Brain network dynamics in the human articulatory loop

Abstract

Objective The articulatory loop is a fundamental component of language function, involved in the short-term buffer of auditory information followed by its vocal reproduction. We characterized the network dynamics of the human articulatory loop, using invasive recording and stimulation. Methods We measured high-gamma activity70-110 Hz recorded intracranially when patients with epilepsy either only listened to, or listened to and then reproduced two successive tones by humming. We also conducted network analyses, and analyzed behavioral responses to cortical stimulation. Results Presentation of the initial tone elicited high-gamma augmentation bilaterally in the superior-temporal gyrus (STG) within 40 ms, and in the precentral and inferior-frontal gyri (PCG and IFG) within 160 ms after sound onset. During presentation of the second tone, high-gamma augmentation was reduced in STG but enhanced in IFG. The task requiring tone reproduction further enhanced high-gamma augmentation in PCG during and after sound presentation. Event-related causality (ERC) analysis revealed dominant flows within STG immediately after sound onset, followed by reciprocal interactions involving PCG and IFG. Measurement of cortico-cortical evoked-potentials (CCEPs) confirmed connectivity between distant high-gamma sites in the articulatory loop. High-frequency stimulation of precentral high-gamma sites in either hemisphere induced speech arrest, inability to control vocalization, or forced vocalization. Vocalization of tones was accompanied by high-gamma augmentation over larger extents of PCG. Conclusions Bilateral PCG rapidly and directly receives feed-forward signals from STG, and may promptly initiate motor planning including sub-vocal rehearsal for short-term buffering of auditory stimuli. Enhanced high-gamma augmentation in IFG during presentation of the second tone may reflect high-order processing of the tone sequence. Significance The articulatory loop employs sustained reciprocal propagation of neural activity across a network of cortical sites with strong neurophysiological connectivity.

Neural dynamics of verbal working memory in auditory description naming

“…Our hypothesis is also consistent with the ‘phonological loop model’, suggesting that accurate vocal responses to speech sounds are secured by “short-term maintenance of stimuli via sub-vocal rehearsal” 3 , 25 , 26 . Convergent with the present data, previous studies using cortico-cortical evoked potentials suggest that STG is directly and functionally connected to iPreCG of the same hemisphere 27 , 28 . Data from MRI tractography suggest that STG and iPreCG are connected mainly via the arcuate and uncinate fasciculi 29 – 33 , which are thus the most likely candidates for the conduction of information through this portion of the phonological loop.…”

“…The collective evidence led to the hypothesis that iPreCG comprises a part of multiple large-scale networks responsible for working memory maintenance, subsequent scanning, as well as overt articulation during auditory naming task. Future studies incorporating cortical mapping using electrical stimulation time-locked to each period of interest, as well as analysis of ECoG high-gamma information flow, such as event-related causality analysis 28 , 48 , may provide important convergent evidence for this hypothesis.…”

Four‐dimensional functional cortical maps of visual and auditory language: Intracranial recording

“…Our recent ECoG study utilizing an auditory verbal working memory task suggested that the left inferior‐precentral gyrus supports initial maintenance of a mental representation of memory items, whereas the left inferior‐frontal gyrus contributes to later scanning function to determine a match among previously encountered items . Studies utilizing corticocortical evoked potentials and diffusion tensor tractography have demonstrated that the left inferior‐precentral gyrus is effectively connected structurally and functionally to both the superior‐temporal and inferior‐frontal gyri …”

Whole-Brain Network Connectivity Underlying the Human Speech Articulation as Emerged Integrating Direct Electric Stimulation, Resting State fMRI and Tractography

“…Secondly, our findings imply a role of the right hemisphere in speech articulation. Previous task-based fMRI and intracranial cortico-cortical studies reported activation of regions of the right hemisphere for speech articulation in right handed subjects ( Basilakos et al, 2015 ; Nishida et al, 2017 ), particularly of the STG and premotor and motor cortices. However, the multimodal approach used in this work (i.e., DES sites based rs-fMRI) allows extending the results from previous studies demonstrating, consistently across subjects, iFC of the articulatory loop between homologous regions across brain hemispheres.…”

“…With respect to functional connectivity of speech articulation, a recent invasive study characterized the temporal evolution of this network using intracranial recording and stimulation on 10 right handed pediatric epilepsy patients responding a tone listening and repetition task ( Nishida et al, 2017 ). The authors recorded cortical–cortical evoked potential in the inferior frontal gyrus (IFG) and superior temporal gyrus (STG) following stimulation of the precentral gyrus (PCG) that caused speech arrest in the investigated hemisphere (five left, five right).…”