Your verbal questions beginning with 'what' will rapidly deactivate the left prefrontal cortex of listeners

Hirotaka Iwaki,Kyoko Suzuki,Yutaro Takayama,Shin-Ichiro Osawa,Kazushi Ukishiro,Brian H Silverstein,Masaki Iwasaki,Teiji Tominaga,Kazuo Kakinuma,Takumi Mitsuhashi,Toshimune Kambara,Masaki Sonoda,Nobukazu Nakasato,Eishi Asano

doi:10.1038/s41598-021-84610-1

Abstract

The left prefrontal cortex is essential for verbal communication. It remains uncertain at what timing, to what extent, and what type of phrase initiates left-hemispheric dominant prefrontal activation during comprehension of spoken sentences. We clarified this issue by measuring event-related high-gamma activity during a task to respond to three-phrase questions configured in different orders. Questions beginning with a wh-interrogative deactivated 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 augmented subsequently and maximized around the 3rd phrase offset. Conversely, questions starting with a concrete phrase deactivated the right orbitofrontal region and then activated the left posterior prefrontal cortex after the 1st phrase offset. Regardless of sentence types, high-gamma activity emerged earlier, by one phrase, in the left posterior prefrontal than anterior prefrontal region. Sentences beginning with a wh-interrogative may initially deactivate the left prefrontal cortex to prioritize the bottom-up processing of upcoming auditory information. A concrete phrase may obliterate 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.

Highlights

The left prefrontal cortex is essential for verbal communication
Our major observations include that neuronal deactivation, as reflected by suppression of high-gamma activity[8,24,27], took place in the left posterior prefrontal regions around the 1st phrase offset only in trials beginning with a wh-interrogative (Fig. 4a,b)
Such rapid left prefrontal deactivation cannot be attributed to the physical acoustic features of wh-interrogatives per se because wh-interrogatives were associated with left prefrontal activation in trials beginning with a concrete phrase (Fig. 3a,b)

Summary

Introduction

The left prefrontal cortex is essential for verbal communication. It remains uncertain at what timing, to what extent, and what type of phrase initiates left-hemispheric dominant prefrontal activation during comprehension of spoken sentences. Though many investigators have studied language-related neuronal activation heavily, it remains to be addressed at what timing, to what extent, and what type of phrase initiates left-hemispheric dominant prefrontal activation during comprehension of spoken sentences We will address this question and improve our understanding of the neurobiology of language by investigating native Japanese-speaking patients undergoing extraoperative iEEG recordings as a part of the presurgical epilepsy evaluation. (ii) We hypothesize that the magnitude of left prefrontal activation at the 1st phrase offset will be higher when a sentence question begins with a concrete phrase compared to a wh-interrogative This hypothesis is based on our expectation that a concrete word would provide listeners with semantic contexts while a wh-interrogative per se would not. This hypothesis is primarily driven by the observations of prior fMRI studies that increased semantic loads were associated with increased hemodynamic activation in the left anterior prefrontal region, including the Brodmann Area 47 (BA47)[23]

Methods

Results

Conclusion