Intrinsic Connectivity Networks, Alpha Oscillations, and Tonic Alertness: A Simultaneous Electroencephalography/Functional Magnetic Resonance Imaging Study

TLDR

Spontaneous fluctuations in intrinsic functional connectivity networks influence perceptual performance, with higher prestimulus activity in a cingulo‑insular‑thalamic network facilitating perception. The study tests whether the cingulo‑insular‑thalamic network underpins tonic alertness and proposes it maintains alertness through generalized cortical alpha oscillations. Simultaneous fMRI and EEG were recorded without a task to examine whether spontaneous ICN activity correlates positively with tonic alertness signatures measured as upper‑alpha band global field power. Activity in the cingulo‑insular‑thalamic network positively correlated with upper‑alpha GFP, while dorsal attention network activity negatively correlated with alpha power, indicating distinct roles for alertness and selective attention.

Abstract

Trial-by-trial variability in perceptual performance on identical stimuli has been related to spontaneous fluctuations in ongoing activity of intrinsic functional connectivity networks (ICNs). In a paradigm requiring sustained vigilance for instance, we previously observed that higher prestimulus activity in a cingulo-insular-thalamic network facilitated subsequent perception. Here, we test our proposed interpretation that this network underpins maintenance of tonic alertness. We used simultaneous acquisition of functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) in the absence of any paradigm to test an ensuing hypothesis, namely that spontaneous fluctuations in this ICN′s activity (as measured by fMRI) should show a positive correlation with the electrical signatures of tonic alertness (as recorded by concurrent EEG). We found in human subjects (19 male, 7 female) that activity in a network comprising dorsal anterior cingulate cortex, anterior insula, anterior prefrontal cortex and thalamus is positively correlated with global field power (GFP) of upper alpha band (10–12 Hz) oscillations, the most consistent electrical index of tonic alertness. Conversely, and in line with earlier findings, alpha band power was negatively correlated with activity in another ICN, the so-called dorsal attention network which is most prominently involved in selective spatial attention. We propose that the cingulo-insular-thalamic network serves maintaining tonic alertness through generalized expression of cortical alpha oscillations. Attention is mediated by activity in other systems, e.g., the dorsal attention network for space, selectively disrupts alertness-related suppression and hence manifests as local attenuation of alpha activity.