Abstracts

Rationale: In human language, each phoneme is produced by vibration of the vocal cord in the throat along with a distinct position of the mouth. Previous neuroimaging studies have localized ‘what’ cortical circuits are involved in perception and production of speech; it was reported that such cortical circuits include the superior temporal gyrus as well as the inferior portion of the Rolandic area bilaterally with larger extent in the left hemisphere. Here, we determined ‘how’ these cortical structures were activated by listening and subsequent overt articulation of syllables, by measuring event-related gamma-oscillations as quantitative measures of cortical activation. Methods: We studied 15 patients with uncontrolled focal seizures (7-18 years) who underwent epilepsy surgery in our institute. All subjects underwent extraoperative electrocorticography (ECoG) and electrical neurostimulation as a part of clinical management. Subdural electrodes were placed on the left hemisphere in six subjects and on the right in the other nine. Subjects were presented an auditory-syllable consisting of either ‘fee [fi:]’, ‘faa [fa:]’, ‘hee [hi:]’, or ‘haa [ha:]’ 80 times; each auditory-syllable was given 20 times in a pseudorandom sequence. Subjects were instructed to overtly repeat each given syllable during ECoG recording. Each ECoG trial was transformed into the time-frequency domain, and we delineated ‘when’ and ‘where’ gamma-oscillations were increased (cortical activation) or decreased (cortical deactivation), using our in-vivo animation technique. Results: Gamma-oscillations in the superior temporal gyrus were highly augmented during syllable-presentation, least augmented at the onset of syllable articulation, and again highly augmented following syllable-articulation. Gamma-oscillations were augmented in the inferior Rolandic area prior to and during syllable-articulation with the onset and peak occurring earlier in the left side. Subsets of the inferior Rolandic sites, more frequently on the left side, showed differential gamma-augmentation induced by articulation of phoneme [f] more than [h] or phoneme [i:] more than [a:]. Overall, statistical analyses suggested that electrical neurostimulation of sites showing event-related gamma-augmentation elicited congruent clinical symptoms more frequently than that of the remaining sites did. Conclusions: The superior temporal gyrus may be active when externally-presented or self-articulated auditory stimuli are present to be processed, and may be modestly active but not necessarily completely suppressed when articulation is initiated. Phoneme-specific differential gamma-augmentation in the inferior Rolandic area may be partially attributed to mouth positioning during phoneme-articulation. Our observations support the hypothesis that positioning of the mouth to articulate phonemes is predominantly driven and/or monitored by the primary sensorimotor area on the left side. (NIH grants NS47550 & NS64033 to E. Asano)