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

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.

Transient perturbation of the left temporal cortex evokes plasticity-related reconfiguration of the lexical network

“…At the neuronal level, the sham condition replicated previous findings of power decreases in the alpha-beta band in left temporal and inferior parietal regions prior to picture onset (Piai et al, 2017(Piai et al, , 2014(Piai et al, , 2015(Piai et al, , 2018. By contrast, the left MTG perturbation resulted in attenuated scalp effects and, at the source level, additional recruitment of left prefrontal regions concurrent with the left posterior activity.…”

“…Behaviorally, we expected a performance decrease in the naming task following real as opposed to sham TMS as a direct marker of the disturbance of the language network. The crucial question was how the oscillatory power modulation in the alpha and beta bands (8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25), as previously observed in the healthy and reorganized brain after left-hemispheric lesions (Piai, Meyer, Dronkers, & Knight, 2017;Piai, Roelofs, & Maris, 2014;Piai, Roelofs, Rommers, & Maris, 2015;Piai, Rommers, & Knight, 2018), would be affected by the focal perturbation. Following lesion evidence, the oscillatory pattern might shift entirely to the right hemisphere.…”

“…We employed the context-driven picture naming task used in previous studies (Piai et al, 2017(Piai et al, , 2014(Piai et al, , 2015(Piai et al, , 2018. 200 pictures were selected which served as target stimuli.…”

The Relation between Alpha/Beta Oscillations and the Encoding of Sentence induced Contextual Information

“…Beyond sensory processing, recent theory and evidence suggests that alpha/beta oscillations would also be involved in linguistic prediction (Kuperberg & Jaeger, 2015;. Decreases in alpha power (Lam et al, 2016;Piai et al, 2017;Wang et al, 2017) and low-beta power (Bastiaansen & Hagoort, 2015;Piai et al, 2017;Wang et al, 2017) have previously been linked to the processing of sentential context constraints. Specifically, the power decrease has been found to be stronger when sentential context is highly predictive of the last word of the sentence (i.e.…”

“…when cloze probability is low) (Bastiaansen & Hagoort, 2015;Lam et al, 2016;Rommers et al, 2017;Piai et al, 2017;Wang et al, 2017;Wang et al, 2012;Weiss & Mueller, 2012;Willems et al, 2008). Yet, the evidence for alpha/beta oscillations in language prediction is still debated, as it has only been observed for strong cloze probability situations (Piai et al, 2017;Wang et al, 2017). If alpha/beta power reflect the degree of predictability of an upcoming word, we hypothesized that alpha/beta power should gradually decrease with higher cloze probability.…”