Saccadic Eye Movement Abnormalities in Children with Epilepsy

PLoS One. 2016 Aug 2;11(8):e0160508. doi: 10.1371/journal.pone.0160508. eCollection 2016.

Abstract

Childhood onset epilepsy is associated with disrupted developmental integration of sensorimotor and cognitive functions that contribute to persistent neurobehavioural comorbidities. The role of epilepsy and its treatment on the development of functional integration of motor and cognitive domains is unclear. Oculomotor tasks can probe neurophysiological and neurocognitive mechanisms vulnerable to developmental disruptions by epilepsy-related factors. The study involved 26 patients and 48 typically developing children aged 8-18 years old who performed a prosaccade and an antisaccade task. Analyses compared medicated chronic epilepsy patients and unmedicated controlled epilepsy patients to healthy control children on saccade latency, accuracy and dynamics, errors and correction rate, and express saccades. Patients with medicated chronic epilepsy had impaired and more variable processing speed, reduced accuracy, increased peak velocity and a greater number of inhibitory errors, younger unmedicated patients also showed deficits in error monitoring. Deficits were related to reported behavioural problems in patients. Epilepsy factors were significant predictors of oculomotor functions. An earlier age at onset predicted reduced latency of prosaccades and increased express saccades, and the typical relationship between express saccades and inhibitory errors was absent in chronic patients, indicating a persistent reduction in tonic cortical inhibition and aberrant cortical connectivity. In contrast, onset in later childhood predicted altered antisaccade dynamics indicating disrupted neurotransmission in frontoparietal and oculomotor networks with greater demand on inhibitory control. The observed saccadic abnormalities are consistent with a dysmaturation of subcortical-cortical functional connectivity and aberrant neurotransmission. Eye movements could be used to monitor the impact of epilepsy on neurocognitive development and help assess the risk for poor neurobehavioural outcomes.

MeSH terms

  • Adolescent
  • Age of Onset
  • Case-Control Studies
  • Cerebral Cortex / pathology
  • Cerebral Cortex / physiopathology*
  • Child
  • Cognitive Dysfunction / complications
  • Cognitive Dysfunction / diagnosis
  • Cognitive Dysfunction / pathology
  • Cognitive Dysfunction / physiopathology*
  • Epilepsy / complications
  • Epilepsy / diagnosis
  • Epilepsy / pathology
  • Epilepsy / physiopathology*
  • Female
  • Humans
  • Male
  • Nerve Net / pathology
  • Nerve Net / physiopathology*
  • Neuropsychological Tests
  • Ocular Motility Disorders / complications
  • Ocular Motility Disorders / diagnosis
  • Ocular Motility Disorders / pathology
  • Ocular Motility Disorders / physiopathology*
  • Photic Stimulation
  • Psychomotor Performance
  • Saccades*
  • Synaptic Transmission

Grants and funding

This work was supported by an Interdisciplinary Medical Research Council (MRC) and Economic and Social Research Council (ESRC) PhD Studentship awarded to Judith Lunn (award number ES/F010141/1). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.