Lesion evidence for a critical role of left posterior but not frontal areas in alpha-beta power decreases during context-driven word production

Vitória Piai (Corresponding Author), Joost Rommers, Robert T. Knight

Research output: Contribution to journalArticle

Abstract

Different frequency bands in the electroencephalogram are postulated to support distinct language functions. Studies have suggested that alpha–beta power decreases may index word‐retrieval processes. In context‐driven word retrieval, participants hear lead‐in sentences that either constrain the final word (‘He locked the door with the’) or not (‘She walked in here with the’). The last word is shown as a picture to be named. Previous studies have consistently found alpha–beta power decreases prior to picture onset for constrained relative to unconstrained sentences, localised to the left lateral‐temporal and lateral‐frontal lobes. However, the relative contribution of temporal versus frontal areas to alpha–beta power decreases is unknown. We recorded the electroencephalogram from patients with stroke lesions encompassing the left lateral‐temporal and inferior‐parietal regions or left‐lateral frontal lobe and from matched controls. Individual participant analyses revealed a behavioural sentence context facilitation effect in all participants, except for in the two patients with extensive lesions to temporal and inferior parietal lobes. We replicated the alpha–beta power decreases prior to picture onset in all participants, except for in the two same patients with extensive posterior lesions. Thus, whereas posterior lesions eliminated the behavioural and oscillatory context effect, frontal lesions did not. Hierarchical clustering analyses of all patients’ lesion profiles, and behavioural and electrophysiological effects identified those two patients as having a unique combination of lesion distribution and context effects. These results indicate a critical role for the left lateral‐temporal and inferior parietal lobes, but not frontal cortex, in generating the alpha–beta power decreases underlying context‐driven word production.
Original languageEnglish
Pages (from-to)2622-2629
Number of pages8
JournalEuropean Journal of Neuroscience
Volume48
Issue number7
Early online date5 Oct 2017
DOIs
Publication statusPublished - Oct 2018

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Parietal Lobe
Frontal Lobe
Electroencephalography
Cluster Analysis
Language
Stroke
Power (Psychology)

Keywords

  • cloze
  • lexical selection
  • prediction
  • priming
  • spreading activation

Cite this

Lesion evidence for a critical role of left posterior but not frontal areas in alpha-beta power decreases during context-driven word production. / Piai, Vitória (Corresponding Author); Rommers, Joost; Knight, Robert T.

In: European Journal of Neuroscience, Vol. 48, No. 7, 10.2018, p. 2622-2629.

Research output: Contribution to journalArticle

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abstract = "Different frequency bands in the electroencephalogram are postulated to support distinct language functions. Studies have suggested that alpha–beta power decreases may index word‐retrieval processes. In context‐driven word retrieval, participants hear lead‐in sentences that either constrain the final word (‘He locked the door with the’) or not (‘She walked in here with the’). The last word is shown as a picture to be named. Previous studies have consistently found alpha–beta power decreases prior to picture onset for constrained relative to unconstrained sentences, localised to the left lateral‐temporal and lateral‐frontal lobes. However, the relative contribution of temporal versus frontal areas to alpha–beta power decreases is unknown. We recorded the electroencephalogram from patients with stroke lesions encompassing the left lateral‐temporal and inferior‐parietal regions or left‐lateral frontal lobe and from matched controls. Individual participant analyses revealed a behavioural sentence context facilitation effect in all participants, except for in the two patients with extensive lesions to temporal and inferior parietal lobes. We replicated the alpha–beta power decreases prior to picture onset in all participants, except for in the two same patients with extensive posterior lesions. Thus, whereas posterior lesions eliminated the behavioural and oscillatory context effect, frontal lesions did not. Hierarchical clustering analyses of all patients’ lesion profiles, and behavioural and electrophysiological effects identified those two patients as having a unique combination of lesion distribution and context effects. These results indicate a critical role for the left lateral‐temporal and inferior parietal lobes, but not frontal cortex, in generating the alpha–beta power decreases underlying context‐driven word production.",
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note = "Acknowledgements The authors are grateful for the patients and their families, as well as for the other volunteer participants for taking part in this study. We would like to thank Donatella Scabini and Brian Curran for patient delineation, Brian Curran, Clay Clayworth and Callum Dewar for lesion reconstruction, Amber Moncrief and Selvi Paulraj for helping design the materials, Paige Mumford and Laura Agee for help with audio recordings, Kristoffer Dahlsl{\"a}tt for invaluable discussions, and the members of the Center for Aphasia and Related Disorders at the VAHCS in Martinez, CA, for neuropsychological testing. Funding This work is supported by grants from the Netherlands Organization for Scientific Research (446‐13‐009 to V.P., 275‐89‐032 to J.R.), the National Institutes of Health (NINDS R37 NS21135 to R.T.K), and by the Nielsen Corporation. Data accessibility This article's supporting data and materials can be obtained upon request.",
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