The spatial learning task of Lhermitte and Signoret: Marker of bilateral hippocampal dysfunction in temporal lobe epilepsy

Abstract

Abstract Objective Bilateral hippocampal compromise in temporal lobe epilepsy (TLE) substantially increases the risk of significant adverse memory outcomes following unilateral anterior temporal lobectomy and may contraindicate surgery. The Spatial Learning Task (SLT) of Lhermitte and Signoret (1972) is a simple object–location arbitrary associative learning task proposed as a marker of bitemporal dysfunction. Here, we test whether the SLT might serve as a useful marker in TLE by examining, in individuals with TLE and hippocampal sclerosis (HS), whether performance on the SLT depends on the laterality of the HS (left, right, bilateral). We hypothesize that performance will be worst in the setting of bilateral HS. Methods Retrospective analysis of 63 surgically naïve TLE‐HS patients (16 bilateral HS, 28 left HS, 19 right HS) who underwent neuropsychological evaluation at a tertiary epilepsy center. Results Bilateral HS cases showed significantly poorer SLT learning and learning efficiency compared to right HS cases (p ≤ .005, BF10 ≥ 25). Left HS cases performed comparably to bilateral HS cases on early trials but typically achieved ceiling performance with repetition, reflecting inefficiency rather than capacity loss. An SLT learning score <13 yielded high specificity (96% [95% CI: 0.85–0.99]) but modest sensitivity (44% [95% CI 0.20–0.70]) for identifying bilateral HS cases. Significance In the setting of TLE‐HS, poor performance on the SLT increases the probability of bilateral hippocampal pathology, supporting its utility as a rule‐in indicator. Although intact scores do not reliably exclude bilateral pathology, a low score on this task should prompt further investigations as to possible bitemporal compromise, and suggest risk of adverse memory outcomes following surgery. Prospective, post‐operative studies will be required to quantify this risk. Plain Language Statement The results of the study show that the ability to learn arbitrary object–location pairings is compromised in the setting of temporal lobe epilepsy with bilateral hippocampal sclerosis (HS). In contrast, patients with unilateral HS generally retained sufficient capacity to learn the task, though those with left HS were slower to acquire the pairings across repeated trials. A low score on this task was a strong indicator of bilateral hippocampal pathology, whereas an intact score did not reliably exclude it. Our results suggest that performance on this simple learning task provides a useful marker of bilateral hippocampal compromise in epilepsy and may be particularly valuable in patients for whom standard memory tests are less suitable. We provide a cutoff score to facilitate clinical interpretation.