Daily circadian misalignment impairs human cognitive performance task-dependently

Abstract

Shift work increases the risk for human errors, such that drowsiness due to shift work has contributed to major industrial disasters, including Space Shuttle Challenger, Chernobyl and Alaska Oil Spill disasters, with extraordinary socio-economical costs. Overnight operations pose a challenge because our circadian biology inhibits cognitive performance at night. Yet how the circadian system modulates cognition over multiple days under realistic shift work conditions remains to be established. Importantly, because task-specific cognitive brain regions show different 24-h circadian dynamics, we hypothesize that circadian misalignment impacts cognition task-dependently. Using a biologically-driven paradigm mimicking night shift work, with a randomized, cross-over design, we show that misalignment between the circadian pacemaker and behavioral/environmental cycles increases cognitive vulnerability on sustained attention, cognitive throughput, information processing and visual-motor performance over multiple days, compared to circadian alignment (day shifts). Circadian misalignment effects are task-dependent: while they acutely impair sustained attention with recovery after 3-days, they progressively hinder daily learning. Individuals felt sleepier during circadian misalignment, but they did not rate their performance as worse. Furthermore, circadian misalignment effects on sustained attention depended on prior sleep history. Collectively, daily circadian misalignment may provide an important biological framework for developing countermeasures against adverse cognitive effects in shift workers.

Differential effects of the circadian system and circadian misalignment on insulin sensitivity and insulin secretion in humans

“…Other aspects of this study—which was designed to test separate hypotheses—have previously been published[6, 21, 22, 23, 24]. …”

Assessing the effects of artificial light at night on biodiversity across latitude – Current knowledge gaps

“…Data sources: Falchi et al (2016), National Aeronotics and Space Administration (NASA), moderateresolution imaging spectroradiometer (MODIS) mission, and Giovanni only data system. For a global map of cloud cover fraction over the period 2002-2018, see Supporting Information Figure generates metabolism, sleep and cognitive disorders, depression syndrome, and may increase risk of some cancers (Bedrosian, Fonken, & Nelson, 2015;Borniger, Maurya, Periasamy, & Nelson, 2014;Chellappa, Morris, & Scheer, 2018;Stevens, Brainard, Blask, Lockley, & Motta, 2013). It inhibits the production of melatonin, a hormone that modifies stress response, mitochondria functioning, oxidative stress, metabolism, and immune defence (Carrillo-Vico, Guerrero, Lardone, & Reiter, 2005;Tallec, Théry, & Perret, 2016;Tan et al, 2010).…”

The importance of being rhythmic: Living in harmony with your body clocks

“…159,160 Altered expression levels of individual core clock genes are | 7 of 14 DIBNER associated with the progression of oncogenic transformation, making these genes plausible candidates for diagnostic biomarkers. 174 Exploring the mechanisms underlying cognitive performance under circadian misalignment is of particular importance, due to the well-established risk of human errors associated with shift work, which has contributed to major industrial catastrophes including the Chernobyl atomic disaster. [164][165][166][167] Furthermore, emerging genetic and molecular studies suggest that alterations in molecular clock components are associated with depression, bipolar disease and other mood disorders.…”

“…42,56,137,[161][162][163] Elegant mechanistic studies have provided molecular links between the circadian clock and cell cycle, suggesting a direct role for core clock proteins in regulating key components of cell cycle progression, tumorigenesis and DNA damage. 174 137,[168][169][170] Biallelic variants of the gene FBXL3, which encodes for 1 subunit of the ubiquitin ligase complex regulating CRY turnover via phosphorylation-dependent degradation, 171,172 were recently associated with autosomal recessive developmental delay and intellectual disability.…”

“…173 Lastly, acute circadian misalignment induced by a forced desynchrony protocol mimicking shift work impaired cognitive performance such as sustained attention and compromised learning capacity. 174 Exploring the mechanisms underlying cognitive performance under circadian misalignment is of particular importance, due to the well-established risk of human errors associated with shift work, which has contributed to major industrial catastrophes including the Chernobyl atomic disaster. 174…”