Specific Deficits of Saccadic Eye Movements after Sleep Deprivation

Abstract

Sleep deprivation (SD) and reduced vigilance impair not only the performance of cognitive tasks, but also of saccadic eye movements. Previous literature reports reduced peak velocities and prolonged latencies of visually-guided saccades, but the latter remained controversial. To clarify which specific saccadic subfunctions reflect reduced vigilance, we investigated the effect of a one-night SD on 3 different types of saccades that are controlled by different cortical networks: 1) visually-guided pro-saccades controlled more by the parietal (PEF) than by the frontal eye field (FEF; 2) anti-saccades (performed into the direction opposite to a peripheral target, with respect to the vertical meridian), controlled by FEF, the dorsolateral prefrontal cortex (DLPFC), and the basal ganglia loop; 3) memory-guided saccades (performed to a peripheral target that had been flashed 1 to 30s before), controlled by the PEF, the FEF, the supplementary eye field (SEF), the DLPFC and the basal ganglia loop. Eye movements were recorded using EOG in 15 healthy adults at 3 different times: in the evening prior to SD (baseline), in the next morning following a one night's SD (day 1), and 24 hours later (day 2), following a night of sufficient sleep. A control group of 15 healthy adults was tested similarly, but without SD. Results showed specific effects of SD only on day 1, that had recovered completely on day 2 and were not found in the control group: 1) reduced peak velocities of all 3 types of saccades, indicating dysfunction of the paramedian pontine reticular formation (PPRF), which is part of the ascending reticular system involved in sleep-wake regulation; 2) prolonged latencies only of memory-guided saccades, but normal metrics, reflecting impaired initiation of voluntary saccades. Due to their long memorization times of up to 30s they had to be initiated almost like self-paced saccades which are controlled by the SEF. 3) Dysmetria (mainly hypometria) of visually-guided saccades, indicating rather a cerebellar dysfunction, as the essential functions of the PEF (latency of visually-guided saccades and metrics of memory-guided saccades) and of the FEF (error rate and latency of anti-saccades) were not affected. We conclude that sleep deprivation and reduced vigilance cause dysfunction of specific brain areas, such as the SEF, the cerebellum, and the PPRF, whereas other areas were not affected, particularly the primary frontal and parietal eye fields.