Connectome spectrum electromagnetic tomography: A method to reconstruct electrical brain source networks at high-spatial resolution.

Connectome spectrum electromagnetic tomography (CSET) combines diffusion MRI-derived structural connectivity data with well-established graph signal processing tools to solve the M/EEG inverse problem. Using simulated EEG signals from fMRI responses, and two EEG datasets on visual-evoked potentials, we provide evidence supporting that (i) CSET captures realistic neurophysiological patterns with better accuracy than state-of-the-art methods, (ii) CSET can reconstruct brain responses more accurately and with more robustness to intrinsic noise in the EEG signal. These results demonstrate that CSET offers high spatio-temporal accuracy, enabling neuroscientists to extend their research beyond the current limitations of low sampling frequency in functional MRI and the poor spatial resolution of M/EEG.

The coupling between the spatial and temporal scales of neural processes revealed by a joint time-vertex connectome spectral analysis.

Brain oscillations are produced by the coordinated activity of large groups of neurons and different rhythms are thought to reflect different modes of information processing. These modes, in turn, are known to occur at different spatial scales. Nevertheless, how these rhythms support different spatial modes of information processing at the brain scale is not yet fully understood. Here we use "Joint Time-Vertex Spectral Analysis" to characterize the joint spectral content of brain activity both in time (temporal frequencies) and in space over the connectivity graph (spatial connectome harmonics). This method allows us to characterize the relationship between spatially localized or distributed neural processes on one side and their respective temporal frequency bands in source-reconstructed M/EEG signals. We explore this approach on two different datasets, an auditory steady-state response (ASSR) and a visual grating task. Our results suggest that different information processing mechanisms are carried out at different frequency bands: while spatially distributed activity (which may also be interpreted as integration) specifically occurs at low temporal frequencies (alpha and theta) and low graph spatial frequencies, localized electrical activity (i.e., segregation) is observed at high temporal frequencies (high and low gamma) over restricted high spatial graph frequencies. Crucially, the estimated contribution of the distributed and localized neural activity predicts performance in a behavioral task, demonstrating the neurophysiological relevance of the joint time-vertex spectral representation.

Structure supports function: Informing directed and dynamic functional connectivity with anatomical priors.

The dynamic repertoire of functional brain networks is constrained by the underlying topology of structural connections. Despite this intrinsic relationship between structural connectivity (SC) and functional connectivity (FC), integrative and multimodal approaches to combine the two remain limited. Here, we propose a new adaptive filter for estimating dynamic and directed FC using structural connectivity information as priors. We tested the filter in rat epicranial recordings and human event-related EEG data, using SC priors from a meta-analysis of tracer studies and diffusion tensor imaging metrics, respectively. We show that, particularly under conditions of low signal-to-noise ratio, SC priors can help to refine estimates of directed FC, promoting sparse functional networks that combine information from structure and function. In addition, the proposed filter provides intrinsic protection against SC-related false negatives, as well as robustness against false positives, representing a valuable new tool for multimodal imaging in the context of dynamic and directed FC analysis.

Source imaging of high-density visual evoked potentials with multi-scale brain parcellations and connectomes.

We describe the multimodal neuroimaging dataset VEPCON (OpenNeuro Dataset ds003505). It includes raw data and derivatives of high-density EEG, structural MRI, diffusion weighted images (DWI) and single-trial behavior (accuracy, reaction time). Visual evoked potentials (VEPs) were recorded while participants (n = 20) discriminated briefly presented faces from scrambled faces, or coherently moving stimuli from incoherent ones. EEG and MRI were recorded separately from the same participants. The dataset contains raw EEG and behavioral data, pre-processed EEG of single trials in each condition, structural MRIs, individual brain parcellations at 5 spatial resolutions (83 to 1015 regions), and the corresponding structural connectomes computed from fiber count, fiber density, average fractional anisotropy and mean diffusivity maps. For source imaging, VEPCON provides EEG inverse solutions based on individual anatomy, with Python and Matlab scripts to derive activity time-series in each brain region, for each parcellation level. The BIDS-compatible dataset can contribute to multimodal methods development, studying structure-function relations, and to unimodal optimization of source imaging and graph analyses, among many other possibilities.

The connectome spectrum as a canonical basis for a sparse representation of fast brain activity.

The functional organization of neural processes is constrained by the brain's intrinsic structural connectivity, i.e., the connectome. Here, we explore how structural connectivity can improve the representation of brain activity signals and their dynamics. Using a multi-modal imaging dataset (electroencephalography, structural MRI, and diffusion MRI), we represent electrical brain activity at the cortical surface as a time-varying composition of harmonic modes of structural connectivity. These harmonic modes are known as connectome harmonics. Here we describe brain activity signal as a time-varying combination of connectome harmonics. We term this description as the connectome spectrum of the signal. We found that: first, the brain activity signal is represented more compactly by the connectome spectrum than by the traditional area-based representation; second, the connectome spectrum characterizes fast brain dynamics in terms of signal broadcasting profile, revealing different temporal regimes of integration and segregation that are consistent across participants. And last, the connectome spectrum characterizes fast brain dynamics with fewer degrees of freedom than area-based signal representations. Specifically, we show that a smaller number of dimensions capture the differences between low-level and high-level visual processing in the connectome spectrum. Also, we demonstrate that connectome harmonics capture more sensitively the topological properties of brain activity. In summary, this work provides statistical, functional, and topological evidence indicating that the description of brain activity in terms of structural connectivity fosters a more comprehensive understanding of large-scale dynamic neural functioning.

Decoding brain states on the intrinsic manifold of human brain dynamics across wakefulness and sleep.

Current state-of-the-art functional magnetic resonance imaging (fMRI) offers remarkable imaging quality and resolution, yet, the intrinsic dimensionality of brain dynamics in different states (wakefulness, light and deep sleep) remains unknown. Here we present a method to reveal the low dimensional intrinsic manifold underlying human brain dynamics, which is invariant of the high dimensional spatio-temporal representation of the neuroimaging technology. By applying this intrinsic manifold framework to fMRI data acquired in wakefulness and sleep, we reveal the nonlinear differences between wakefulness and three different sleep stages, and successfully decode these different brain states with a mean accuracy across participants of 96%. Remarkably, a further group analysis shows that the intrinsic manifolds of all participants share a common topology. Overall, our results reveal the intrinsic manifold underlying the spatiotemporal dynamics of brain activity and demonstrate how this manifold enables the decoding of different brain states such as wakefulness and various sleep stages.

Connectome spectral analysis to track EEG task dynamics on a subsecond scale.

We present an approach for tracking fast spatiotemporal cortical dynamics in which we combine white matter connectivity data with source-projected electroencephalographic (EEG) data. We employ the mathematical framework of graph signal processing in order to derive the Fourier modes of the brain structural connectivity graph, or "network harmonics". These network harmonics are naturally ordered by smoothness. Smoothness in this context can be understood as the amount of variation along the cortex, leading to a multi-scale representation of brain connectivity. We demonstrate that network harmonics provide a sparse representation of the EEG signal, where, at certain times, the smoothest 15 network harmonics capture 90% of the signal power. This suggests that network harmonics are functionally meaningful, which we demonstrate by using them as a basis for the functional EEG data recorded from a face detection task. There, only 13 network harmonics are sufficient to track the large-scale cortical activity during the processing of the stimuli with a 50 â€‹ms resolution, reproducing well-known activity in the fusiform face area as well as revealing co-activation patterns in somatosensory/motor and frontal cortices that an unconstrained ROI-by-ROI analysis fails to capture. The proposed approach is simple and fast, provides a means of integration of multimodal datasets, and is tied to a theoretical framework in mathematics and physics. Thus, network harmonics point towards promising research directions both theoretically - for example in exploring the relationship between structure and function in the brain - and practically - for example for network tracking in different tasks and groups of individuals, such as patients.