Spectral-power associations reflect amplitude modulation and within-frequency interactions on the sub-second timescale and cross-frequency interactions on the seconds timescale.

Melisa Menceloglu,Satoru Suzuki,Marcia Grabowecky,Vladyslav Vyazovskiy

doi:10.1371/journal.pone.0228365

Abstract

We investigated the global structure of intrinsic cross-frequency dynamics by systematically examining power-based temporal associations among a broad range of oscillation frequencies both within and across EEG-based current sources (sites). We focused on power-based associations that could reveal unique timescale dependence independently of interacting frequencies. Large spectral-power fluctuations across all sites occurred at two characteristic timescales, sub-second and seconds, yielding distinct patterns of cross-frequency associations. On the fast sub-second timescale, within-site (local) associations were consistently between pairs of β-γ frequencies differing by a constant Δf (particularly Δf ~ 10 Hz at posterior sites and Δf ~ 16 Hz at lateral sites) suggesting that higher-frequency oscillations are organized into Δf amplitude-modulated packets, whereas cross-site (long-distance) associations were all within-frequency (particularly in the >30 Hz and 6-12 Hz ranges, suggestive of feedforward and feedback interactions). On the slower seconds timescale, within-site (local) associations were characterized by a broad range of frequencies selectively associated with ~10 Hz at posterior sites and associations among higher (>20 Hz) frequencies at lateral sites, whereas cross-site (long-distance) associations were characterized by a broad range of frequencies at posterior sites selectively associated with ~10 Hz at other sites, associations among higher (>20 Hz) frequencies among lateral and anterior sites, and prevalent associations at ~10 Hz. Regardless of timescale, within-site (local) cross-frequency associations were weak at anterior sites indicative of frequency-specific operations. Overall, these results suggest that the fast sub-second-timescale coordination of spectral power is limited to local amplitude modulation and insulated within-frequency long-distance interactions (likely feedforward and feedback interactions), while characteristic patterns of cross-frequency interactions emerge on the slower seconds timescale. The results also suggest that the occipital α oscillations play a role in organizing higher-frequency oscillations into ~10 Hz amplitude-modulated packets to communicate with other regions. Functional implications of these timescale-dependent cross-frequency associations await future investigations.

Highlights

Because oscillatory dynamics are prevalent in the brain (e.g., [1]), many EEG, MEG, and Electrocorticography (ECoG) studies have examined the roles of oscillatory neural activity in perception (e.g., [2,3,4,5]), attention (e.g., [6,7,8,9]), memory (e.g., [10]), cognition (e.g., [11,12,13,14]), and the general control of neural communications (e.g., [15])
Regardless of timescale, within-site cross-frequency associations were weak at anterior sites indicative of frequency-specific operations. These results suggest that the fast sub-second-timescale coordination of spectral power is limited to local amplitude modulation and insulated within-frequency long-distance interactions, while characteristic patterns of cross-frequency interactions emerge on the slower seconds timescale
Some studies examined the dynamics of oscillatory activity while people rested with their eyes closed to identify intrinsic spatial networks of oscillatory activity (e.g., [16,17,18,19]) that may correlate with individual differences (e.g., [20]) or neural dysfunctions (e.g., [21,22,23])

Summary

Introduction

Because oscillatory dynamics are prevalent in the brain (e.g., [1]), many EEG, MEG, and Electrocorticography (ECoG) studies have examined the roles of oscillatory neural activity in perception (e.g., [2,3,4,5]), attention (e.g., [6,7,8,9]), memory (e.g., [10]), cognition (e.g., [11,12,13,14]), and the general control of neural communications (e.g., [15]). The goal of the current study was complementary in that instead of identifying spatial networks based on associations within specific frequency bands, we examined the global distribution of cross-frequency associations, focusing on both local characteristics reflected in crossfrequency associations within individual EEG-derived current sources (which we call sites here) and long-distance characteristics reflected in cross-frequency associations between sites. We observed that spectral power universally (across oscillation frequencies and sites) fluctuated on two distinct timescales, sub-second and seconds. Because these fast and slow fluctuations are mathematically orthogonal (see below), distinct cross-frequency mechanisms may operate on these timescales, potentially yielding timescale-dependent patterns of cross-frequency associations at local and long-distance levels. Analyses of spectral-power associations (though less temporally precise than analyses of phase coupling) provide additional advantages for characterizing the overarching structure of cross-frequency interactions

Objectives

Methods

Results