Distinct age-related alterations in alpha-beta neural oscillatory activity during verbal working memory encoding in children and adolescents.

Abstract

Emerging imaging studies of working memory (WM) have identified significant WM-related oscillatory events that are unique to each phase of working memory (e.g. encoding, maintenance). Although many previous imaging studies have shown age-related changes within the frontoparietal network when performing a WM task, understanding of the age-related changes in the oscillatory dynamics underlying each phase of WM during development and their relationships to other cognitive function is still in its infancy. To this end, we enrolled a group of 74 typically-developing youths aged 7-15 years to perform a letter-based Sternberg WM task during magnetoencephalography. Trial-wise data were transformed into the time-frequency domain, and significant oscillatory responses during the encoding and maintenance phases of the task were independently imaged using beamforming. Our results revealed widespread age-related power differences in alpha-beta oscillatory activity during encoding throughout left frontal, parietal, temporal, occipital and cerebellar regions. By contrast, age-related differences in maintenance-related activity were limited to a small area in the superior temporal gyrus and parieto-occipital regions. Follow-up exploratory factor analysis of age-related encoding alpha-beta activity revealed two distinct factors, and these factors were each found to significantly mediate age-related improvements in both verbal and non-verbal cognitive ability. Additionally, late maintenance alpha activity was related to reaction time on the task. Taken together, our results indicate that the neural dynamics in the alpha and beta bands are uniquely sensitive to age-related changes throughout this developmental period and are related to both task performance and other aspects of cognitive development. KEY POINTS: Understanding of the age-related changes in neural oscillatory dynamics serving verbal working memory function is in its infancy. This study identified the age-related neural alterations during each phase of working memory processing in youths. Developmental differences during working memory processing were primarily isolated to alpha-beta activity during the encoding phase. Alpha-beta activity during encoding significantly mediated age-related improvements in both verbal and non-verbal ability. This study establishes new brain-behaviour relationships linking working memory function to other aspects of cognitive development.