Slower Ageing of Cross-Frequency Coupling Mechanisms Across Resting-State Networks Is Associated with Better Cognitive Performance in the Picture Priming Task
Source abstract
Abstract
The brain age gap (BAG), the divergence of an individual’s neurobiologically predicted brain age from their chronological age, is a key indicator of brain health. While BAG can be derived from diverse brain metrics, its interpretation often polarizes between early-life trait influences and current state-dependent factors like cognitive decline. Here, we propose an integrative framework that moves beyond single summary statistics by considering the full distribution of brain metrics across regions or time. We distinguish between a neural system’s “baseline” (typical values, e.g., mean) and its “capacity” (extreme values, e.g., maximum) within these distributions. To test this, we analyzed resting-state magnetoencephalography (MEG) from the Cam-CAN adult cohort, focusing on cross-frequency coupling (CFC) within functional MRI-defined networks. We derived network-specific CFC baseline (mean) and capacity (maximum) measures. Separate brain age prediction models were trained for each measure. The resulting BAGs (baseline-BAG and capacity-BAG) for each network were then correlated with cognitive performance on a picture priming task. Both baseline-BAG and capacity-BAG profiles showed associations with cognitive scores, with younger predicted brain age correlating with better performance. However, capacity-BAG exhibited more conclusive relationships, suggesting that metrics reflecting a neural system’s peak operational ability (capacity) may better capture an individual’s current cognitive state. These findings indicate that brain age models emphasizing neural capacity, rather than just baseline activity, could offer a more sensitive lens for understanding the state-dependent aspects of brain ageing.
Source: crossref · Quality: baseline
Research context
OpenAlex topics: Functional Brain Connectivity Studies · Neural dynamics and brain function · EEG and Brain-Computer Interfaces
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
Affiliations
Department of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, BC V5A 1S6, Canada
Royal Columbian Hospital, Fraser Health Authority, New Westminster, BC V3L 0A2, Canada
School of Public Health Sciences, University of Waterloo, Waterloo, ON N2L 3G1, Canada
School of Interactive Arts and Technology, Simon Fraser University, Surrey, BC V3T 0A3, Canada
Funding
Age Well
References (61)
Show source-provided references
1. A Perspective on Brain-Age Estimation and Its Clinical Promise10.1038/s43588-024-00659-8 ↗
2. Franke, K., and Gaser, C. (2019). Ten Years of BrainAGE as a Neuroimaging Biomarker of Brain Aging: What Insights Have We Gained?. Front. Neurol., 10.10.3389/fneur.2019.00789 ↗
3. Individual Variations in ‘Brain Age’ Relate to Early-Life Factors More than to Longitudinal Brain Change10.7554/eLife.69995 ↗
4. Brain Age Revisited: Investigating the State vs. Trait Hypotheses of EEG-Derived Brain-Age Dynamics with Deep Learning10.1162/imag_a_00210 ↗
5. Brain Age Gap in Early Illness Schizophrenia and the Clinical High-Risk Syndrome: Associations with Experiential Negative Symptoms and Conversion to Psychosis10.1093/schbul/sbae074 ↗
6. Deep Learning-Based Brain Age Prediction in Normal Aging and Dementia10.1038/s43587-022-00219-7 ↗
7. Dular, L., Špiclin, Ž., for the Alzheimer’s Disease Neuroimaging Initiative, and the Australian Imaging Biomarkers and Lifestyle Flagship Study of Ageing (2024). Analysis of Brain Age Gap across Subject Cohorts and Prediction Model Architectures. Biomedicines, 12.10.3390/biomedicines12092139 ↗
8. Jawinski, P., Markett, S., Drewelies, J., Düzel, S., Demuth, I., Steinhagen-Thiessen, E., Wagner, G.G., Gerstorf, D., Lindenberger, U., and Gaser, C. (2022). Linking Brain Age Gap to Mental and Physical Health in the Berlin Aging Study II. Front. Aging Neurosci., 14.10.3389/fnagi.2022.791222 ↗
9. Kalapun, O., Moiseev, A., Medvedev, G., Doesburg, S.M., Xi, P., Moreno, S., Ribary, U., and Vakorin, V.A. (2024, January 3). Biological Age from Electroencephalographic Activity Could Be Decoupled from a Gradual Stochastic Accumulation of Pathologies over Adulthood. Proceedings of the 2024 IEEE International Conference on Bioinformatics and Biomedicine (BIBM), Lisbon, Portugal.10.1109/BIBM62325.2024.10821857 ↗
10. State and Trait Components of Functional Connectivity: Individual Differences Vary with Mental State10.1523/JNEUROSCI.1324-15.2015 ↗
11. Waschke, L., Wöstmann, M., and Obleser, J. (2017). States and Traits of Neural Irregularity in the Age-Varying Human Brain. Sci. Rep., 7.10.1038/s41598-017-17766-4 ↗
12. The Heavy Tail of the Human Brain10.1016/j.conb.2014.10.014 ↗
13. The Log-Dynamic Brain: How Skewed Distributions Affect Network Operations10.1038/nrn3687 ↗
14. Banerjee, S., Scheirer, W.J., and Li, L. (2019). An Extreme Value Theory Model of Cross-Modal Sensory Information Integration in Modulation of Vertebrate Visual System Functions. Front. Comput. Neurosci., 13.10.3389/fncom.2019.00003 ↗
15. Mean and Variability in Functional Brain Activations Differentially Predict Executive Function in Older Adults: An Investigation Employing Functional near-Infrared Spectroscopy10.1117/1.NPh.5.1.011013 ↗
16. “Average Is Good, Extremes Are Bad”—Non-Linear Inverted U-Shaped Relationship between Neural Mechanisms and Functionality of Mental Features10.1016/j.neubiorev.2019.06.030 ↗
17. Timme, N.M., Marshall, N.J., Bennett, N., Ripp, M., Lautzenhiser, E., and Beggs, J.M. (2016). Criticality Maximizes Complexity in Neural Tissue. Front. Physiol., 7.10.3389/fphys.2016.00425 ↗
18. Individual (Co)Variation in Resting and Maximal Metabolic Rates in Wild Mice10.1086/716042 ↗
19. Computer-Assisted Analysis of Routine EEG to Identify Hidden Biomarkers of Epilepsy: A Systematic Review10.1016/j.csbj.2023.12.006 ↗
20. Shafto, M.A., Tyler, L.K., Dixon, M., Taylor, J.R., Rowe, J.B., Cusack, R., Calder, A.J., Marslen-Wilson, W.D., Duncan, J., and Dalgleish, T. (2014). The Cambridge Centre for Ageing and Neuroscience (Cam-CAN) Study Protocol: A Cross-Sectional, Lifespan, Multidisciplinary Examination of Healthy Cognitive Ageing. BMC Neurol., 14.10.1186/s12883-014-0204-1 ↗
21. The Cambridge Centre for Ageing and Neuroscience (Cam-CAN) Data Repository: Structural and Functional MRI, MEG, and Cognitive Data from a Cross-Sectional Adult Lifespan Sample10.1016/j.neuroimage.2015.09.018 ↗
22. Estimating Brain Age from Structural MRI and MEG Data: Insights from Dimensionality Reduction Techniques10.1016/j.neuroimage.2021.117822 ↗
23. MNE Software for Processing MEG and EEG Data10.1016/j.neuroimage.2013.10.027 ↗
24. Integration of Amplitude and Phase Statistics for Complete Artifact Removal in Independent Components of Neuromagnetic Recordings10.1109/TBME.2008.926677 ↗
25. An Algorithm for Linearly Constrained Adaptive Array Processing10.1109/PROC.1972.8817 ↗
26. Ilmoniemi, R.J., and Sarvas, J. (2019). Brain Signals: Physics and Mathematics of MEG and EEG, MIT Press.10.7551/mitpress/10745.001.0001 ↗
27. Cortical Surface-Based Analysis10.1006/nimg.1998.0395 ↗
28. Automatically Parcellating the Human Cerebral Cortex10.1093/cercor/bhg087 ↗
29. FreeSurfer10.1016/j.neuroimage.2012.01.021 ↗
30. Local-Global Parcellation of the Human Cerebral Cortex from Intrinsic Functional Connectivity MRI10.1093/cercor/bhx179 ↗
31. The Organization of the Human Cerebral Cortex Estimated by Intrinsic Functional Connectivity10.1152/jn.00338.2011 ↗
32. Jirsa, V., and Müller, V. (2013). Cross-Frequency Coupling in Real and Virtual Brain Networks. Front. Comput. Neurosci., 7.10.3389/fncom.2013.00078 ↗
33. Neural Cross-Frequency Coupling: Connecting Architectures, Mechanisms, and Functions10.1016/j.tins.2015.09.001 ↗
34. The Functional Role of Cross-Frequency Coupling10.1016/j.tics.2010.09.001 ↗
35. A Critical Note on the Definition of Phase–Amplitude Cross-Frequency Coupling10.1016/j.jneumeth.2011.08.014 ↗
36. Phase-Amplitude Coupling and Phase Synchronization Between Medial Temporal, Frontal and Posterior Brain Regions Support Episodic Autobiographical Memory Recall10.1007/s10548-022-00890-4 ↗
37. PyWavelets: A Python Package for Wavelet Analysis10.21105/joss.01237 ↗
38. Sparse Bayesian Learning and the Relevance Vector Machine
39. The Distance Correlation t -Test of Independence in High Dimension10.1016/j.jmva.2013.02.012 ↗
40. Partial Least Squares Analysis of Neuroimaging Data: Applications and Advances10.1016/j.neuroimage.2004.07.020 ↗
41. Partial Least Squares (PLS) Methods for Neuroimaging: A Tutorial and Review10.1016/j.neuroimage.2010.07.034 ↗
42. Vakorin, V.A., McIntosh, A.R., Mišić, B., Krakovska, O., Poulsen, C., Martinu, K., and Paus, T. (2013). Exploring Age-Related Changes in Dynamical Non-Stationarity in Electroencephalographic Signals During Early Adolescence. PLoS ONE, 8.10.1371/journal.pone.0057217 ↗
43. Developmental Changes in Neuromagnetic Rhythms and Network Synchrony in Autism10.1002/ana.24836 ↗
44. Scale-Free Networks Are Rare10.1038/s41467-019-08746-5 ↗
45. Joshua Davis, J.J., Schubeler, F., Ji, S., and Kozma, R. (2020, January 11). Discrimination Between Brain Cognitive States Using Shannon Entropy and Skewness Information Measure. Proceedings of the 2020 IEEE International Conference on Systems, Man, and Cybernetics (SMC), Toronto, ON, Canada.10.1109/SMC42975.2020.9283315 ↗
46. Kurtosis-Based Detection of Intracranial High-Frequency Oscillations for the Identification of the Seizure Onset Zone10.1142/S0129065718500016 ↗
47. The Use of Kurtosis De-Noising for EEG Analysis of Patients Suffering from Alzheimer’s Disease
48. The Study of Classification of Motor Imaginaries Based on Kurtosis of EEG
49. Vakorin, V.A., Liaqat, H., Doesburg, S.M., and Moreno, S. (2025). Extreme Signal Amplitude Events in Neuromagnetic Oscillations Reveal Brain Aging Processing across Adulthood. Front. Aging Neurosci., 17.10.3389/fnagi.2025.1498400 ↗
50. Estimating Fugl-Meyer Upper Extremity Motor Score from Functional-Connectivity Measures10.1109/TNSRE.2020.2978381 ↗
51. Weng, T.-W., Zhang, H., Chen, P.-Y., Yi, J., Su, D., Gao, Y., Hsieh, C.-J., and Daniel, L. (2018). Evaluating the Robustness of Neural Networks: An Extreme Value Theory Approach. arXiv.
52. Fluid Intelligence and the Cross-Frequency Coupling of Neuronal Oscillations10.1017/sjp.2016.86 ↗
53. Cross Frequency Coupling in next Generation Inhibitory Neural Mass Models10.1063/1.5125216 ↗
54. Qin, Y., and Sheremet, A. (2022). Mesoscopic Collective Activity in Excitatory Neural Fields: Cross-Frequency Coupling. arXiv.
55. Neuronal Ensembles: Building Blocks of Neural Circuits10.1016/j.neuron.2023.12.008 ↗
56. Bybee, C., Belsten, A., and Sommer, F.T. (2022). Cross-Frequency Coupling Increases Memory Capacity in Oscillatory Neural Networks. arXiv.10.1145/3517343.3517369 ↗
57. A Network Correspondence Toolbox for Quantitative Evaluation of Novel Neuroimaging Results10.1038/s41467-025-58176-9 ↗
58. Object Repetition Leads to Local Increases in the Temporal Coordination of Neural Responses
59. Phase-Amplitude Coupling and Long-Range Phase Synchronization Reveal Frontotemporal Interactions During Visual Working Memory10.1523/JNEUROSCI.2130-16.2016 ↗
60. Minati, G., Abram, M.R., and Pessa, E. (2016). Cross-Frequency Modulation, Network Information Integration and Cognitive Performance in Complex Systems. Towards a Post-Bertalanffy Systemics, Springer International Publishing. Contemporary Systems Thinking.10.1007/978-3-319-24391-7 ↗
61. EEG Cross-Frequency Phase Synchronization as an Index of Memory Matching in Visual Search10.1016/j.neuroimage.2021.117971 ↗