Altered topological properties and their relationship to cognitive functions in unilateral temporal lobe epilepsy

Abstract

Objective: To investigate abnormalities in topological properties in unilateral temporal lobe epilepsy (TLE) with hippocampal sclerosis and their correlations with cognitive functions.

Methods: Thirty-eight patients with TLE and 19 age- and sex-matched healthy controls (HCs) were enrolled in this research and underwent resting-state functional magnetic resonance imaging (fMRI) examinations. Whole-brain functional networks of participants were constructed based on the fMRI data. Topological characteristics of the functional network were compared between patients with left and right TLE and HCs. Correlations between altered topological properties and cognitive measurements were explored.

Results: Compared with the HCs, patients with left TLE showed decreased clustering coefficient, global efficiency, and local efficiency (E_loc), and patients with right TLE showed decreased E_loc. We found altered nodal centralities in six regions related to the basal ganglia (BG) network or default mode network (DMN) in patients with left TLE and those in three regions related to reward/emotion network or ventral attention network in patients with right TLE. Patients with right TLE showed higher integration (reduced nodal shortest path length) in four regions related to the DMN and lower segregation (reduced nodal local efficiency and nodal clustering coefficient) in the right middle temporal gyrus. When comparing left TLE with right TLE, no significant differences were detected in global parameters, but the nodal centralities in the left parahippocampal gyrus and the left pallidum were decreased in left TLE. The E_loc and several nodal parameters were significantly correlated with memory functions, duration, national hospital seizure severity scale (NHS3), or antiseizure medications (ASMs) in patients with TLE.

Conclusions: The topological properties of whole-brain functional networks were disrupted in TLE. Networks of left TLE were characterized by lower efficiency; right TLE was preserved in global efficiency but disrupted in fault tolerance. Several nodes with abnormal topological centrality in the basal ganglia network beyond the epileptogenic focus in the left TLE were not found in the right TLE. Right TLE had some nodes with reduced shortest path length in regions of the DMN as compensation. These findings provide new insights into the effect of lateralization on TLE and help us to understand the cognitive impairment of patients with TLE.

Keywords: cognition; functional magnetic resonance imaging; graph theory; temporal lobe epilepsy.