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Research ArticleResearch 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, 11 (4) ENEURO.0312-23.2024; https://doi.org/10.1523/ENEURO.0312-23.2024
Ioanna Zioga
1Donders Centre for Cognitive Neuroimaging, Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen 6525 EN, The Netherlands
2Max Planck Institute for Psycholinguistics, Nijmegen 6525 XD, The Netherlands
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Ying Joey Zhou
1Donders Centre for Cognitive Neuroimaging, Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen 6525 EN, The Netherlands
3Department of Psychiatry, Oxford Centre for Human Brain Activity, Oxford, United Kingdom
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  • ORCID record for Ying Joey Zhou
Hugo Weissbart
1Donders Centre for Cognitive Neuroimaging, Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen 6525 EN, The Netherlands
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Andrea E. Martin
1Donders Centre for Cognitive Neuroimaging, Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen 6525 EN, The Netherlands
2Max Planck Institute for Psycholinguistics, Nijmegen 6525 XD, The Netherlands
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Saskia Haegens
1Donders Centre for Cognitive Neuroimaging, Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen 6525 EN, The Netherlands
4Department of Psychiatry, Columbia University, New York, New York 10032
5Division of Systems Neuroscience, New York State Psychiatric Institute, New York, New York 10032
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    Figure 1.

    Trial structure. The experimental stimuli were in Dutch; for illustrative purposes, the English translation is shown here.

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    Figure 2.

    Behavioral performance. A, Accuracy (rate of correct responses), separately for pre- versus retro-cue trials and for exemplars (purple) versus features (green). B, Reaction times. C, Speed–accuracy trade-off: rate of correct responses for fast to slow reaction time bins. D, Logarithm base 10 of the word frequency of responses. E, Intersubject variability (how many different responses were given over all participants). F, Results from a generalized linear mixed-effects model predicting reaction times from word frequency with subject as random-effects predictor. For plotting purposes, the raincloud plot shows coefficients of a GLM per subject. ***p < 0.001, **p < 0.010.

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    Figure 3.

    Time-frequency analysis comparing pre- versus retro-cue conditions. A, TFRs of pre- versus retro-cue trials, showing t values averaged over significant sensors denoted in the topography (right), masked by significance (opacity mask). B, Power averaged over significant sensors and time points (time window 4.9–11.5 s), separately for exemplar (purple) and feature (green) and for pre- and retro-cue conditions. Power values were converted to decibel by calculating the 10 times base 10 logarithm of the ratio versus baseline power (averaged from −0.45 to −0.25 s). C, Left, Time courses of alpha power (8–13 Hz) for pre- (dark gray) and retro-cue conditions (light gray). Horizontal lines indicate significant time windows. Right, Source reconstructions for pre- versus retro-cue, showing t values exceeding the 95th percentile. D, Same as C for the beta band (14–25 Hz). Error bars represent ±1 SEM. ***p < 0.001.

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    Figure 4.

    Time-frequency analysis comparing exemplar versus feature conditions. A, TFRs of exemplar versus feature in pre-cue trials, showing t values averaged over significant sensors denoted in the topographies (bottom), separately for the alpha (left), and the beta band cluster (right), masked by significance. B, Time courses of alpha (10–12 Hz) (left) and beta power (13–22 Hz) (right) for exemplar (purple) and feature (green). Horizontal lines indicate significant time windows. C, Source reconstructions for exemplar versus feature in pre-cue trials, showing t values exceeding the 95th-percentile (left, alpha; right, beta). Bar plots show power averaged over significant sensors and time points (time window 6–8 s), separately for each condition. Error bars represent ±1 SEM. ***p < 0.001.

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    Figure 5.

    Relationship between neural measures and reaction times. A, Scatterplot showing a positive relationship between IAF power in left frontal channels (denoted in the topography) and reaction times, as evidenced by a generalized linear mixed-effects model. B, Same as A for the beta band.

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    Table 1.

    Model fit statistics and log likelihood comparisons between mixed-effects regression models predicting reaction times

    Model nComparisonPredictorsdfχ2p
    Behavioral GLMMs
     1-WF4−411.31ΝΑ
     22 vs 1WF + cue5−211.88<0.001
     33 vs 1WF + task5−396.160.001
     4a4 vs 2aWF + cueXtaska7a−185.58a<0.001a
     55 vs 4WFXcueXtask10−184.560.564
    Neural GLMMs
     1-IAF4−485.49ΝΑ
     22 vs 1IAF + cue5−260.17<0.001
     33 vs 1IAF + task5−460.33<0.001
     4a4 vs 2aIAF + cueXtaska7a−224.57a<0.001a
     55 vs 4IAFXcueXtask10−222.740.301
    • Model n: model number. Comparison: contrasted models. Predictors: predictors included in the model. LRT, log likelihood ratio test; WF, word frequency; Task, task rule; IAF, individual alpha peak frequency power at left frontal sensors; χ2, chi-squared test. X denotes main effect and interaction.

    • ↵a Best model based on likelihood ratio tests.

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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, 11 (4) 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, 11 (4) ENEURO.0312-23.2024; DOI: 10.1523/ENEURO.0312-23.2024
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Keywords

  • alpha oscillations
  • beta oscillations
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