semantic categorization. Moreover, whether putative neural activity elicited by this paradigm in the ventral temporal lobe would be critically involved in semantic word categorization is unknown. Here we report a unique opportunity to address the issue of the ventro-temporal sources of semantic categorization of written words with FPVS, as well as their criticality, in a single patient (CD) with refractory focal epilepsy undergoing SEEG as part of clinical evaluation with a large number (99) of intracerebral electrode contacts in the ventral temporal lobe. During the FPVS semantic categorization paradigm, 39 electrode contacts showed significance, with a pair of contacts located in the left ventromedial temporal lobe (TM’1- TM’2, collateral sulcus/ perirhinal cortex) eliciting the highest amplitude (both for low and high frequency bands), followed by a pair of contacts in the anterior collateral sulcus (TB’3-TB’4). During a similar semantic categorization task with pictures, the spatial distribution of responsive contacts substantially overlapped with significant contacts for written words categorization, although located more posteriorly, with the highest amplitude response in the left middle fusiform gyrus (F’4-F’5). Strikingly, among all electrically stimulated sites (31 in total), transient anomia was only elicited by stimulation on the same pair of contact in the collateral sulcus/perirhinal cortex showing the largest response for word semantic categorization (TM’1-TM’2). This site was further stimulated during assessment of other language functions, showing impairments/slowing down for semantic matching of written words, non-significantly for semantic matching of pictures and auditory definition, and no effect during word reading. Overall, these observations show a tight relationship between the largest semantic category discrimination response for written words during FPVS in the left ventromedial temporal lobe and transient picture naming failure during DES on the critical contact. Beyond semantic categorization per se, these results strengthen the critical role of this region in linking verbal representations to conceptual referents (Liuzzi et al., 2019), and further support the validity of the FPVS approach for electrophysiological investigation of semantic cognition in the human brain.

Topic Areas: Meaning: Lexical Semantics, Methods

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