Distinct pattern of oculomotor impairment associated with acute sleep loss and circadian misalignment

Abstract

Key points Inadequate sleep and irregular work schedules have not only adverse consequences for individual health and well‐being, but also enormous economic and safety implications for society as a whole.This study demonstrates that visual motion processing and coordinated eye movements are significantly impaired when performed after sleep loss and during the biological night, and thus may be contributing to human error and accidents.Because affected individuals are often unaware of their sensorimotor and cognitive deficits, there is a critical need for non‐invasive, objective indicators of mild, yet potentially unsafe, impairment due to disrupted sleep or biological rhythms.Our findings show that a set of eye‐movement measures can be used to provide sensitive and reliable indicators of such mild neural impairments. AbstractSleep loss and circadian misalignment have long been known to impair human cognitive and motor performance with significant societal and health consequences. It is well known that human reaction time to a visual cue is impaired following sleep loss and circadian misalignment, but it has remained unclear how more complex visuomotor control behaviour is altered under these conditions. In this study, we measured 14 parameters of the voluntary ocular tracking response of 12 human participants (six females) to systematically examine the effects of sleep loss and circadian misalignment using a constant routine 24‐h acute sleep‐deprivation paradigm. The combination of state‐of‐the‐art oculometric and sleep‐research methodologies allowed us to document, for the first time, large changes in many components of pursuit, saccades and visual motion processing as a function of time awake and circadian phase. Further, we observed a pattern of impairment across our set of oculometric measures that is qualitatively different from that observed previously with other mild neural impairments. We conclude that dynamic vision and visuomotor control exhibit a distinct pattern of impairment linked with time awake and circadian phase. Therefore, a sufficiently broad set of oculometric measures could provide a sensitive and specific behavioural biomarker of acute sleep loss and circadian misalignment. We foresee potential applications of such oculometric biomarkers assisting in the assessment of readiness‐to‐perform higher risk tasks and in the characterization of sub‐clinical neural impairment in the face of a multiplicity of potential risk factors, including disrupted sleep and circadian rhythms.

Sleep deprivation‐induced oculomotor dysfunction: implications for surgical and medical performance

“…Secondly, according to Stone et al . (2019), participants who had experienced acute total sleep deprivation (TSD) in the prior 12 months were excluded from the study. This may limit the transferability of the data to chronically sleep deprived populations such as those that are in the healthcare industry, as it is still unclear whether acute TSD leads to the development of tolerance or adaptation towards impairment, or whether it worsens it.…”

“…Despite the aforementioned weaknesses and uncertainties, one must credit Stone et al . (2019) for their innovative and robust study design and the execution of the design, and their use of cutting‐edge technology in controlling participants’ ambient conditions in their holding rooms, plotting participants’ circadian rhythms, and detecting and tracking eye movements (using ultra‐high fidelity (250 Hz) eye trackers) and rigorous analysis algorithms and procedures.…”

“…A study by Stone et al . (2019) published in a previous issue of The Jounral of Physiology has gone beyond the established correlation between sleep loss and impaired oculomotor performance, pinpointing the exact functions impacted and quantitatively investigating the degree of impairment (Stone et al . 2019).…”

“…Stone et al . (2019) also demonstrated the relationship between impaired features of eye movements and sleep loss and circadian misalignment (SLCM) (Stone et al . 2019).…”

Accelerating eye movement research via accurate and affordable smartphone eye tracking

“…Beyond basic vision research, eye movements have also been of interest to the broader research community with applications ranging from saliency models for visual content analysis 19 , design evaluation 20 , usability and consumer behavior research 21 – 23 , driving 24 , gaming 25 , 26 , gaze-based interaction for accessibility 27 to medical research 28 , 29 . The underlying methodology, known as eye tracking, has been used for decades as a reliable way to measure eye movements 30 – 32 .…”