The frequency of alpha oscillations: Task-dependent modulation and its functional significance

Abstract

Power (amplitude) and frequency are two important characteristics of EEG alpha oscillations (8-12 Hz). There is an extensive literature showing that alpha power can be modulated in a goal-oriented manner to either enhance or suppress sensory information processing. Only a few studies to date have examined the task-dependent modulation of alpha frequency. Instead, alpha frequency is often viewed as a trait variable, and used to characterize individual differences in cognitive functioning. We performed two experiments to examine the task-dependent modulation of alpha frequency and its functional significance. In the first experiment, high-density EEG was recorded from 21 participants performing a Sternberg working memory task. The results showed that: (1) during memory encoding, alpha frequency decreased with increasing memory load, whereas during memory retention and retrieval, alpha frequency increased with increasing memory load, (2) higher alpha frequency prior to the onset of probe was associated with longer reaction time, and (3) higher alpha frequency prior to the onset of cue or probe was associated with weaker early cue-evoked or probe-evoked neural responses. In the second experiment, simultaneous EEG-fMRI was recorded from 59 participants during resting state. An EEG-informed fMRI analysis revealed that the spontaneous fluctuations of alpha frequency, but not alpha power, were inversely associated with BOLD activity in the visual cortex. Taken together, these findings suggest that alpha frequency is task-dependent, may serve as an indicator of cortical excitability, and along with alpha power, provides more comprehensive indexing of sensory gating.

Keywords: Alpha frequency; Alpha modulation; Alpha oscillation; Alpha power; Alpha source; Simultaneous EEG-fMRI; Working memory.

Figure 1:

Paradigm and behavioral results. (A) Schematic illustration of the working memory task. Depicted is a trial where the memory load is 5 and a yes answer is the correct response. (B) Definition of time periods of analysis for pre-cue, encoding, retention, pre-probe, and retrieval. (C) Reaction time. (D) Accuracy. (The p-values in C and D were obtained from a mixed-effects linear model fit on the behavioral data.)

Figure 2:

Memory load modulation of alpha power and alpha frequency during different stages of working memory processing. A-D: encoding. E-H: retention. I-L retrieval. (The p-values in B, C, F, G, J and K are obtained from the mixed-effects linear model fit on the alpha power and alpha frequency.)

Figure 3:

Functional significance of alpha frequency modulation. (1) Association of alpha frequency during retention and retrieval with RT (A-D): (A) Power spectra of fast RT and slow RT trials during retention time period and (B) alpha frequency difference between fast RT and slow RT trials during retention time period; (C) power spectra of fast RT and slow RT trials during retrieval and (D) alpha frequency difference between fast RT and slow RT trials during retrieval. (2) Relation between alpha frequency and early stimulus-evoked responses (E-G): (E) and (F) Probe-evoked ERPs of low response trials and high response trials; (G) alpha frequency difference between high response trials and (G) low response trials during pre-cue, encoding, pre-probe and retrieval period. Note: For pre-cue and encoding, the cue-evoked responses were considered.

Figure 4:

Alpha variable fluctuations and BOLD activity. (A) Alpha frequency time series for a representative subject during resting state. (B) HRF-convolved alpha frequency time series and BOLD time series from a voxel in visual cortex (18, −79, −10) of a representative subject. (C) Regions of interest (ROIs) in the visual cortex. (D) Association between alpha power fluctuation and BOLD activity from different visual ROIs at the group level. (E) Association between alpha frequency fluctuation and BOLD activity from different visual ROIs at the group level. FDR-corrected p-values were given.

Figure 5:

Exploratory whole brain analysis. (A) Low-threshold maps of alpha frequency - BOLD coupling. (B) Low-threshold maps of alpha power - BOLD coupling. ACC – anterior cingulate cortex, FC - frontal cortex, mPFC - medial pre-frontal cortex, PC – parietal cortex, PCC - posterior cingulate cortex.