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Journal Article Ahead of print

PubMed: 41884995 DOI: 10.1002/epi4.70195

Evaluating the task-specificity model of verbal memory: Regional volumetric analyses in temporal lobe epilepsy with hippocampal sclerosis.

Epilepsia Open

Authors: Andy Sitoh, David Weintrob, Jacqueline F I Anderson, Heath R Pardoe, Marie F O'Shea, Graeme D Jackson, Piero Perucca, Chris Tailby

Affiliations

  • School of Psychological Sciences, University of Melbourne, Melbourne, Victoria, Australia. Department of Clinical Neuropsychology, Austin Health, Melbourne, Victoria, Australia.
  • Department of Clinical Neuropsychology, Austin Health, Melbourne, Victoria, Australia. Bladin-Berkovic Comprehensive Epilepsy Program, Department of Neurology, Austin Health, Melbourne, Victoria, Australia.
  • School of Psychological Sciences, University of Melbourne, Melbourne, Victoria, Australia.
  • Florey Institute of Neuroscience and Mental Health, Melbourne, Victoria, Australia.
  • Department of Clinical Neuropsychology, Austin Health, Melbourne, Victoria, Australia.
  • Bladin-Berkovic Comprehensive Epilepsy Program, Department of Neurology, Austin Health, Melbourne, Victoria, Australia.
  • Bladin-Berkovic Comprehensive Epilepsy Program, Department of Neurology, Austin Health, Melbourne, Victoria, Australia. Department of Medicine (Austin Health), The University of Melbourne, Melbourne, Victoria, Australia. Department of Neuroscience, School of Translational Medicine, Monash University, Melbourne, Victoria, Australia. Department of Neurology, Alfred Health, Melbourne, Victoria, Australia. Department of Neurology, The Royal Melbourne Hospital, Melbourne, Victoria, Australia.

Abstract

OBJECTIVE

Verbal memory tasks differ in their cognitive demands and may rely on distinct left medial temporal structures. One model holds that verbal delayed recall is hippocampal dependent, whereas verbal paired associate learning relies on adjacent rhinal cortex. We test this by examining the relationship between task performance and regional temporal lobe volumes in individuals with temporal lobe epilepsy and hippocampal sclerosis (TLE-HS).

METHODS

Retrospective analysis of 99 surgically naïve TLE patients (12 bilateral TLE-HS, 35 left TLE-HS, 28 right TLE-HS, and 24 MRI-negative left TLE) with contemporaneous neuropsychological and T1-weighted MRI data. Delayed recall was operationalized using the Rey Auditory Verbal Learning Test, and arbitrary associative learning with the Paired Associates Learning subtest. Linear regressions assessed associations between memory performance and temporal lobe volumes. We also studied a cohort with nonlesional left TLE to better distinguish the relative impact on verbal memory of left temporal onset seizures versus the structural integrity of the left mesial temporal lobe.

RESULTS

Patients with left-sided TLE-HS (unilateral/bilateral) performed significantly worse on both memory measures compared to right TLE-HS and MRI-negative left TLE (p < 0.001). Left hippocampal volume significantly predicted performance on both measures (both p < 0.001), whereas rhinal cortex volumes were not significantly associated with either. Secondary analyses revealed associations between left temporal pole volume and both memory measures, and between inferior temporal gyrus volume and delayed recall.

SIGNIFICANCE

Despite differing cognitive demands, both verbal arbitrary associative learning and delayed recall were primarily linked to left hippocampal volume, underscoring its central role in verbal memory impairment in TLE. Associations with the temporal pole and inferior temporal regions suggest additional contributions from extrahippocampal areas. Left hippocampal atrophy exacerbates verbal memory impairment beyond what would be expected from seizure activity alone.

PLAIN LANGUAGE STATEMENT

The results of this study show that the ability to learn semantically unrelated information and recall unstructured information after a period of delay is particularly compromised in individuals with left hippocampal atrophy. These impairments were strongly associated with reduced left hippocampal volume. In contrast, volumes of the adjacent rhinal cortex were not related to memory performance. These findings underscore the central role of the left hippocampus in supporting verbal memory in temporal lobe epilepsy.

MeSH

Sclerosis, Epilepsy, Atrophy, Mental Recall, Paired-Associate Learning, Epilepsy, Temporal Lobe, Seizures, Learning, Memory, Temporal Lobe, Hippocampal Sclerosis