Abstracts

Rationale: The articulatory loop is a fundamental language network, involved in the perception and short-term storage of auditory information, as well as the subsequent production of vocal output. We determined 'when' and 'where' the articulatory loop system works in human brain using electrocorticography (ECoG) and stimulation mapping.Methods: We studied 10 right-handed children with focal epilepsy (age range: 11-17 years; average age: 14 years; seven females). We characterized the temporal-spatial profiles of high-gamma activity (70-110 Hz) recorded intracranially when participants either only listened to or listened to and reproduced two successive tones by humming.Results: Presentation of the initial tone elicited high-gamma augmentation bilaterally in the posterior half of the superior-temporal gyri within 40 ms, and subsequently in the lateral-precentral gyri 4-5cm above the Sylvian fissure and in the inferior-frontal gyri within 160 ms after sound onset. During presentation of the second tone, high-gamma augmentation was reduced in the superior-temporal gyrus but enhanced in the inferior frontal gyrus. Increasing working memory demand within the articulatory loop, by requesting participants to reproduce given tones, resulted in a rapid and sustained enhancement of high-gamma augmentation in the lateral-precentral gyri. Measurement of cortico-cortical evoked potentials revealed the presence of efficient cortico-cortical connectivity between the superior-temporal, lateral-precentral, and inferior-frontal sites showing high-gamma augmentation. Overt reproduction of tone stimuli was accompanied by high-gamma augmentation over larger extents of the lateral-precentral gyri. High-frequency stimulation of lateral-precentral sites showing the earliest high-gamma augmentation in either hemisphere induced speech arrest, inability to control vocalization, or forced vocalization.Conclusions: In summary, portions of bilateral lateral-precentral and inferior-frontal gyri rapidly and directly receive feed-forward signals from the superior-temporal gyri where auditory information is initially perceived. The earliest sound-listening-related high-gamma augmentation within the lateral-precentral gyri may reflect rapid initiation of motor planning such as subvocal rehearsal for short-term storage of auditory stimuli. Such lateral-precentral sites are suggested to communicate with the superior-temporal and inferior-frontal gyri during and after the sound presentation. Enhanced high-gamma augmentation in the inferior-frontal gyri during the second tone presentation may reflect high-order processing of auditory stimuli. Widespread lateral-precentral high-gamma augmentation peaking during the humming responses likely reflected execution of overt vocalization. Our findings suggest that the human articulatory loop employs sustained propagation of neural activity across a network of cortical sites with strong neurophysiological connectivity.