- Open Access
Unraveling network dynamics via Riemannian filtering of network interactions
Phys. Rev. Research 8, 033277 – Published 4 September, 2026
DOI: https://doi.org/10.1103/xzdr-sh34
Abstract
Functional connectivity (FC) is fundamentally nonstationary, undergoing continuous reconfigurations that track shifting behavioral and cognitive states. Despite the importance of these transitions, existing analytical frameworks struggle to reconcile the high-dimensional nature of these reconfigurations with the need for structured trajectories and mechanistic interpretability. Specifically, identifying the precise network components responsible for driving these dynamics remains a significant challenge. To bridge this gap, we introduce RONI (Riemannian filtering of network interactions), a geometry-aware, unsupervised framework that treats time-varying FC as a signal evolving on the manifold of symmetric positive semidefinite (SPSD) matrices. By defining intrinsic filtering operators along the SPSD geodesics, RONI produces a multiresolution decomposition of FC dynamics directly on the manifold. This representation allows for the isolation of “dynamic drivers”—specific network elements that dominate coherent connectivity modes across distinct temporal scales. We demonstrate the versatility of RONI by applying it to a diverse array of large-scale neural recordings, including hippocampal electrophysiology data, cortex-wide and dendritic calcium imaging, and human electroencephalography. Across these varied modalities and spatiotemporal scales, RONI identifies biologically meaningful subnetworks that shape the geometry of the connectivity trajectory, providing a unified, interpretable, and quantitative framework for studying the evolution of distributed neural interactions.
Physics Subject Headings (PhySH)
Article Text
References (52)
- M. Fu, X. Yu, J. Lu, and Y. Zuo, Repetitive motor learning induces coordinated formation of clustered dendritic spines in vivo, Nature (London) 483, 92 (2012).
- J. Cichon and W.-B. Gan, Branch-specific dendritic spikes cause persistent synaptic plasticity, Nature (London) 520, 180 (2015).
- A. J. Peters, J. Lee, N. G. Hedrick, K. O’Neil, and T. Komiyama, Reorganization of corticospinal output during motor learning, Nat. Neurosci. 20, 1133 (2017).
- M. Kumar, G. Handy, S. Kouvaros, Y. Zhao, L. L. Brinson, E. Wei, B. Bizup, B. Doiron, and T. Tzounopoulos, Cell-type-specific plasticity of inhibitory interneurons in the rehabilitation of auditory cortex after peripheral damage, Nat. Commun. 14, 4170 (2023).
- H. Safaai, A. Y. Wang, S. Kira, S. B. Malerba, S. Panzeri, and C. D. Harvey, Specialized structure of neural population codes in parietal cortex outputs, Nat. Neurosci. 28, 2550 (2025).
- Y.-L. Shi, R. Zeraati, A. Levina, and T. A. Engel, Spatial and temporal correlations in neural networks with structured connectivity, Phys. Rev. Res. 5, 013005 (2023).
- Y.-L. Shi, N. A. Steinmetz, T. Moore, K. Boahen, and T. A. Engel, Cortical state dynamics and selective attention define the spatial pattern of correlated variability in neocortex, Nat. Commun. 13, 44 (2022).
- R. Jiang, N. Zuo, J. M. Ford, S. Qi, D. Zhi, C. Zhuo, Y. Xu, Z. Fu, J. Bustillo, J. A. Turner, et al., Task-induced brain connectivity promotes the detection of individual differences in brain-behavior relationships, NeuroImage 207, 116370 (2020).
- L. Varga, V. V. Moca, B. Molnár, L. Perez-Cervera, M. K. Selim, A. Díaz-Parra, D. Moratal, B. Péntek, W. H. Sommer, R. C. Mureşan, S. Canals, and M. Ercsey-Ravasz, Brain dynamics supported by a hierarchy of complex correlation patterns defining a robust functional architecture, Cell Syst. 15, 770 (2024).
- O. Hazon, V. H. Minces, D. P. Tomàs, S. Ganguli, M. J. Schnitzer, and P. E. Jercog, Noise correlations in neural ensemble activity limit the accuracy of hippocampal spatial representations, Nat. Commun. 13, 4276 (2022).
- L. Kunz, B. P. Staresina, P. C. Reinacher, A. Brandt, T. A. Guth, A. Schulze-Bonhage, and J. Jacobs, Ripple-locked coactivity of stimulus-specific neurons and human associative memory, Nat. Neurosci. 27, 587 (2024).
- S. Lohani, A. H. Moberly, H. Benisty, B. Landa, M. Jing, Y. Li, M. J. Higley, and J. A. Cardin, Spatiotemporally heterogeneous coordination of cholinergic and neocortical activity, Nat. Neurosci. 25, 1706 (2022).
- A. Gilad and F. Helmchen, Spatiotemporal refinement of signal flow through association cortex during learning, Nat. Commun. 11, 1744 (2020).
- K. Jiang, Y. Yi, L. Li, H. Li, H. Shen, F. Zhao, Y. Xu, and A. Zheng, Functional network connectivity changes in children with attention-deficit hyperactivity disorder: A resting-state fMRI study, Int. J. Dev. Neurosci. 78, 1 (2019).
- R. Wang, M. Liu, X. Cheng, Y. Wu, A. Hildebrandt, and C. Zhou, Segregation, integration, and balance of large-scale resting brain networks configure different cognitive abilities, Proc. Natl. Acad. Sci. USA 118, e2022288118 (2021).
- W. Chang, J. Liu, L. Nie, X. Pang, Z. Lv, and J. Zheng, The degree centrality and functional connectivity in patients with temporal lobe epilepsy presenting as ictal panic: A resting state fMRI study, Front. Neurol. 13, 822253 (2022).
- L. Song, M. Kolar, and E. Xing, Time-varying dynamic Bayesian networks, in Advances in Neural Information Processing Systems, edited by Y. Bengio, D. Schuurmans, J. Lafferty, C. Williams, and A. Culotta (Curran Associates, Inc., Red Hook, NY, 2009), Vol. 22.
- R. F. Betzel, K. C. Wood, C. Angeloni, M. Neimark Geffen, and D. S. Bassett, Stability of spontaneous, correlated activity in mouse auditory cortex, PLoS Comput. Biol. 15, e1007360 (2019).
- T. F. Varley and O. Sporns, Network analysis of time series: Novel approaches to network neuroscience, Front. Neurosci. 15, 787068 (2022).
- J. Faskowitz, F. Z. Esfahlani, Y. Jo, O. Sporns, and R. F. Betzel, Edge‐centric functional network representations of human cerebral cortex reveal overlapping system‐level architecture, Nat. Neurosci. 23, 1644 (2020).
- O. Sporns, J. Faskowitz, A. S. Teixeira, S. A. Cutts, and R. F. Betzel, Dynamic expression of brain functional systems disclosed by fine-scale analysis of edge time series, Network Neurosci. 5, 405 (2021).
- F. Z. Esfahlani, L. Byrge, J. Tanner, O. Sporns, D. P. Kennedy, and R. F. Betzel, Edge‐centric analysis of time‐varying functional brain networks with applications in autism spectrum disorder, NeuroImage 263, 119591 (2022).
- T. Azevedo, A. Campbell, R. Romero-Garcia, L. Passamonti, R. A. Bethlehem, P. Liò, and N. Toschi, A deep graph neural network architecture for modelling spatio-temporal dynamics in resting-state functional MRI data, Med. Image Anal. 79, 102471 (2022).
- I. Ricchi, A. Tarun, H. P. Maretic, P. Frossard, and D. Van De Ville, Dynamics of functional network organization through graph mixture learning, NeuroImage 252, 119037 (2022).
- L. Novelli and A. Razi, A mathematical perspective on edge‐centric brain functional connectivity, Nat. Commun. 13, 2693 (2022).
- M. G. Preti, T. A. Bolton, and D. Van De Ville, The dynamic functional connectome: State-of-the-art and perspectives, NeuroImage 160, 41 (2017).
- F. Z. Esfahlani, Y. Jo, J. Faskowitz, L. Byrge, D. P. Kennedy, O. Sporns, and R. F. Betzel, High-amplitude cofluctuations in cortical activity drive functional connectivity, Proc. Natl. Acad. Sci. USA 117, 28393 (2020).
- Y. E. Pollak, R. Sachdev, M. Larkum, and A. Gilad, Cortex-wide laminar dynamics diverge during learning, bioRxiv (2025), https://doi.org/10.1101/2025.07.15.664840.
- H. Benisty, D. Barson, A. H. Moberly, S. Lohani, L. Tang, R. R. Coifman, M. C. Crair, G. Mishne, J. A. Cardin, and M. J. Higley, Rapid fluctuations in functional connectivity of cortical networks encode spontaneous behavior, Nat. Neurosci. 27, 148 (2024).
- A. Ghanayim, H. Benisty, A. Cohen Rimon, S. Schwartz, S. Dabdoob, S. Lifshitz, R. Talmon, and J. Schiller, VTA projections to M1 are essential for reorganization of layer 2–3 network dynamics underlying motor learning, Nat. Commun. 16, 200 (2025).
- Z. Dai, Z. Zhang, and A. Srivastava, Analyzing dynamical brain functional connectivity as trajectories on space of covariance matrices, IEEE Trans. Med. Imaging 38, 2196 (2019).
- Y.-T. Pan, J.-L. Chou, and C.-S. Wei, MATT: A manifold attention network for EEG decoding, Adv. Neural Inf. Process. Syst. 35, 31116 (2022).
- R. Kobler, J.-i. Hirayama, Q. Zhao, and M. Kawanabe, SPD domain-specific batch normalization to crack interpretable unsupervised domain adaptation in EEG, Adv. Neural Inf. Process. Syst. 35, 6219 (2022).
- X. S. Nguyen, S. Yang, and A. Histace, Neural networks on symmetric spaces of noncompact type, in The 13th International Conference on Learning Representations (OpenReview.net, 2025).
- M. Wang, Y. Wang, and Y. Yang, Dynamic and low-dimensional modeling of brain functional connectivity on Riemannian manifolds, NeuroImage 314, 121243 (2025).
- T. Dan, Z. Huang, H. Cai, P. J. Laurienti, and G. Wu, Learning brain dynamics of evolving manifold functional MRI data using geometric-attention neural network, IEEE Trans. Med. Imaging 41, 2752 (2022).
- T. Dan, J. Ding, and G. Wu, Geodynamics: A geometric state-space neural network for understanding brain dynamics on Riemannian manifolds, in NeurIPS 2025 Conference (Curran Associates, Inc., Red Hook, NY, 2025).
- E. Wong, J. S. Anderson, B. A. Zielinski, and P. T. Fletcher, Riemannian regression and classification models of brain networks applied to autism, in Connectomics in Neuroimaging: 2nd International Workshop (CNI) @ MICCAI (Springer International Publishing, Cham, Switzerland, 2018), pp. 78–87.
- K. You and H.-J. Park, Re-visiting Riemannian geometry of symmetric positive definite matrices for the analysis of functional connectivity, NeuroImage 225, 117464 (2021).
- C. L. Naranjo, F. A. Razzaq, M. Li, Y. Wang, J. F. Bosch‐Bayard, M. A. Lindquist, A. G. Mitjans, R. Garcia, A. G. Rabinowitz, S. G. Anderson, G. A. Chiarenza, A. Calzada‐Reyes, T. Virues‐Alba, J. R. Galler, L. Minati, M. L. B. Vega, and P. A. Valdes‐Sosa, EEG functional connectivity as a Riemannian mediator: An application to malnutrition and cognition, Hum. Brain Mapp. 45, e26698 (2024).
- G. Simeon, G. Piella, O. Camara, and D. Pareto, Riemannian geometry of functional connectivity matrices for multi-site attention-deficit/hyperactivity disorder data harmonization, Front. Neuroinf. 16, 769274 (2022).
- T. Shnitzer, H.-T. Wu, and R. Talmon, Spatiotemporal analysis using Riemannian composition of diffusion operators, Appl. Comput. Harmon. Anal. 68, 101583 (2024).
- M. Venkatesh, J. Jaja, and L. Pessoa, Comparing functional connectivity matrices: A geometry-aware approach applied to participant identification, NeuroImage 207, 116398 (2020).
- R. R. Coifman and S. Lafon, Diffusion maps, Appl. Comput. Harmon. Anal. 21, 5 (2006).
- S. Bonnabel and R. Sepulchre, Riemannian metric and geometric mean for positive semidefinite matrices of fixed rank, SIAM J. Matrix Anal. Appl. 31, 1055 (2010).
- S. Musall, X. R. Sun, H. Mohan, X. An, S. Gluf, S.-J. Li, R. Drewes, E. Cravo, I. Lenzi, C. Yin, et al., Pyramidal cell types drive functionally distinct cortical activity patterns during decision-making, Nat. Neurosci. 26, 495 (2023).
- C. Brunner, R. Leeb, G. Müller-Putz, A. Schlögl, and G. Pfurtscheller, BCI competition 2008—Graz data set A, J. Neural Eng. 5, 1 (2008).
- https://github.com/BenistyLab/RONI.
- L. N. Trefethen and M. Embree, Spectra and Pseudospectra: The Behavior of Nonnormal Matrices and Operators (Princeton University Press, 2020).
- M. Pachitariu, S. Sridhar, J. Pennington, and C. Stringer, Spike sorting with Kilosort4, Nat. Methods 21, 914 (2024).
- J. M. J. Fabre, E. H. van Beest, A. J. Peters, M. Carandini, and K. D. Harris, Bombcell: Automated curation and cell classification of spike-sorted electrophysiology, data (Version 1.0.0) [Computer software], Zenodo, 2023, https://doi.org/10.5281/zenodo.8172822.
- J. Couto, S. Musall, X. R. Sun, A. Khanal, S. Gluf, S. Saxena, I. Kinsella, T. Abe, J. P. Cunningham, L. Paninski, et al., Chronic, cortex-wide imaging of specific cell populations during behavior, Nat. Protoc. 16, 3241 (2021).