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PreprintCited by 2Neurobiology of Language and BilingualismPhonetics and Phonology ResearchMotor Control and Adaptation

Supplementary motor area in speech initiation: a large-scale intracranial EEG evaluation of stereotyped word articulation

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Bullock, Latané, Forseth, Kiefer J, Woolnough, Oscar, Rollo, Patrick S, Tandon, Nitin·2023·bioRxiv (Cold Spring Harbor Laboratory)
DOI 10.1101/2023.04.04.535557

Preprint — published as 10.1016/j.isci.2024.111531

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Abstract

Speech production is known to engage a distributed network. The brain regions responsible for the initiation of articulation are unclear, and they would be expected to coordinate a distributed network. Using direct intracranial recordings in a large cohort, during stereotyped speech production to eliminate confounds of phonological and semantic complexity, we performed a comprehensive analysis of cortical sites engaged in speech initiation. We found that the supplementary motor area (SMA) was the earliest speech motor region to be active prior to speech onset and was active almost exclusively prior to articulation. Broadband gamma activity in the SMA was predictive of the response time of word production, predicting response time from 250 ms after stimulus onset. Neural activity in SMA began at a highly predictable time after stimulus onset and extended until speech onset. SMA activity offset coincided with ventral premotor cortex and primary motor activity onset . This suggests that the SMA may coordinate the concerted activation of motor execution cortex. Our results support the idea that SMA is a key node in the speech initiation network. Significance statement: Producing speech requires coordination across multiple brain regions. One cortical region - the supplementary motor area (SMA) - has long been a candidate region to coordinate across other regions to initiate speech production. In this study, we used human intracranial recordings from patients with epilepsy to investigate the role of the SMA in initiating speech. In a picture-naming task, subjects repeated the word “scrambled” scores of times; using this condition to eliminate any linguistic confounds, we found that the SMA was consistently one of the earliest regions to activate during word production. We also uncovered the SMA’s temporally precise tuning to speech onset at the single-trial level.

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  • Speech decoders have yet to fully leverage feedback-based learning paradigms that could entrain new patterns of neural activity for better control.

    “Finally, speech decoders have yet to fully leverage paradigms of feedback-based learning that have the potential to entrain new patterns of neural activity for better control171–174.”

    From The speech neuroprosthesis (2024) · cites this paper as [171]

    The Introduction and Experimental Paradigm describe intracranial recordings during speech initiation and a picture-naming task, not speech-decoder training. Searches for feedback-based learning, entrainment, and decoders found no passage addressing whether such paradigms have been underused or could improve decoder control. Page numbers were not provided in our copy. (LLM, conf=0.75)

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Research works printed but not linked: 12

  1. was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. The copyright holder for this preprint (which this version posted April 4, 2023. ; https://doi.org/10.1101/2023.04.04.535557 doi: bioRxiv preprint
  2. Dale, A. M., Fischl, B., & Sereno, M. I. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage, 9(2), 179-194. https://doi.org/10.1006/nimg.1998.0395 · DOI · Paper page
  3. was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. The copyright holder for this preprint (which this version posted April 4, 2023. ; https://doi.org/10.1101/2023.04.04.535557 doi: bioRxiv preprint
  4. Forseth, K. J., Pitkow, X., Fischer-Baum, S., & Tandon, N. (2021). What The Brain Does As We Speak (p. 2021.02.05.429841). bioRxiv. https://doi.org/10.1101/2021.02.05.429841 · DOI
  5. Guenther, F. H. (2016). Neural Control of Speech. MIT Press.
  6. Hayes, B. (2011). Introductory Phonology. John Wiley & Sons.
  7. Hickok, G. (2012). Computational neuroanatomy of speech production. Nature Reviews Neuroscience, 13(2), 135-145. https://doi.org/10.1038/nrn3158 · DOI · Paper page
  8. was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. The copyright holder for this preprint (which this version posted April 4, 2023. ; https://doi.org/10.1101/2023.04.04.535557 doi: bioRxiv preprint
  9. was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. The copyright holder for this preprint (which this version posted April 4, 2023. ; https://doi.org/10.1101/2023.04.04.535557 doi: bioRxiv preprint
  10. McGraw Hill.
  11. Zentner, J., Hufnagel, A., Pechstein, U., Wolf, H. K., & Schramm, J. (1996). Functional results after resective procedures involving the supplementary motor area. Journal of Neurosurgery, 85(4), 542-549. https://doi.org/10.3171/jns.1996.85.4.0542 · DOI
  12. was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission.

Cited by

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  • The speech neuroprosthesis

    Silva, A. B., Littlejohn, K. T., Liu, J. R., Moses, D. A., & Chang, E. F. (2024) · Nature Reviews Neuroscience · doi:10.1038/s41583-024-00819-9 · Cited by 103 · see citing works

    “A recent non-peer-reviewed preprint found that neural populations in the SMA are among the earliest predictors of speech onset and may remain strongly activated in imagined and attempted speech 170 .”

Related

Authors
Bullock, L., Forseth, K. J., Woolnough, O., Rollo, P. S., & Tandon, N.
Affiliations
  • The University of Texas Health Science Center at Houston (US)
  • University of California San Diego (US)
  • Memorial Hermann (US)
Corresponding author
Tandon, Nitin
ORCID
Venue
bioRxiv (Cold Spring Harbor Laboratory)
Publisher
openRxiv
Published
2023-04-04
DOI
10.1101/2023.04.04.535557
OpenAlex
W4362528251
Cited by
2
References
72
Citations by year
2024: 2
Type
posted content
Language
en
Open access
Locations
bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
Funders
  • University of Texas System
  • National Institutes of Health (NIH-R01)
  • National Institute on Deafness and Other Communication Disorders (R01DC014589)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neurobiology of Language and Bilingualism
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Phonetics and Phonology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
Keywords
supplementary motor area, speech initiation, speech production, intracranial EEG, response time prediction, ventral premotor cortex, primary motor cortex, picture naming, epilepsy patients

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