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Research Article: New Research, Cognition and Behavior

Alpha and beta oscillations differentially support word production in a rule-switching task

Ioanna Zioga, Ying Joey Zhou, Hugo Weissbart, Andrea E. Martin and Saskia Haegens
eNeuro 15 March 2024, ENEURO.0312-23.2024; https://doi.org/10.1523/ENEURO.0312-23.2024
Ioanna Zioga
1Radboud University, Donders Institute for Brain, Cognition and Behaviour, Center for Cognitive Neuroimaging, 6525 EN Nijmegen, the Netherlands
2Max Planck Institute for Psycholinguistics, 6525 XD Nijmegen, the Netherlands
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Ying Joey Zhou
1Radboud University, Donders Institute for Brain, Cognition and Behaviour, Center for Cognitive Neuroimaging, 6525 EN Nijmegen, the Netherlands
3Oxford Centre for Human Brain Activity, Department of Psychiatry, Oxford, UK
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Hugo Weissbart
1Radboud University, Donders Institute for Brain, Cognition and Behaviour, Center for Cognitive Neuroimaging, 6525 EN Nijmegen, the Netherlands
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Andrea E. Martin
1Radboud University, Donders Institute for Brain, Cognition and Behaviour, Center for Cognitive Neuroimaging, 6525 EN Nijmegen, the Netherlands
2Max Planck Institute for Psycholinguistics, 6525 XD Nijmegen, the Netherlands
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Saskia Haegens
1Radboud University, Donders Institute for Brain, Cognition and Behaviour, Center for Cognitive Neuroimaging, 6525 EN Nijmegen, the Netherlands
4Department of Psychiatry, Columbia University, New York 10032, USA
5Division of Systems Neuroscience, New York State Psychiatric Institute, New York 10032, USA
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Abstract

Research into the role of brain oscillations in basic perceptual and cognitive functions has suggested the alpha rhythm reflects functional inhibition while the beta rhythm reflects neural ensemble (re)activation. However, little is known regarding the generalization of these proposed fundamental operations to linguistic processes, such as speech comprehension and production. Here, we recorded magnetoencephalography (MEG) in participants performing a novel rule-switching paradigm. Specifically, Dutch native speakers had to produce an alternative exemplar from the same category or a feature of a given target word embedded in spoken sentences (e.g., for the word tuna an exemplar from the same category—seafood—would be shrimp, and a feature would be pink). A cue indicated the task rule—exemplar or feature—either before (pre-cue) or after (retro-cue) listening to the sentence. Alpha power during the working-memory delay was lower for retro-cue compared to pre-cue in left hemispheric language-related regions. Critically, alpha power negatively correlated with reaction times, suggestive of alpha facilitating task performance by regulating inhibition in regions linked to lexical retrieval. Furthermore, we observed a different spatiotemporal pattern of beta activity for exemplars vs. features in right temporo-parietal regions, in line with the proposed role of beta in recruiting neural networks for the encoding of distinct categories. Overall, our study provides evidence for the generalizability of the role of alpha and beta oscillations from perceptual to more complex (linguistic) processes, and offers a novel task to investigate links between rule-switching, working memory, and word production.

Significance Statement It remains unclear whether the proposed functional role of alpha and beta oscillations in perceptual function is generalizable to higher-level cognitive processes. We constructed a novel rule-switching paradigm involving speech comprehension and word production. We found that alpha power is modulated by cognitive load and is linked to task performance, potentially by regulating inhibition in brain regions linked to lexical retrieval. Additionally, the spatiotemporal pattern of beta activity differed between two distinct task rules, in line with the proposed role of beta in encoding of distinct categories and recruitment of respective neural networks. We offer experimental findings that support the view of a domain-general role of oscillations across the hierarchy of cognitive functions, from low-level sensory operations to high-level processes.

Footnotes

  • We would like to thank Dennis Joosen and Cas Coopmans for helping with stimuli creation, Fan Bai for providing scripts for processing of the stimuli, and Lisa Horstman for helping with the evaluation of participants’ responses. We thank the LiI BQ5 team for collegial support and discussion.

  • Authors report no conflict of interest.

  • IZ was supported by Big Question 5 (to Prof. dr. Roshan Cools & Dr. Andrea E. Martin) of the Language in Interaction Consortium funded by NWO Gravitation Grant 024.001.006 to Prof. dr. Peter Hagoort. HW was supported by NWO Vidi grant 016.Vidi.188.029 (to AEM). SH was supported by the Netherlands Organisation for Scientific Research (NWO) Vidi grant 016.Vidi.185.137. AEM was supported by an Independent Max Planck Research Group and a Lise Meitner Research Group “Language and Computation in Neural Systems” and by NWO Vidi grant 016.Vidi.188.029.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Alpha and beta oscillations differentially support word production in a rule-switching task
Ioanna Zioga, Ying Joey Zhou, Hugo Weissbart, Andrea E. Martin, Saskia Haegens
eNeuro 15 March 2024, ENEURO.0312-23.2024; DOI: 10.1523/ENEURO.0312-23.2024

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Alpha and beta oscillations differentially support word production in a rule-switching task
Ioanna Zioga, Ying Joey Zhou, Hugo Weissbart, Andrea E. Martin, Saskia Haegens
eNeuro 15 March 2024, ENEURO.0312-23.2024; DOI: 10.1523/ENEURO.0312-23.2024
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