Temporally and spatially distinct theta oscillations dissociate a language-specific from a domain-general processing mechanism across the age trajectory

Caroline Beese,Benedict Vassileiou,Angela D Friederici,Lars Meyer

doi:10.1038/s41598-017-11632-z

Caroline Beese, Benedict Vassileiou + Show 2 more

Open Access

https://doi.org/10.1038/s41598-017-11632-z

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Abstract

The cognitive functionality of neural oscillations is still highly debated, as different functions have been associated with identical frequency ranges. Theta band oscillations, for instance, were proposed to underlie both language comprehension and domain-general cognitive abilities. Here we show that the ageing brain can provide an answer to the open question whether it is one and the same theta oscillation underlying those functions, thereby resolving a long-standing paradox. While better cognitive functioning is predicted by low theta power in the brain at rest, resting state (RS) theta power declines with age, but sentence comprehension deteriorates in old age. We resolve this paradox showing that sentence comprehension declines due to changes in RS theta power within domain-general brain networks known to support successful sentence comprehension, while low RS theta power within the left-hemispheric dorso-frontal language network predicts intact sentence comprehension. The two RS theta networks were also found to functionally decouple relative to their independent internal coupling. Thus, both temporally and spatially distinct RS theta oscillations dissociate a language-specific from a domain-general processing mechanism.

Highlights

Language comprehension in general remains remarkably stable across the lifespan; sentence comprehension, is known to decline with age[1, 2]
The ANOVA of the behavioural data showed a main effect of age group, F(2,54) = 11.74, p = 5.86 × 10−5, η2 = 0.30, indicating that d-prime decreases with age (Fig. 2a)
Given that those domain-general measures are all significantly correlated with the sentence comprehension task, this may suggest a role for the age-related decline in domain-general cognitive

Summary

Introduction

Language comprehension in general remains remarkably stable across the lifespan; sentence comprehension, is known to decline with age[1, 2] This age-related decline holds for working memory-intensive sentences[3], which predominantly tax the encoding and retention of verbal information across increased intervals[3,4,5,6]. Likewise, processing differences have been found during the disambiguation of ambiguous sentences, with larger ERP differences for high-span readers than for low-span readers[7] Such differences are pronounced when ambiguities are extended[7], possibly suggesting[3] that low-span readers’ verbal working memory resources are exhausted by the increased duration of an ambiguity[4, 5, 9, 15]. Increasing sentence duration decreases older adults’ sentence comprehension accuracy[18, 19, 24]: Poorer repetition accuracy was found for 8-word sentences compared to 5-word sentences in older but not in young adults[24]

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