Macroscale intrinsic dynamics are associated with microcircuit function in focal and generalized epilepsies

• Published in: Communications biology 2024-02, Vol.7 (1), p.145-12, Article 145
• Main Authors: Yang, Siqi, Zhou, Yimin, Peng, Chengzong, Meng, Yao, Chen, Huafu, Zhang, Shaoshi, Kong, Xiaolu, Kong, Ru, Yeo, B. T. Thomas, Liao, Wei, Zhang, Zhiqiang
• Format: Article
• Language: English
• Subjects: 59; 59/36; 631/114/2397; 692/617/375/178; Biomedical and Life Sciences; Brain - diagnostic imaging; Brain architecture; Brain mapping; Circuits; Epilepsy; Epilepsy, Generalized; Epilepsy, Temporal Lobe; Functional magnetic resonance imaging; Humans; Life Sciences; Neurological diseases; Seizures; Temporal lobe; Temporal variations; Time series
• ISSN: 2399-3642; 2399-3642
• DOI: 10.1038/s42003-024-05819-0

Epilepsies are a group of neurological disorders characterized by abnormal spontaneous brain activity, involving multiscale changes in brain functional organizations. However, it is not clear to what extent the epilepsy-related perturbations of spontaneous brain activity affect macroscale intrinsic dynamics and microcircuit organizations, that supports their pathological relevance. We collect a sample of patients with temporal lobe epilepsy (TLE) and genetic generalized epilepsy with tonic-clonic seizure (GTCS), as well as healthy controls. We extract massive temporal features of fMRI BOLD time-series to characterize macroscale intrinsic dynamics, and simulate microcircuit neuronal dynamics used a large-scale biological model. Here we show whether macroscale intrinsic dynamics and microcircuit dysfunction are differed in epilepsies, and how these changes are linked. Differences in macroscale gradient of time-series features are prominent in the primary network and default mode network in TLE and GTCS. Biophysical simulations indicate reduced recurrent connection within somatomotor microcircuits in both subtypes, and even more reduced in GTCS. We further demonstrate strong spatial correlations between differences in the gradient of macroscale intrinsic dynamics and microcircuit dysfunction in epilepsies. These results emphasize the impact of abnormal neuronal activity on primary network and high-order networks, suggesting a systematic abnormality of brain hierarchical organization. An fMRI study suggests that epilepsy-related perturbations of spontaneous brain activity affect macroscale intrinsic dynamics and microcircuit organizations, and that they are highly spatially correlated.