Accelerated cognitive ageing (ACA) is an ageing co-morbidity in epilepsy that is diagnosed through the observation of an evident IQ decline of more than 1 standard deviation (15 points) around the age of 50 years old. To understand the mechanism of action of this pathology, we assessed brain dynamics with the use of resting-state fMRI data. In this paper, we present novel and promising methods to extract brain dynamics between large-scale resting-state networks: the emulative power, wavelet coherence, and granger causality between the networks were extracted in two resting-state sessions of 24 participants (10 ACA, 14 controls). We also calculated the widely used static functional connectivity to compare the methods. To find the best biomarkers of ACA, and have a better understanding of this epilepsy co-morbidity we compared the aforementioned between-network neurodynamics using classifiers and known machine learning algorithms; and assessed their performance. Results show that features based on the evolutionary game theory on networks approach, the emulative powers, are the best descriptors of the co-morbidity, using dynamics associated with the default mode and dorsal attention networks. With these dynamic markers, linear discriminant analysis could identify ACA patients at 82.9% accuracy. Using wavelet coherence features with decision-tree algorithm, and static functional connectivity features with support vector machine, ACA could be identified at 77.1% and 77.9% accuracy respectively. Granger causality fell short of being a relevant biomarker with best classifiers having an average accuracy of 67.9%. Combining the features based on the game theory, wavelet coherence, Granger-causality, and static functional connectivity- approaches increased the classification performance up to 90.0% average accuracy using support vector machine with a peak accuracy of 95.8%. The dynamics of the networks that lead to the best classifier performances are known to be challenged in elderly. Since our groups were age-matched, the results are in line with the idea of ACA patients having an accelerated cognitive decline. This classification pipeline is promising and could help to diagnose other neuropsychiatric disorders, and contribute to the field of psychoradiology.