Locus coeruleus activity while awake is associated with REM sleep quality in older individuals
Ekaterina Koshmanova, Alexandre Berger, Elise Beckers, Islay Campbell, Nasrin Mortazavi, Roya Sharifpour, Ilenia Paparella, Fermin Balda, Christian Berthomier, Christian Degueldre, Eric Salmon, Laurent Lamalle, Christine Bastin, Maxime Van Egroo, Christophe Phillips, Pierre Maquet, Fabienne Collette, Vincenzo Muto, Daphne Chylinski, Heidi I.L. Jacobs, Puneet Talwar, Siya Sherif, Gilles Vandewalle
Ekaterina Koshmanova, Alexandre Berger, Elise Beckers, Islay Campbell, Nasrin Mortazavi, Roya Sharifpour, Ilenia Paparella, Fermin Balda, Christian Berthomier, Christian Degueldre, Eric Salmon, Laurent Lamalle, Christine Bastin, Maxime Van Egroo, Christophe Phillips, Pierre Maquet, Fabienne Collette, Vincenzo Muto, Daphne Chylinski, Heidi I.L. Jacobs, Puneet Talwar, Siya Sherif, Gilles Vandewalle
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Clinical Research and Public Health Aging Neuroscience

Locus coeruleus activity while awake is associated with REM sleep quality in older individuals

Abstract

BACKGROUND The locus coeruleus (LC) is the primary source of norepinephrine in the brain and regulates arousal and sleep. Animal research shows that it plays important roles in the transition between sleep and wakefulness, and between slow wave sleep and rapid eye movement sleep (REMS). It is unclear, however, whether the activity of the LC predicts sleep variability in humans.METHODS We used 7-Tesla functional MRI, sleep electroencephalography (EEG), and a sleep questionnaire to test whether the LC activity during wakefulness was associated with sleep quality in 33 healthy younger (~22 years old; 28 women, 5 men) and 19 older (~61 years old; 14 women, 5 men) individuals.RESULTS We found that, in older but not in younger participants, higher LC activity, as probed during an auditory attentional task, was associated with worse subjective sleep quality and with lower power over the EEG theta band during REMS. The results remained robust even when accounting for the age-related changes in the integrity of the LC.CONCLUSION These findings suggest that LC activity correlates with the perception of the sleep quality and an essential oscillatory mode of REMS, and we found that the LC may be an important target in the treatment of sleep- and age-related diseases.FUNDING This work was supported by Fonds National de la Recherche Scientifique (FRS-FNRS, T.0242.19 & J. 0222.20), Action de Recherche Concertée – Fédération Wallonie-Bruxelles (ARC SLEEPDEM 17/27-09), Fondation Recherche Alzheimer (SAO-FRA 2019/0025), ULiège, and European Regional Development Fund (Radiomed & Biomed-Hub).

Authors

Ekaterina Koshmanova, Alexandre Berger, Elise Beckers, Islay Campbell, Nasrin Mortazavi, Roya Sharifpour, Ilenia Paparella, Fermin Balda, Christian Berthomier, Christian Degueldre, Eric Salmon, Laurent Lamalle, Christine Bastin, Maxime Van Egroo, Christophe Phillips, Pierre Maquet, Fabienne Collette, Vincenzo Muto, Daphne Chylinski, Heidi I.L. Jacobs, Puneet Talwar, Siya Sherif, Gilles Vandewalle

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Figure 1

Overview of the study protocol.

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Overview of the study protocol. (A) In total, 67 participants were recru...
(A) In total, 67 participants were recruited, of which 15 did not participate in the study, as they were excluded based on inclusion criteria, they did not complete the oddball task, or the MRI data did not pass the quality control. (B–D) All enrolled participants completed all the steps of the protocol detailed in B–D. (B) The volunteers completed a structural 7T MRI (sMRI) session including a sequence for the segmentation of the LC. The latter was used to create individual LC masks in each participant’s brain space, as shown in a representative participant (red, left LC; yellow, right LC) and to compute the LC contrast, reflecting the structural integrity of the LC. (C) Participants’ habitual baseline sleep data were recorded overnight in-lab under EEG before the fMRI session to extract our main objective sleep features of interest. They further provided a subjective evaluation of their habitual sleep quality using a validated questionnaire. (D) After the baseline night, participants underwent an fMRI session, during which they completed an auditory oddball task. Brain responses to the deviant tones are displayed as in ref. 29 over the group average brain structural image (top row; P < 0.001 uncorrected, t-values between 3.26 [red] and 8 [yellow]) and only over the group-wise template of the LC built based on individual LC masks (bottom row; P < 0.05 FWE corrected).