Oscillation-Based Connectivity Architecture Is Dominated by an Intrinsic Spatial Organization, Not Cognitive State or Frequency

Abstract

Functional connectivity of neural oscillations (oscillation-based FC) is thought to afford dynamic information exchange across task-relevant neural ensembles. Although oscillation-based FC is classically defined relative to a prestimulus baseline, giving rise to rapid, context-dependent changes in individual connections, studies of distributed spatial patterns show that oscillation-based FC is omnipresent, occurring even in the absence of explicit cognitive demands. Thus, the issue of whether oscillation-based FC is primarily shaped by cognitive state or is intrinsic in nature remains open. Accordingly, we sought to reconcile these observations by interrogating the ECoG recordings of 18 presurgical human patients (8 females) for state dependence of oscillation-based FC in five canonical frequency bands across an array of six task states. FC analysis of phase and amplitude coupling revealed a highly similar, largely state-invariant (i.e., intrinsic) spatial component across cognitive states. This spatial organization was shared across all frequency bands. Crucially, however, each band also exhibited temporally independent FC dynamics capable of supporting frequency-specific information exchange. In conclusion, the spatial organization of oscillation-based FC is largely stable over cognitive states (i.e., primarily intrinsic in nature) and shared across frequency bands. Together, our findings converge with previous observations of spatially invariant patterns of FC derived from extremely slow and aperiodic fluctuations in fMRI signals. Our observations indicate that "background" FC should be accounted for in conceptual frameworks of oscillation-based FC targeting task-related changes.

Connectomics of Human Electrophysiology

“…An EEG study in source-space showed that phase-coupling is spatially consistent when calculated over several minutes of different tasks (resting state, video viewing, and flashing gratings) with similar modular organization across frequency bands (Nentwich et al, 2020). Finally, a recent ECoG study contrasted various cognitive states including rest and short (1.5-2.5 s) pre-stimulus and post-stimulus epochs of different tasks (Mostame and Sadaghiani, 2021). Phase-and amplitude-coupling revealed a highly similar, largely state-invariant spatial component across cognitive states.…”

Genetic polymorphisms in COMT and BDNF influence synchronization dynamics of human neuronal oscillations

“…During rest, brain activity in sub-second time-scales is dominated by alpha oscillations [6], but involves frequency-specific inter-areal correlation structures throughout the 1-100 Hz range [9][10][11][12][13][14]. Importantly, the intrinsic spatial organization of spontaneous restingstate FCs observed both with MEG and functional magnetic resonance imaging (fMRI) is predictive of individual variability in task performance [12,[14][15][16], suggesting that such resting-state FC networks reflect underlying individual brain structural organization [17,18].…”

“…We hypothesized that modulations in oscillation dynamics would be obtained via inter-individual differences in the neuromodulation levels, which could result in differences in systems-level net E/I balance (or neural gain). In the brain criticality framework, the carriers of different variants of the COMT Val 158 Alternatively, COMT and especially BDNF could induce plastic changes in the structural connectivity networks (SC) [50,51] which in turn could lead to changes in FC [17]. To test these hypotheses, we measured resting-state brain dynamics with MEG and estimated local oscillation amplitudes, large-scale phase synchronization, and LRTCs from individually source-reconstructed MEG data.…”

“…Resting-state FC networks reflect individual trait-like behavior 23 that could arise from the underlying individual brain structural organization 24,25 and neuromodulation [26][27][28][29] . Amplitude envelopes of fast (> 1 Hz) oscillations are also characterized by slow (0.1-1 Hz) and infra-slow (0.01-0.1 Hz) fluctuations 12,30,31 .…”

“…Global α band synchronization was stronger for BDNF Val homozygotes than Met carriers in all functional subsystems except within the visual system.BDNF Val homozygotes also had stronger θ synchronization within DAN and stronger lefthemispheric β synchronization between various subsystems, particularly involving DAN and DMN. This robust modulation of synchronization dynamics by BDNF polymorphism could contribute to significant differences across individuals in behavior and cognition, which have been shown to be strongly influenced by spatial and spectral characteristics of oscillatory synchronization15,17,24 . However, large-scale synchronization was not influenced by COMT Val 158 Met polymorphism, although it has been shown that neuropharmacologically elevated levels of catecholamines are related to fMRI-based changes in functional connectivity 27 .…”