Slide Slam N8
Spatiotemporal brain dynamics of sentence reading
Oscar Woolnough1, Elliot Murphy1, Patrick Rollo1, Cristian Donos2, Stanislas Dehaene3, Nitin Tandon1; 1University of Texas Health Science Center at Houston, 2University of Bucharest, 3College de France
Reading a sentence entails inferring meaning from combinations of multiple lexical objects that are combined into phrases and sentences, allowing us to derive complex meaning. Studies of cortical activity underlying semantic and syntactic operations implicate inferior frontal gyrus (IFG) and middle temporal gyrus (MTG), yet the relative contributions of these regions to sentence comprehension remain controversial. We used direct intracranial recordings from the IFG and MTG in the left, language-dominant hemisphere within a large cohort to map the spatiotemporal neural correlates of multi-word semantics and sentence structure building. 29 patients undergoing semi-chronic implantation of intracranial electrodes for localising pharmaco-resistant epilepsy silently read sets of Sentences, Jabberwocky sentences, Unstructured word lists, and Pseudoword lists, all 8 words long and presented in rapid serial visual presentation. Broadband gamma activity (70-150Hz) was extracted from electrodes across the left hemisphere (n>2,500) and subjected to linear mixed effects modelling to dissociate the impact of sentence structure, word frequency and lexicality on the recorded activations. Contrary to predictions from prior studies, we found that sentence structure did not lead to a simple monotonic increase in activation across the duration of the sentence, relative to word lists. Instead, we observed an initial suppression of activity for sentences, coinciding with the formation of a minimal phrase structure at word 2, followed then by a progressive increase in activity along the remaining duration of the sentence. This pattern was identical for electrodes in MTG, anterior IFG and medial frontal operculum. Ventral visual cortex, parietal cortex and posterior IFG did not show modulation by sentence structure. Jabberwocky sentences and pseudoword lists did not display systematic differences related to sentence construction in any region. Lastly, a tuning to word frequency was observed broadly across ventral occipitotemporal cortex, appearing earliest in mid-fusiform cortex, and preceding frequency tuned responses in IFG and traditional visual word form regions by around 200 ms. Our work suggests that the neural correlates of sentence structure comprehension primarily care about an accumulation of semantic rather than syntactic information. Both IFG and MTG demonstrate comparable sensitivity to sentence structure. The IFG is sensitive to lexical properties of single words, subserving an item-specific representation, while MTG appears to be involved in the generation of abstract, structural inferences. We also demonstrate a three-way functional dissociation of lexical and sentence level sensitivity within the frontal lobe, between anterior and posterior lateral IFG and the medial frontal operculum. Our work provides crucial insight into the integration of individual words into complex semantic concepts and highlights the critical need for large cohort studies of sentence processing utilising methods that provide high spatiotemporal resolution.