SPM analysis of ictal–interictal SPECT in mesial temporal lobe epilepsy: Relationships between ictal semiology and perfusion changes

Summary

A combination of temporo-limbic hyperperfusion and extratemporal hypoperfusion was observed during complex partial seizures (CPS) in temporal lobe epilepsy (TLE). To investigate the clinical correlate of perfusion changes in TLE, we analyzed focal seizures of increasing severity using voxel-based analysis of ictal SPECT.

We selected 26 pre-operative pairs of ictal–interictal SPECTs from adult mesial TLE patients, seizure-free after surgery. Ictal SPECTs were classified in three groups: motionless seizures (group ML, n = 8), seizures with motor automatisms (MA) without dystonic posturing (DP) (group MA, n = 8), and seizures with DP with or without MA (DP, n = 10). Patients of group ML had simple partial seizures (SPS), while others had CPS. Groups of ictal–interictal SPECT were compared to a control group using statistical parametric mapping (SPM).

In ML group, SPM analysis failed to show significant changes. Hyperperfusion involved the anteromesial temporal region in MA group, and also the insula, posterior putamen and thalamus in DP group. Hypoperfusion was restricted to the posterior cingulate and prefrontal regions in MA group, and involved more widespread associative anterior and posterior regions in DP group.

Temporal lobe seizures with DP show the most complex pattern of combined hyper–hypoperfusion, possibly related both to a larger spread and the recruitment of more powerful inhibitory processes.

Introduction

SPECT have an established role for peri-ictal imaging in patients with focal drug-resistant epilepsy considered for surgical treatment (Cascino et al., 2004, Devous et al., 1998). In the syndrome of mesial temporal lobe epilepsy (MTLE), the most common type of refractory focal epilepsy, ictal perfusion changes involve not only the ictal onset zone (mesial temporal region), but also cortical and subcortical regions beyond the temporal lobe (Blumenfeld et al., 2004, Tae et al., 2005, Van Paesschen et al., 2003).

Hyperperfusion is also associated with ictal hypoperfusion during temporal lobe seizures (Chang et al., 2002, Lee et al., 2000, Tae et al., 2005, Van Paesschen et al., 2003). The underlying mechanism and clinical significance of the latter phenomenon is unclear, although some authors suggested that ictal hypoperfusion could be the consequence of a remote effect arising from subcortical structures (Blumenfeld et al., 2004).

More complex patterns of hyperperfusion with the increasing level of complexity and duration of temporal lobe seizures were reported using visual analysis of subtracted SPECT (Kaiboriboon et al., 2005, Shin et al., 2002), but most ictal SPECT studies pooled together various subtypes of complex partial seizures (CPS), without further details about the clinical semiology. Therefore, correlations between ictal blood flow patterns and ictal semiology are still lacking, while MTLE patients may have seizures of various complexities.

Although the terms complex partial seizures (CPS) and simple partial seizures (SPS) of the first classification are still widely used (Commission of ILAE, 1981), the task force for epilepsy classification and terminology recently proposed the term “focal motor seizures with typical (temporal lobe) automatisms” to refer to seizures of temporal lobe origin (Engel, 2001). Motor automatisms (MA) and contralateral dystonic posturing (DP) are typical motor symptoms of temporal lobe seizures. Whether and to what extent these symptoms contribute to the complexity of seizures, and therefore reflect different spreading pathways or remote effects, is still unclear. Despite the lack of evidence, MA are believed to result from the functional “release” of extratemporal regions (Loddenkemper and Kotagal, 2005). The pathophysiology of ictal DP is also not fully understood, although neuroimaging clues are pointing to the basal ganglia (Dupont et al., 1998, Mizobuchi et al., 2004).

Using ictal SPECT and voxel-based analysis, the aim of our study was to investigate relationships between ictal semiology and ictal blood flow patterns, focusing on the influence of motor outstanding symptoms of “typical” temporal lobe seizures, i.e. motor automatisms (MA) and dystonic posturing (DP). We hypothesized that the ictal blood flow patterns of CPS with DP versus no DP should be different and that seizures with DP should show more widespread remote effects on extratemporal areas, through the modulatory influence of basal ganglia. To test this hypothesis, we compared ictal SPECTs of temporal lobe seizures, classified according to the presence or absence of MA and DP.