Factors affecting reorganisation of memory encoding networks in temporal lobe epilepsy

M.K Sidhu,J Stretton,G.P Winston,M Symms,P.J Thompson,M.J Koepp,J.S Duncan

doi:10.1016/j.eplepsyres.2014.11.001

M.K Sidhu, J Stretton + Show 5 more

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https://doi.org/10.1016/j.eplepsyres.2014.11.001

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Abstract

In temporal lobe epilepsy (TLE) due to hippocampal sclerosis reorganisation in the memory encoding network has been consistently described. Distinct areas of reorganisation have been shown to be efficient when associated with successful subsequent memory formation or inefficient when not associated with successful subsequent memory. We investigated the effect of clinical parameters that modulate memory functions: age at onset of epilepsy, epilepsy duration and seizure frequency in a large cohort of patients. We studied 53 patients with unilateral TLE and hippocampal sclerosis (29 left). All participants performed a functional magnetic resonance imaging memory encoding paradigm of faces and words. A continuous regression analysis was used to investigate the effects of age at onset of epilepsy, epilepsy duration and seizure frequency on the activation patterns in the memory encoding network. Earlier age at onset of epilepsy was associated with left posterior hippocampus activations that were involved in successful subsequent memory formation in left hippocampal sclerosis patients. No association of age at onset of epilepsy was seen with face encoding in right hippocampal sclerosis patients. In both left hippocampal sclerosis patients during word encoding and right hippocampal sclerosis patients during face encoding, shorter duration of epilepsy and lower seizure frequency were associated with medial temporal lobe activations that were involved in successful memory formation. Longer epilepsy duration and higher seizure frequency were associated with contralateral extra-temporal activations that were not associated with successful memory formation. Age at onset of epilepsy influenced verbal memory encoding in patients with TLE due to hippocampal sclerosis in the speech-dominant hemisphere. Shorter duration of epilepsy and lower seizure frequency were associated with less disruption of the efficient memory encoding network whilst longer duration and higher seizure frequency were associated with greater, inefficient, extra-temporal reorganisation.

Highlights

Temporal lobe epilepsy (TLE) is associated with impaired episodic memory
By performing an event-related subsequent memory analysis and correlations with out of scanner neuropsychometry measures we further classified these encoding activations as being associated with successful subsequent memory formation, and encoding activations not associated with successful subsequent memory formation (Sidhu et al, 2013).fMRI studies have shown that memory reorganisation within medial temporal lobe structures are influenced by age at onset of epilepsy, epilepsy duration and seizure frequency
There was no significant difference between the patient groups on the verbal memory measures (Independent sample t-test, p > 0.05) but left hippocampal sclerosis (LHS) patients performed significantly better than right hippocampal sclerosis (RHS) patients in the design learning and delayed design recall tasks (Independent sample two-tailed t-test p < 0.01), (Table 1)

Summary

Introduction

Temporal lobe epilepsy (TLE) is associated with impaired episodic memory. In healthy individuals functional imaging has shown material specific activation patterns, left hemispheric activation for verbal memory encoding and right for visual (Golby et al, 2002). We recently showed areas of increased temporal and extra-temporal activations during memory encoding in patients with left and right unilateral hippocampal sclerosis (HS) compared to healthy controls, a process that has been consistently described as functional reorganisation (Sidhu et al, 2013). By performing an event-related subsequent memory analysis and correlations with out of scanner neuropsychometry measures we further classified these encoding activations as being associated with successful subsequent memory formation, and encoding activations not associated with successful subsequent memory formation (Sidhu et al, 2013).fMRI studies have shown that memory reorganisation within medial temporal lobe structures are influenced by age at onset of epilepsy, epilepsy duration and seizure frequency. Factors influencing extra-temporal memory reorganisation have not been investigated

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