Impaired naming performance in temporal lobe epilepsy: language fMRI responses are modulated by disease characteristics

Karin Trimmel,Louis A Van Graan,Lorenzo Caciagli,Fenglai Xiao,Pamela J Thompson,John S Duncan,Matthias J Koepp

doi:10.1007/s00415-020-10116-x

Abstract

ObjectiveTo investigate alterations of language networks and their relation to impaired naming performance in temporal lobe epilepsy (TLE) using functional MRI.MethodsSeventy-two adult TLE patients (41 left) and 36 controls were studied with overt auditory and picture naming fMRI tasks to assess temporal lobe language areas, and a covert verbal fluency task to probe frontal lobe language regions. Correlation of fMRI activation with clinical naming scores, and alteration of language network patterns in relation to epilepsy duration, age at onset and seizure frequency, were investigated with whole-brain multiple regression analyses.ResultsAuditory and picture naming fMRI activated the left posterior temporal lobe, and stronger activation correlated with better clinical naming scores. Verbal fluency MRI mainly activated frontal lobe regions. In left and right TLE, a later age of epilepsy onset related to stronger temporal lobe activations, while earlier age of onset was associated with impaired deactivation of extratemporal regions. In left TLE patients, longer disease duration and higher seizure frequency were associated with reduced deactivation. Frontal lobe language networks were unaffected by disease characteristics.ConclusionsWhile frontal lobe language regions appear spared, temporal lobe language areas are susceptible to dysfunction and reorganisation, particularly in left TLE. Early onset and long duration of epilepsy, and high seizure frequency, were associated with compromised activation and deactivation patterns of task-associated regions, which might account for impaired naming performance in individuals with TLE.

Highlights

Temporal lobe epilepsy (TLE) is associated with impaired naming, when seizure onset is lateralised to the speech-dominant hemisphere [1, 2]
We recently showed that psychophysiological interaction (PPI)-based functional connectivity of left posterior temporal lobe language networks was reduced with earlier age of onset of epilepsy and longer disease duration in left TLE [8]
We show that functionally relevant temporal lobe fMRI activations are related to shorter disease duration, later age of onset and lower seizure frequency, whereas less favourable disease characteristics relate to impaired deactivation of task-negative regions, in LTLE, which might imply a higher risk for these patients to develop naming deficits following temporal lobe resection

Summary

Introduction

Temporal lobe epilepsy (TLE) is associated with impaired naming, when seizure onset is lateralised to the speech-dominant hemisphere [1, 2]. Especially posterior and basal temporal regions, are strongly involved in clinical naming performance [4], highlighting the importance of fMRI tasks that consistently activate these networks when evaluating TLE, such as the recently introduced auditory and visual naming fMRI paradigms [5]. The underlying patterns of language reorganisation leading to naming impairment in TLE, the role of temporal lobe language networks, as well as the effects of disease duration, age of onset and frequency of ongoing seizures are poorly understood. We recently showed that psychophysiological interaction (PPI)-based functional connectivity of left posterior temporal lobe language networks was reduced with earlier age of onset of epilepsy and longer disease duration in left TLE [8]. We hypothesised that: 1. Task-positive and task-negative fMRI responses during naming and verbal fluency fMRI predict clinical naming performance

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Results

Discussion

Conclusion