Time-varying changes in whole-brain connectivity patterns, or connectome state dynamics, hold significant implications for cognition. However, connectome dynamics at fast (>1 Hz) timescales highly relevant to cognition are poorly understood due to the dominance of inherently slow fMRI in connectome studies. Here, we investigated the behavioral significance of rapid electrophysiological connectome dynamics using source-localized EEG connectomes during resting state ( N = 926, 473 females). We focused on dynamic connectome features pertinent to individual differences, specifically those with established heritability: Fractional Occupancy (i.e., the overall duration spent in each recurrent connectome state) in beta and gamma bands and Transition Probability (i.e., the frequency of state switches) in theta, alpha, beta, and gamma bands. Canonical correlation analysis found a significant relationship between the heritable phenotypes of subsecond connectome dynamics and cognition. Specifically, principal components of Transition Probabilities in alpha (followed by theta and gamma bands) and a cognitive factor representing visuospatial processing (followed by verbal and auditory working memory) most notably contributed to the relationship. We conclude that rapid connectome state transitions shape individuals’ cognitive abilities and traits. Such subsecond connectome dynamics may inform about behavioral function and dysfunction and serve as endophenotypes for cognitive abilities. Author Summary This study investigates the behavioral significance of rapid electrophysiological connectome dynamics features with established heritability. The heritable phenotypes that describe the duration (Fractional Occupancy) and frequency of connectome state switches (Transition Probability) were obtained using hidden Markov model on source-localized EEG data at rest. Using the canonical correlation analysis approach, we found that connectome state transitions unfolding at multiple speeds (e.g., alpha, theta, and gamma) collectively contribute to shape cognitive abilities.

Time-varying changes in whole-brain connectivity patterns, or connectome state dynamics, are a prominent feature of brain activity with broad functional implications. While infraslow (<0.1 Hz) connectome dynamics have been extensively studied with fMRI, rapid dynamics highly relevant for cognition are poorly understood. Here, we asked whether rapid electrophysiological connectome dynamics constitute subject-specific brain traits and to what extent they are under genetic influence. Using source-localized EEG connectomes during resting state ( N = 928, 473 females), we quantified the heritability of multivariate (multistate) features describing temporal or spatial characteristics of connectome dynamics. States switched rapidly every ~60–500 ms. Temporal features were heritable, particularly Fractional Occupancy (in theta, alpha, beta, and gamma bands) and Transition Probability (in theta, alpha, and gamma bands), representing the duration spent in each state and the frequency of state switches, respectively. Genetic effects explained a substantial proportion of the phenotypic variance of these features: Fractional Occupancy in beta (44.3%) and gamma (39.8%) bands and Transition Probability in theta (38.4%), alpha (63.3%), beta (22.6%), and gamma (40%) bands. However, we found no evidence for the heritability of dynamic spatial features, specifically states’ Modularity and connectivity pattern. We conclude that genetic effects shape individuals’ connectome dynamics at rapid timescales, specifically states’ overall occurrence and sequencing. Author Summary In this study, we investigate the genetic influence on rapid electrophysiological connectome dynamics. Using hidden Markov model on source-localized EEG data at rest, we obtained measures describing temporal trajectories and time-varying spatial characteristics of connectome states. Applying two heritability assessment methods to these multivariate, time-varying connectome dynamics features, we discovered that the duration (Fractional Occupancy) and frequency of state switches (Transition Probability) were heritable, particularly in theta, alpha, beta, and gamma bands. However, no genetic influence was observed on spatial features.

Progress in scientific disciplines is accompanied by standardization of terminology. Network neuroscience, at the level of macroscale organization of the brain, is beginning to confront the challenges associated with developing a taxonomy of its fundamental explanatory constructs. The Workgroup for HArmonized Taxonomy of NETworks (WHATNET) was formed in 2020 as an Organization for Human Brain Mapping (OHBM)–endorsed best practices committee to provide recommendations on points of consensus, identify open questions, and highlight areas of ongoing debate in the service of moving the field toward standardized reporting of network neuroscience results. The committee conducted a survey to catalog current practices in large-scale brain network nomenclature. A few well-known network names (e.g., default mode network) dominated responses to the survey, and a number of illuminating points of disagreement emerged. We summarize survey results and provide initial considerations and recommendations from the workgroup. This perspective piece includes a selective review of challenges to this enterprise, including (1) network scale, resolution, and hierarchies; (2) interindividual variability of networks; (3) dynamics and nonstationarity of networks; (4) consideration of network affiliations of subcortical structures; and (5) consideration of multimodal information. We close with minimal reporting guidelines for the cognitive and network neuroscience communities to adopt.

Concurrent electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) bridge brain connectivity across timescales. During concurrent EEG-fMRI resting-state recordings, whole-brain functional connectivity (FC) strength is spatially correlated across modalities. However, cross-modal investigations have commonly remained correlational, and joint analysis of EEG-fMRI connectivity is largely unexplored. Here we investigated if there exist (spatially) independent FC networks linked between modalities. We applied the recently proposed hybrid connectivity independent component analysis (connICA) framework to two concurrent EEG-fMRI resting-state datasets (total 40 subjects). Two robust components were found across both datasets. The first component has a uniformly distributed EEG frequency fingerprint linked mainly to intrinsic connectivity networks (ICNs) in both modalities. Conversely, the second component is sensitive to different EEG frequencies and is primarily linked to intra-ICN connectivity in fMRI but to inter-ICN connectivity in EEG. The first hybrid component suggests that connectivity dynamics within well-known ICNs span timescales, from millisecond range in all canonical frequencies of FC EEG to second range of FC fMRI . Conversely, the second component additionally exposes linked but spatially divergent neuronal processing at the two timescales. This work reveals the existence of joint spatially independent components, suggesting that parts of resting-state connectivity are co-expressed in a linked manner across EEG and fMRI over individuals. Author Summary Functional connectivity is governed by a whole-brain organization measurable over multiple timescales by functional magnetic resonance imaging (fMRI) and electroencephalography (EEG). The relationship across the whole-brain organization captured at the different timescales of EEG and fMRI is largely unknown. Using concurrent EEG-fMRI, we identified spatially independent components consisting of brain connectivity patterns that co-occur in EEG and fMRI over subjects. We observed a component with similar connectivity organization across EEG and fMRI as well as a component with divergent connectivity. The former component governed all EEG frequencies while the latter was modulated by frequency. These findings show that part of functional connectivity organizes in a common spatial layout over several timescales, while a spatially independent part is modulated by frequency-specific information.

The discovery of a stable, whole-brain functional connectivity organization that is largely independent of external events has drastically extended our view of human brain function. However, this discovery has been primarily based on functional magnetic resonance imaging (fMRI). The role of this whole-brain organization in fast oscillation-based connectivity as measured, for example, by electroencephalography (EEG) and magnetoencephalography (MEG) is only beginning to emerge. Here, we review studies of intrinsic connectivity and its whole-brain organization in EEG, MEG, and intracranial electrophysiology with a particular focus on direct comparisons to connectome studies in fMRI. Synthesizing this literature, we conclude that irrespective of temporal scale over four orders of magnitude, intrinsic neurophysiological connectivity shows spatial similarity to the connectivity organization commonly observed in fMRI. A shared structural connectivity basis and cross-frequency coupling are possible mechanisms contributing to this similarity. Acknowledging that a stable whole-brain organization governs long-range coupling across all timescales of neural processing motivates researchers to take “baseline” intrinsic connectivity into account when investigating brain-behavior associations, and further encourages more widespread exploration of functional connectomics approaches beyond fMRI by using EEG and MEG modalities.

In cognitive neuroscience, focus is commonly placed on associating brain function with changes in objectively measured external stimuli or with actively generated cognitive processes. In everyday life, however, many forms of cognitive processes are initiated spontaneously, without an individual’s active effort and without explicit manipulation of behavioral state. Recently, there has been increased emphasis, especially in functional neuroimaging research, on spontaneous correlated activity among spatially segregated brain regions (intrinsic functional connectivity) and, more specifically, on intraindividual fluctuations of such correlated activity on various time scales (time-varying functional connectivity). In this Perspective, we propose that certain subtypes of spontaneous cognitive processes are detectable in time-varying functional connectivity measurements. We define these subtypes of spontaneous cognitive processes and review evidence of their representations in time-varying functional connectivity from studies of attentional fluctuations, memory reactivation, and effects of baseline states on subsequent perception. Moreover, we describe how these studies are critical to validating the use of neuroimaging tools (e.g., fMRI) for assessing ongoing brain network dynamics. We conclude that continued investigation of the behavioral relevance of time-varying functional connectivity will be beneficial both in the development of comprehensive neural models of cognition, and in informing on best practices for studying brain network dynamics.