Altered Sleep Microarchitecture and Cognitive Impairment in Patients With Temporal Lobe Epilepsy

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Abstract
Objectives: To investigate the spatiotemporal characteristics of sleep waveforms in temporal lobe epilepsy (TLE) and examine their association with cognition. Methods: In this retrospective, cross-sectional study, we examined overnight EEG data from adult patients with temporal lobe epilepsy (TLE) and non-epilepsy comparisons (NEC) admitted to the epilepsy monitoring unit (EMU) at Mass General Brigham hospitals. Automated algorithms were used to characterize sleep macro-architecture (sleep stages), and micro-architecture (spindles, slow oscillations) on scalp EEG, and to detect hippocampal interictal epileptiform discharges (hIEDs) from foramen ovale (FO) electrodes simultaneously recorded in a subset of TLE patients. We examined the association of sleep features and hIEDs with memory and executive function from clinical neuropsychological evaluations. Results: A total of 81 TLE and 28 NEC adult patients were included with similar mean ages. There were no significant differences in sleep macro-architecture between groups, including relative time spent in each sleep stage, sleep efficiency, and sleep fragmentation. In contrast, the spatiotemporal characteristics of sleep micro-architecture were altered in TLE compared to NEC and were associated with cognitive impairments. Specifically, we observed a ∼30% reduction in spindle density in TLE compared to NEC patients, which was significantly associated with worse memory performance. Spindle-slow oscillation (SO) coupling strength was also reduced in TLE and, in contrast to spindles, was associated with diminished executive function. We found no significant association between sleep macro- and micro-architectural parameters and hIEDs. Conclusion: There is a fundamental alteration of sleep micro-architecture in TLE, characterized by a reduction in spindle density and spindle-SO coupling, and these changes may contribute to neurocognitive comorbidity in this disorder.

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