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. 2019 Jun:193:58-72.
doi: 10.1016/j.bandl.2016.06.001. Epub 2016 Jul 19.

The peri-Sylvian cortical network underlying single word repetition revealed by electrocortical stimulation and direct neural recordings

Matthew K Leonard  1 , Ruofan Cai  1 , Miranda C Babiak  1 , Angela Ren  1 , Edward F Chang  2
Affiliations

The peri-Sylvian cortical network underlying single word repetition revealed by electrocortical stimulation and direct neural recordings

Matthew K Leonard et al. Brain Lang. 2019 Jun.

Abstract

Verbal repetition requires the coordination of auditory, memory, linguistic, and motor systems. To date, the basic dynamics of neural information processing in this deceptively simple behavior are largely unknown. Here, we examined the neural processes underlying verbal repetition using focal interruption (electrocortical stimulation) in 58 patients undergoing awake craniotomies, and neurophysiological recordings (electrocorticography) in 8 patients while they performed a single word repetition task. Electrocortical stimulation revealed that sub-components of the left peri-Sylvian network involved in single word repetition could be differentially interrupted, producing transient perceptual deficits, paraphasic errors, or speech arrest. Electrocorticography revealed the detailed spatio-temporal dynamics of cortical activation, involving a highly-ordered, but overlapping temporal progression of cortical high gamma (75-150Hz) activity throughout the peri-Sylvian cortex. We observed functionally distinct serial and parallel cortical processing corresponding to successive stages of general auditory processing (posterior superior temporal gyrus), speech-specific auditory processing (middle and posterior superior temporal gyrus), working memory (inferior frontal cortex), and motor articulation (sensorimotor cortex). Together, these methods reveal the dynamics of coordinated activity across peri-Sylvian cortex during verbal repetition.

Keywords: Electrocortical stimulation; Electrocorticography; Neurosurgery; Peri-Sylvian cortex; Speech perception; Speech production; Verbal repetition.

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Figures

Figure 1
Figure 1. Two complementary methods for examining the cortical networks involved in verbal repetition
(a) Example intraoperative photograph showing exposed craniotomy and markers where electrocortical stimulation was performed. (b) Reconstructed brain showing all positive stimulation sites across 47 patients, covering the major peri-Sylvian regions hypothesized to be involved in verbal repetition. (c) Example intraoperative photograph showing exposed craniotomy and high-density 256-channel ECoG grid covering peri-Sylvian cortex. (d) Reconstructed brain showing all electrode locations included in the ECoG analyses for 8 patients.
Figure 2
Figure 2. 7 error types elicited by ECS to peri-Sylvian cortex
(a) Perceptual errors (patient “did not hear”) stimulus. (b) Phonological errors (addition, deletion, or change of phonemes/syllables in the target word). (c) No response errors. (d) Neologism errors (patient says a phonologically plausible pseudoword). (e) Perseveration errors (patient repeats previous stimulus). (f) Motor speech errors (slurred or distorted speech). (g) Offset errors (no response until after ECS).
Figure 3
Figure 3. Phonological errors broken down by syllable position
There was a significant decrease in the number of correct responses over the course of each word. This effect was driven by significant increases in syllable deletion and syllable addition across syllables 1–4. There were no significant effects of syllable position on phoneme-related phonological errors (“Vow” = vowels, “Con” = consonants). Asterisks represent statistical significance at P < 0.05 (Bonferroni corrected).
Figure 4
Figure 4. Functional clustering of ECoG responses using NMF reveals distributed and overlapping functions underlying verbal repetition
(a) During the listening phase of the task, participants heard a cue (slide projector sound), followed by a word. (b) After a 2 second delay, participants heard a cue (beep) and then repeated the word they had heard in the listening phase. The data from both phases were concatenated and clustered using convex NMF, a ‘soft’ clustering technique that assigns probabilities for each electrode belonging to one of five clusters. Early auditory responses to all acoustic input during the listening (c) and speaking (d) phases were localized primarily to posterior STG (e). Auditory responses unique to spoken input during listening (f) and speaking (g) were localized to the entire extent of STG, with additional electrodes in ventral and dorsal frontal areas (h). Ongoing activity during the delay period between listening (i) and speaking (j) was associated with working memory, and was primarily localized to lateral frontal cortex, with some electrodes in auditory regions (k). A separate cluster of speech-specific auditory responses during listening (l) and speaking (m) showed similar localization as cluster 2 (n), except with longer latency peaks. Finally, a cluster showed no responses during listening (o), followed by large production-evoked responses around movement onset (p), primarily in vSMC electrodes (q).
Figure 5
Figure 5. Clusters involved in various stages of verbal repetition are modulated by word length and lexical frequency
(a) For each of the 438 electrodes at each time point during the listening phase, high-gamma activity was predicted from a linear combination of word length and lexical frequency using regression. R2 values for these models (P < 0.05) peaked between 500–1000ms after stimulus onset (dashed lines). These two variables accounted for up to ~75% of the variance on some electrodes. (b) To determine whether word length and lexical frequency effects differed across the 5 clusters identified in previous analyses, the R2 distributions for each frequency were plotted. While mean R2 differed slightly (black dots), there were no significant differences across clusters. (c) Electrodes plotted with dominant cluster membership (color) and peak R2 value (intensity) demonstrate that word length and lexical frequency effects are pervasive throughout peri-Sylvian regions that are involved in verbal repetition.
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