Dissociating Contributions of Theta and Alpha Oscillations from Aperiodic Neural Activity in Human Visual Working Memory.

UNLABELLED

While visual working memory (WM) is strongly associated with reductions in occipitoparietal 8-12 Hz alpha power, the role of 4-7 Hz frontal midline theta power is less clear, with both increases and decreases widely reported. Here, we test the hypothesis that this theta paradox can be explained by non-oscillatory, aperiodic neural activity dynamics. Because traditional time-frequency analyses of electroencephalopgraphy (EEG) data conflate oscillations and aperiodic activity, event-related changes in aperiodic activity can manifest as task-related changes in apparent oscillations, even when none are present. Reanalyzing EEG data from two visual WM experiments (n = 74), and leveraging spectral parameterization, we found systematic changes in aperiodic activity with WM load, and we replicated classic alpha, but not theta, oscillatory effects after controlling for aperiodic changes. Aperiodic activity decreased during WM retention, and further flattened over the occipitoparietal cortex with an increase in WM load. After controlling for these dynamics, aperiodic-adjusted alpha power decreased with increasing WM load. In contrast, aperiodic-adjusted theta power increased during WM retention, but because aperiodic activity reduces more, it falsely appears as though theta "oscillatory" power (e.g., bandpower) is reduced. Furthermore, only a minority of participants (31/74) had a detectable degree of theta oscillations. These results offer a potential resolution to the theta paradox where studies show contrasting power changes. We identify novel aperiodic dynamics during human visual WM that mask the potential role that neural oscillations play in cognition and behavior.

SIGNIFICANCE STATEMENT

Working Memory (WM) is our ability to hold information in mind without it being present in our external environment. Years of research focused on oscillatory brain dynamics to discover the mechanisms of WM. Here, we specifically look at oscillatory and non-oscillatory, aperiodic activity as measured with scalp EEG to test their significance in supporting WM. We challenge earlier findings regarding theta oscillations with our analysis approach, while replicating alpha oscillation findings. Furthermore, aperiodic activity is found to be involved in WM, over frontal regions in a task-general manner, and over anterior regions this activity is reduced with an increase the number of items that are remembered. Thus, we have identified novel aperiodic dynamics during human visual WM.