Verbal paired associates learning lateralizes left hippocampal sclerosis in temporal lobe epilepsy

Abstract Objective Left hippocampal sclerosis (HS) is associated with verbal‐specific memory impairment. This association is well established for word list learning tasks, and there is some evidence that this may also be relevant to verbal paired associates learning (PAL), though the evidence is lim...

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Main Authors: Andy Sitoh, David Weintrob, Jacqueline F. I. Anderson, Angela R. Jackman, Marie F. O'Shea, Graeme D. Jackson, Piero Perucca, Chris Tailby
Format: Article
Language:English
Published: Wiley 2025-02-01
Series:Epilepsia Open
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Online Access:https://doi.org/10.1002/epi4.13118
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author Andy Sitoh
David Weintrob
Jacqueline F. I. Anderson
Angela R. Jackman
Marie F. O'Shea
Graeme D. Jackson
Piero Perucca
Chris Tailby
author_facet Andy Sitoh
David Weintrob
Jacqueline F. I. Anderson
Angela R. Jackman
Marie F. O'Shea
Graeme D. Jackson
Piero Perucca
Chris Tailby
author_sort Andy Sitoh
collection DOAJ
description Abstract Objective Left hippocampal sclerosis (HS) is associated with verbal‐specific memory impairment. This association is well established for word list learning tasks, and there is some evidence that this may also be relevant to verbal paired associates learning (PAL), though the evidence is limited. We aimed to evaluate the utility of verbal PAL as a marker for left HS, compare this with word list learning, and derive cutoff scores to facilitate clinical application. Methods Retrospective analysis of Rey Auditory Verbal Learning Test (RAVLT) and PAL scores obtained from 116 surgically naïve temporal lobe epilepsy patients with HS (14 bilateral, 57 left, 45 right; range of N across test indices: 77–110). Results Relative to right HS, left HS and bilateral HS were associated with poorer performance on PAL Hard Pairs (p < 0.001) and all RAVLT indices (p < 0.001), with performance comparable in left HS and bilateral HS (p > 0.05). PAL Hard Pairs and all RAVLT indices displayed acceptable discriminatory ability (AUC > 0.70) in classifying left‐sided HS (unilateral left or bilateral HS), with RAVLT delayed recall the strongest predictor (AUC = 0.87; PAL Hard Pairs Learning and Delay = 0.80 and 0.83, respectively). Optimal cutoff scores for left‐sided HS classification were generated. Significance Although the RAVLT delayed recall was the strongest predictor of left‐sided HS, PAL Hard Pairs also demonstrated excellent discriminatory capacity, offering an additional cognitive marker of left hippocampal integrity to complement word list learning in clinical assessments. Plain Language Statement The results of the study show that the ability to learn unrelated pairs of words (e.g., “silver”–“run”) is compromised in the setting of epilepsy with left‐sided hippocampal sclerosis (HS), be it unilateral left HS or bilateral HS. The ability of unrelated word pair learning to discriminate left vs. right HS was comparable to word list learning, a task with demonstrated sensitivity to left HS. Our results suggest that the ability to learn unrelated pairs of words provides another useful marker of left‐sided hippocampal compromise in epilepsy. We provide cutoff scores to facilitate clinical interpretation.
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spelling doaj-art-b2c44f8d36fe49f6bb0405d25ffceed52025-02-07T09:12:45ZengWileyEpilepsia Open2470-92392025-02-0110128629710.1002/epi4.13118Verbal paired associates learning lateralizes left hippocampal sclerosis in temporal lobe epilepsyAndy Sitoh0David Weintrob1Jacqueline F. I. Anderson2Angela R. Jackman3Marie F. O'Shea4Graeme D. Jackson5Piero Perucca6Chris Tailby7School of Psychological Sciences University of Melbourne Melbourne Victoria AustraliaDepartment of Clinical Neuropsychology Austin Health Melbourne Victoria AustraliaSchool of Psychological Sciences University of Melbourne Melbourne Victoria AustraliaMonash Health Clayton Victoria AustraliaSchool of Psychological Sciences University of Melbourne Melbourne Victoria AustraliaBladin‐Berkovic Comprehensive Epilepsy Program, Department of Neurology Austin Health Melbourne Victoria AustraliaBladin‐Berkovic Comprehensive Epilepsy Program, Department of Neurology Austin Health Melbourne Victoria AustraliaDepartment of Clinical Neuropsychology Austin Health Melbourne Victoria AustraliaAbstract Objective Left hippocampal sclerosis (HS) is associated with verbal‐specific memory impairment. This association is well established for word list learning tasks, and there is some evidence that this may also be relevant to verbal paired associates learning (PAL), though the evidence is limited. We aimed to evaluate the utility of verbal PAL as a marker for left HS, compare this with word list learning, and derive cutoff scores to facilitate clinical application. Methods Retrospective analysis of Rey Auditory Verbal Learning Test (RAVLT) and PAL scores obtained from 116 surgically naïve temporal lobe epilepsy patients with HS (14 bilateral, 57 left, 45 right; range of N across test indices: 77–110). Results Relative to right HS, left HS and bilateral HS were associated with poorer performance on PAL Hard Pairs (p < 0.001) and all RAVLT indices (p < 0.001), with performance comparable in left HS and bilateral HS (p > 0.05). PAL Hard Pairs and all RAVLT indices displayed acceptable discriminatory ability (AUC > 0.70) in classifying left‐sided HS (unilateral left or bilateral HS), with RAVLT delayed recall the strongest predictor (AUC = 0.87; PAL Hard Pairs Learning and Delay = 0.80 and 0.83, respectively). Optimal cutoff scores for left‐sided HS classification were generated. Significance Although the RAVLT delayed recall was the strongest predictor of left‐sided HS, PAL Hard Pairs also demonstrated excellent discriminatory capacity, offering an additional cognitive marker of left hippocampal integrity to complement word list learning in clinical assessments. Plain Language Statement The results of the study show that the ability to learn unrelated pairs of words (e.g., “silver”–“run”) is compromised in the setting of epilepsy with left‐sided hippocampal sclerosis (HS), be it unilateral left HS or bilateral HS. The ability of unrelated word pair learning to discriminate left vs. right HS was comparable to word list learning, a task with demonstrated sensitivity to left HS. Our results suggest that the ability to learn unrelated pairs of words provides another useful marker of left‐sided hippocampal compromise in epilepsy. We provide cutoff scores to facilitate clinical interpretation.https://doi.org/10.1002/epi4.13118receiver operating characteristicRey auditory verbal learning taskverbal memoryverbal paired associate learningWeschler memory scaleword list learning
spellingShingle Andy Sitoh
David Weintrob
Jacqueline F. I. Anderson
Angela R. Jackman
Marie F. O'Shea
Graeme D. Jackson
Piero Perucca
Chris Tailby
Verbal paired associates learning lateralizes left hippocampal sclerosis in temporal lobe epilepsy
Epilepsia Open
receiver operating characteristic
Rey auditory verbal learning task
verbal memory
verbal paired associate learning
Weschler memory scale
word list learning
title Verbal paired associates learning lateralizes left hippocampal sclerosis in temporal lobe epilepsy
title_full Verbal paired associates learning lateralizes left hippocampal sclerosis in temporal lobe epilepsy
title_fullStr Verbal paired associates learning lateralizes left hippocampal sclerosis in temporal lobe epilepsy
title_full_unstemmed Verbal paired associates learning lateralizes left hippocampal sclerosis in temporal lobe epilepsy
title_short Verbal paired associates learning lateralizes left hippocampal sclerosis in temporal lobe epilepsy
title_sort verbal paired associates learning lateralizes left hippocampal sclerosis in temporal lobe epilepsy
topic receiver operating characteristic
Rey auditory verbal learning task
verbal memory
verbal paired associate learning
Weschler memory scale
word list learning
url https://doi.org/10.1002/epi4.13118
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