Ocular motility as a measure of cerebral dysfunction in adults with focal epilepsy

Hue Mun Au Yong; Meaghan Clough; Piero Perucca; Charles B Malpas; Patrick Kwan; Terence J O'Brien; Joanne Fielding

doi:10.1016/j.yebeh.2023.109140

Ocular motility as a measure of cerebral dysfunction in adults with focal epilepsy

Epilepsy Behav. 2023 Apr:141:109140. doi: 10.1016/j.yebeh.2023.109140. Epub 2023 Feb 20.

Authors

Hue Mun Au Yong¹, Meaghan Clough², Piero Perucca³, Charles B Malpas⁴, Patrick Kwan⁵, Terence J O'Brien⁶, Joanne Fielding⁷

Affiliations

¹ Department of Neurology, Alfred Health, Melbourne, Victoria, Australia; Department of Neuroscience, The Central Clinical School, Monash University, Melbourne, Victoria, Australia; Department of Neurology, Royal Melbourne Hospital, Parkville, Victoria, Australia. Electronic address: hue.auyong@monash.edu.
² Department of Neuroscience, The Central Clinical School, Monash University, Melbourne, Victoria, Australia. Electronic address: Meaghan.Clough@monash.edu.
³ Department of Neurology, Alfred Health, Melbourne, Victoria, Australia; Department of Neuroscience, The Central Clinical School, Monash University, Melbourne, Victoria, Australia; Department of Neurology, Royal Melbourne Hospital, Parkville, Victoria, Australia; Epilepsy Research Centre, Department of Medicine (Austin Health), The University of Melbourne, Heidelberg, Victoria, Australia; Bladin-Berkovic Comprehensive Epilepsy Program, Department of Neurology, Austin Health, Heidelberg, Victoria, Australia. Electronic address: piero.perucca@unimelb.edu.au.
⁴ Department of Neurology, Alfred Health, Melbourne, Victoria, Australia; Department of Neuroscience, The Central Clinical School, Monash University, Melbourne, Victoria, Australia; Department of Neurology, Royal Melbourne Hospital, Parkville, Victoria, Australia; Department of Medicine, Royal Melbourne Hospital, The University of Melbourne, Parkville, Victoria, Australia. Electronic address: charles.malpas@unimelb.edu.au.
⁵ Department of Neurology, Alfred Health, Melbourne, Victoria, Australia; Department of Neuroscience, The Central Clinical School, Monash University, Melbourne, Victoria, Australia; Department of Neurology, Royal Melbourne Hospital, Parkville, Victoria, Australia; Department of Medicine, Royal Melbourne Hospital, The University of Melbourne, Parkville, Victoria, Australia. Electronic address: patrick.kwan@monash.edu.
⁶ Department of Neurology, Alfred Health, Melbourne, Victoria, Australia; Department of Neuroscience, The Central Clinical School, Monash University, Melbourne, Victoria, Australia; Department of Neurology, Royal Melbourne Hospital, Parkville, Victoria, Australia; Department of Medicine, Royal Melbourne Hospital, The University of Melbourne, Parkville, Victoria, Australia. Electronic address: te.obrien@alfred.org.au.
⁷ Department of Neurology, Alfred Health, Melbourne, Victoria, Australia; Department of Neuroscience, The Central Clinical School, Monash University, Melbourne, Victoria, Australia. Electronic address: joanne.fielding@monash.edu.

PMID: 36812874
DOI: 10.1016/j.yebeh.2023.109140

Abstract

Objective: Using objective oculomotor measures, we aimed to: (1) compare oculomotor performance in patients with drug-resistant focal epilepsy to healthy controls, and (2) investigate the differential impact of epileptogenic focus laterality and location on oculomotor performance.

Methods: We recruited 51 adults with drug-resistant focal epilepsy from the Comprehensive Epilepsy Programs of two tertiary hospitals and 31 healthy controls to perform prosaccade and antisaccade tasks. Oculomotor variables of interest were latency, visuospatial accuracy, and antisaccade error rate. Linear mixed models were performed to compare interactions between groups (epilepsy, control) and oculomotor tasks, and between epilepsy subgroups and oculomotor tasks for each oculomotor variable.

Results: Compared to healthy controls, patients with drug-resistant focal epilepsy exhibited longer antisaccade latencies (mean difference = 42.8 ms, P = 0.001), poorer spatial accuracy for both prosaccade (mean difference = 0.4°, P = 0.002), and antisaccade tasks (mean difference = 2.1°, P < 0.001), and more antisaccade errors (mean difference = 12.6%, P < 0.001). In the epilepsy subgroup analysis, left-hemispheric epilepsy patients exhibited longer antisaccade latencies compared to controls (mean difference = 52.2 ms, P = 0.003), while right-hemispheric epilepsy was the most spatially inaccurate compared to controls (mean difference = 2.5°, P = 0.003). The temporal lobe epilepsy subgroup displayed longer antisaccade latencies compared to controls (mean difference = 47.6 ms, P = 0.005).

Significance: Patients with drug-resistant focal epilepsy exhibit poor inhibitory control as evidenced by a high percentage of antisaccade errors, slower cognitive processing speed, and impaired visuospatial accuracy on oculomotor tasks. Patients with left-hemispheric epilepsy and temporal lobe epilepsy have markedly impaired processing speed. Overall, oculomotor tasks can be a useful tool to objectively quantify cerebral dysfunction in drug-resistant focal epilepsy.

Keywords: Drug-resistant focal epilepsy; Inhibition; Oculomotor; Processing speed; Spatial accuracy.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adult
Epilepsies, Partial* / complications
Epilepsies, Partial* / diagnosis
Epilepsy* / complications
Epilepsy* / diagnosis
Epilepsy, Temporal Lobe*
Eye Movements
Humans
Reaction Time
Saccades