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Spontaneous attentional failures reflect multiplicative interactions of chronic sleep loss with acute sleep loss and circadian misalignment

Spontaneous attentional failures reflect multiplicative interactions of chronic sleep loss with acute sleep loss and circadian misalignment
Spontaneous attentional failures reflect multiplicative interactions of chronic sleep loss with acute sleep loss and circadian misalignment

Objectives: acute and chronic sleep loss and circadian timing interact such that, depending on their combination, small or very large performance decrements are observed in tasks of attention. Here, we tested whether such nonlinear interactions extend to a physiological measure of spontaneous visual attentional failures, indicating a fundamental principle of sleep-wake regulation. 

Methods: nine healthy volunteers completed an in-laboratory 3-week forced desynchrony protocol consisting of 12 consecutive 42.85-hour cycles with a sleep-wake ratio of 1:3.3. The protocol induced increasing chronic sleep loss, while extended wake (32.85 hours) and sleep episodes (10 hours) occurred at multiple circadian phases. Attentional failure rate was quantified from continuous electrooculograms (number of 30-second epochs with slow eye movements/h of wakefulness) as a function of time since scheduled wake (acute sleep loss), week of study (chronic sleep loss), and circadian (melatonin) phase. 

Results: during the first ∼8 hours awake, attentional failure rate was low, irrespective of the week. During the following wake hours, attentional failure rate increased steadily but at a faster rate in weeks 2 and 3 compared to week 1. The effects of acute and chronic sleep loss on attentional failure rate were magnified during the biological night compared to the biological day. 

Conclusions: a single extended sleep episode can only temporarily reverse attentional impairment associated with chronic sleep loss. Multiplicative effects of acute and chronic sleep loss—further amplified during the biological night—substantiate the interaction of 2 homeostatic response mechanisms and caution against underestimating their disproportionate combined impact on performance, health, and safety.

Acute sleep loss, Attentional failure, Chronic sleep loss, Circadian phase, Sleep homeostasis, Slow eye movements
2352-7218
Aeschbach, Daniel
38d78c5b-ea35-46ce-ad05-e81b2849e57b
Cohen, Daniel A.
b64e253f-d28c-4c36-8f3d-277a00c71e9b
Lockyer, Brandon J.
ff2c8c1d-a9b7-4cfe-9cf1-b6acfa6b4fdc
Chellappa, Sarah L.
516582b5-3cba-4644-86c9-14c91a4510f2
Klerman, Elizabeth B.
1dd2633f-ee36-4a1e-ac32-604763f3b7d1
Aeschbach, Daniel
38d78c5b-ea35-46ce-ad05-e81b2849e57b
Cohen, Daniel A.
b64e253f-d28c-4c36-8f3d-277a00c71e9b
Lockyer, Brandon J.
ff2c8c1d-a9b7-4cfe-9cf1-b6acfa6b4fdc
Chellappa, Sarah L.
516582b5-3cba-4644-86c9-14c91a4510f2
Klerman, Elizabeth B.
1dd2633f-ee36-4a1e-ac32-604763f3b7d1

Aeschbach, Daniel, Cohen, Daniel A., Lockyer, Brandon J., Chellappa, Sarah L. and Klerman, Elizabeth B. (2023) Spontaneous attentional failures reflect multiplicative interactions of chronic sleep loss with acute sleep loss and circadian misalignment. Sleep Health. (doi:10.1016/j.sleh.2023.07.013).

Record type: Article

Abstract

Objectives: acute and chronic sleep loss and circadian timing interact such that, depending on their combination, small or very large performance decrements are observed in tasks of attention. Here, we tested whether such nonlinear interactions extend to a physiological measure of spontaneous visual attentional failures, indicating a fundamental principle of sleep-wake regulation. 

Methods: nine healthy volunteers completed an in-laboratory 3-week forced desynchrony protocol consisting of 12 consecutive 42.85-hour cycles with a sleep-wake ratio of 1:3.3. The protocol induced increasing chronic sleep loss, while extended wake (32.85 hours) and sleep episodes (10 hours) occurred at multiple circadian phases. Attentional failure rate was quantified from continuous electrooculograms (number of 30-second epochs with slow eye movements/h of wakefulness) as a function of time since scheduled wake (acute sleep loss), week of study (chronic sleep loss), and circadian (melatonin) phase. 

Results: during the first ∼8 hours awake, attentional failure rate was low, irrespective of the week. During the following wake hours, attentional failure rate increased steadily but at a faster rate in weeks 2 and 3 compared to week 1. The effects of acute and chronic sleep loss on attentional failure rate were magnified during the biological night compared to the biological day. 

Conclusions: a single extended sleep episode can only temporarily reverse attentional impairment associated with chronic sleep loss. Multiplicative effects of acute and chronic sleep loss—further amplified during the biological night—substantiate the interaction of 2 homeostatic response mechanisms and caution against underestimating their disproportionate combined impact on performance, health, and safety.

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More information

Accepted/In Press date: 22 July 2023
e-pub ahead of print date: 7 September 2023
Keywords: Acute sleep loss, Attentional failure, Chronic sleep loss, Circadian phase, Sleep homeostasis, Slow eye movements

Identifiers

Local EPrints ID: 484815
URI: http://eprints.soton.ac.uk/id/eprint/484815
ISSN: 2352-7218
PURE UUID: 5ad91235-8366-40bf-b915-5ce3065d07dd
ORCID for Sarah L. Chellappa: ORCID iD orcid.org/0000-0002-6190-464X

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Date deposited: 22 Nov 2023 17:33
Last modified: 18 Mar 2024 04:12

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Contributors

Author: Daniel Aeschbach
Author: Daniel A. Cohen
Author: Brandon J. Lockyer
Author: Sarah L. Chellappa ORCID iD
Author: Elizabeth B. Klerman

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