Differential representations of spatial location by aperiodic and alpha oscillatory activity in working memory

Abstract

Decades of research have shown working memory (WM) relies on sustained pre-frontal cortical activity and visual extrastriate activity, particularly in the alpha (8-12 Hz) frequency range. This alpha activity tracks the spatial location of WM items, even when spatial position is task-irrelevant and there is no stimulus currently being presented. Traditional analyses of putative oscillations using bandpass filters, however, conflate oscillations with non-oscillatory aperiodic activity. Here, we reanalyzed seven different human electroencephalography (EEG) visual WM datasets to test the hypothesis that aperiodic activity-which is thought to reflect the relative contributions of excitatory and inhibitory drive-plays a distinct role in visual WM from true alpha oscillations. To do this, we developed a novel, time-resolved spectral parameterization approach to disentangle oscillations from aperiodic activity during WM encoding and maintenance. Across all seven tasks, totaling 112 participants, we captured the representation of spatial location from total alpha power using an inverted encoding model (IEM), replicating traditional analyses. We then trained separate IEMs to estimate the strength of spatial location representation from aperiodic-adjusted alpha (reflecting just the oscillatory component) and aperiodic activity, and find that IEM performance improves for aperiodic-adjusted alpha compared to total alpha power that blends the two signals. We also discover a novel role for aperiodic activity, where IEM performance trained on aperiodic activity is highest during stimulus presentation, but not during the WM maintenance period. Our results emphasize the importance of controlling for aperiodic activity when studying neural oscillations while uncovering a novel functional role for aperiodic activity in the encoding of visual WM information. Significance statementWorking memory is a crucial component of cognition, yet its neural mechanisms are not fully understood. Research shows that alpha activity - presumed to reflect neural oscillations - tracks the location of items we hold in memory. However, these analyses assume that all alpha power is oscillatory, even though oscillations are mixed with non-oscillatory, aperiodic activity that may be physiologically and functionally distinct. Here, we use a novel analytical approach for separating alpha oscillations and aperiodic activity dynamically across time. Our results reveal distinct roles for each in human visual working memory: aperiodic activity encodes the spatial location of information whereas alpha oscillations maintain the location of that information.