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

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.

Figure 1

Four-frame cartoon summarizing the results of the present study. (a) and (b) The present study will demonstrate that verbal questions beginning with a wh-interrogative deactivate the left posterior prefrontal regions immediately after the 1st phrase offset. (c) and (d) Conversely, those beginning with a concrete word activate the left posterior prefrontal regions immediately after the 1st phrase offset. It should be noted that an adposition follows a noun in Japanese but precedes in English.

Figure 2

Spoken sentence stimuli used for measurement of task-related high-gamma modulations. (a) Patients were instructed to listen to a series of sentence questions and overtly provide a relevant answer to each item during extraoperative intracranial EEG recording. The response time was defined as the period between sentence offset (i.e., 3rd phrase offset) and response onset. A 400-ms resting period, at 200–600 ms before the stimulus onset, was treated as the baseline period for measurement of task-related high-gamma modulations. We have prepared 192 sentence stimuli, in total, for the present study. (b) Ninety-six stimuli were characterized by the following order of three phrases: [adverb or object], [verb], and [what, when, or where]. Each of the 96 sentence stimuli begins with a concrete word; [adverb or object] starts with a concrete noun because an adposition (e.g., ’-o’) follows a noun in Japanese but precedes in English (e.g., ’in the’). (c) Each of the other 96 sentence stimuli (each with the same semantic context as one of the former 96) begins with a wh-interrogative and is characterized by the following order of three phrases: [what, when, or where], [adverb or object], and [verb]. A given patient was assigned 48 question stimuli beginning with a concrete phrase and 48 beginning with a wh-interrogative; thereby, none of the assigned 96 questions shared the same semantic context. Sentence types were counterbalanced across patients.

Figure 3

Snapshots of task-related high-gamma modulations. The video snapshots demonstrate the percent change of high-gamma activity relative to the baseline period (i.e., between − 600 and − 200 ms relative to stimulus onset). (a) At 120 ms following the 1st phrase onset, the bilateral superior-temporal gyri (STG) showed high-gamma augmentation. (b) At 700 ms following stimulus onset (i.e., after the 1st phrase offset), high-gamma activity in the left posterior prefrontal region was augmented during trials beginning with a concrete phrase (red arrow) but suppressed during those beginning with a wh-interrogative (blue arrow). (c) At 1,950 ms following the 1st phrase onset (i.e., after the 3rd phrase offset), high-gamma augmentation involved the left temporal and frontal lobe regions, extensively, commonly across the sentence types. (d) At 120 ms after response onset, high-gamma augmentation involved the Rolandic areas and STG bilaterally.

Figure 4

The dynamics of high-gamma modulations during sentence comprehension task. (a)-(d) High-gamma modulations in the left hemisphere. (e) High-gamma modulations in the right hemisphere. The mean percent change in high-gamma activity is presented with a standard error bar. Red plots and bars: Trials beginning with a concrete phrase. Blue plots and bars: Trials beginning with a wh-interrogative. Upper horizontal bars: Significant amplitude augmentation lasting at least 60 ms (including at least four 65 Hz-band oscillations). Lower horizontal bars: Significant amplitude suppression lasting at least 60 ms. First column: Time-locked to the 1st phrase onset (i.e., sentence onset). Second column: Time-locked to the 1st phrase offset. Third column: Time-locked to the 2nd phrase offset. Fourth column: Time-locked to the 3rd phrase offset (i.e., sentence offset). (a) and (b) The left posterior middle- and inferior-frontal gyri (MFG and IFG) showed a rising of high-gamma activity around the 1st phrase offset during trials beginning with a concrete phrase. These regions showed high-gamma suppression maximally around the 1st phrase offset during trials beginning with a wh-interrogative. (c) and (d) The left anterior MFG and orbitofrontal regions showed high-gamma suppression maximally around the 2nd phrase offset during trials beginning with a wh-interrogative. (e) The right orbitofrontal region showed high-gamma suppression maximally before the 1st phrase offset during trials beginning with a concrete phrase.

Figure 5

Phrase order-specific high-gamma modulations during sentence comprehension. (a) and (c) The left posterior middle- and inferior-frontal gyri (MFG and IFG) showed a rising of high-gamma activity around the 1st phrase offset during trials beginning with a concrete phrase. These regions showed high-gamma suppression maximally around the 1st phrase offset during trials beginning with a wh-interrogative. (b) and (d) The left anterior MFG and orbitofrontal regions showed high-gamma suppression maximally around the 2nd phrase offset during trials beginning with a wh-interrogative. (i) The right posterior MFG showed high-gamma suppression immediately before the 2nd phrase onset specifically during trials beginning with a concrete phrase. (l) The right orbitofrontal region showed high-gamma suppression immediately before the 1st phrase offset specifically during trials beginning with a concrete phrase.