Robust fMRI time-varying functional connectivity analysis using multivariate swarm decomposition

Time-varying functional connectivity (TVFC) measured with functional MRI (fMRI) captures dynamic changes in statistical dependencies among regional time series, which can be studied with instantaneous phase synchronization analyses. Phase extraction requires narrow-banded resting-state fMRI (rs-fMRI) data typically extracted with conventional band-pass filtering or advanced mode decomposition techniques. However, filtering methods often struggle to eliminate noise effectively, require prior knowledge of cutoff frequencies, and fail to account for non-stationarity in the data. Likewise, existing mode decomposition techniques strongly depend on input parameters and are less reliable for multivariate analyses. Here, we introduce multivariate swarm decomposition (MSwD), a bio-inspired signal decomposition technique that combines the iterative nature of empirical methods with a robust mathematical foundation. Using synthetic signals and real rs-fMRI data from the Human Connectome Project and the Autism Brain Imaging Data Exchange I, we showed that MSwD-based PS (MSwD-PS) outperforms four state-of-the-art decomposition techniques in several key areas: (1) being more robust to input parameters and better at detecting true synchronizations, showing a 3%–65% lower normalized root mean square error in simulated data and being 15.8-73.1% less prone to identifying short biologically implausible transitions between brain states, and (2) showing a reduced likelihood of false positives, being less affected by spurious synchronizations. Likewise, MSwD-informed functional connectivity analysis improved subject fingerprinting and autism spectrum disorder classification using graph neural networks. Overall, MSwD-PS can reduce the risk of false positives in TVFC, which could be extremely useful for processing rs-fMRI data with unknown ground truth in diverse clinical populations. • This work introduces a novel Multivariate Swarm Decomposition for phase synchronization (MSwD-PS). • MSwD-PS can assess time-varying functional connectivity from fMRI data. • MSwD-PS can identify biologically plausible transitions between brain states. • MSwD-PS is robust to input parameters and has a low risk for false positive synchronizations.