Abstracts

Rationale:
The left prefrontal cortex is essential for verbal communication. It remains uncertain how rapidly and extensively the left prefrontal cortex is recruited for comprehension of verbal sentence questions. We addressed this issue by measuring neuronal modulations, quantified with event-related high-gamma activity, during the understanding of three-phrase questions configured in different orders.
Method:
The study included 23 native Japanese speakers with drug-resistant focal epilepsy (age: 15-54 years) who underwent extraoperative ECoG recording in two tertiary epilepsy centers in Japan. Each patient was instructed to overtly answer each of the 96 auditory sentence questions of 1.8 s. Thereby, 48 trials consisted of [wh-interrogative], [adverb or object], and [verb], whereas the other 48 consisted of [adverb or object], [verb], and [wh-interrogative]. The frequency of words and total numbers of syllables within sentences were controlled between the two trial groups. By employing time-frequency analysis on ECoG signals, we compared the spatiotemporal dynamics of high-gamma modulations between the two trial groups (Figure 1).
Results:
Questions beginning with a wh-interrogative suppressed the left posterior prefrontal cortex right after the 1st phrase offset and the anterior prefrontal cortex after the 2nd phrase offset. Left prefrontal high-gamma activity subsequently began to rise and maximized around the 3rd phrase offset. Conversely, questions beginning with a concrete phrase suppressed the right orbitofrontal and then activated the left posterior prefrontal cortex after the 1st phrase offset. In all sentence types, high-gamma activity began to rise earlier, by one phrase, in the left posterior prefrontal than anterior prefrontal regions (Figure 2).
Conclusion:
Sentences beginning with a wh-interrogative may initially suppress the left prefrontal cortex to prioritize the bottom-up processing of upcoming auditory information. A concrete phrase may suppress the inhibitory function of the right orbitofrontal region and facilitate top-down lexical prediction by the left prefrontal cortex. The left anterior prefrontal regions may be recruited for semantic integration of multiple concrete phrases.
Funding:
:This work was supported by Intramural Research Grant 28-4 Clinical Research for Diagnostic and Therapeutic Innovations in Developmental Disorders (to M.I.), JSPS KAKENHI Grant Number 19K09494 (to M.I.), MEXT Grant-in-Aid for Scientific Research on Innovative Areas 19H04890 (to K.S.), and NIH grant NS64033 (to E.A.).