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. 2023 Mar 22;43(12):2168-2177.
doi: 10.1523/JNEUROSCI.0790-22.2023. Epub 2023 Feb 20.

Total Sleep Deprivation Increases Brain Age Prediction Reversibly in Multisite Samples of Young Healthy Adults

Congying Chu  1   2 , Sebastian C Holst  3   4 , Eva-Maria Elmenhorst  5   6 , Anna L Foerges  1   7 , Changhong Li  1 , Denise Lange  5 , Eva Hennecke  5 , Diego M Baur  4 , Simone Beer  1 , Felix Hoffstaedter  8   9 , Gitte M Knudsen  3   10 , Daniel Aeschbach  5   11   12   13 , Andreas Bauer  1   14 , Hans-Peter Landolt  4   15 , David Elmenhorst  16   17   18
Affiliations

Total Sleep Deprivation Increases Brain Age Prediction Reversibly in Multisite Samples of Young Healthy Adults

Congying Chu et al. J Neurosci. .

Abstract

Sleep loss pervasively affects the human brain at multiple levels. Age-related changes in several sleep characteristics indicate that reduced sleep quality is a frequent characteristic of aging. Conversely, sleep disruption may accelerate the aging process, yet it is not known what will happen to the age status of the brain if we can manipulate sleep conditions. To tackle this question, we used an approach of brain age to investigate whether sleep loss would cause age-related changes in the brain. We included MRI data of 134 healthy volunteers (mean chronological age of 25.3 between the age of 19 and 39 years, 42 females/92 males) from five datasets with different sleep conditions. Across three datasets with the condition of total sleep deprivation (>24 h of prolonged wakefulness), we consistently observed that total sleep deprivation increased brain age by 1-2 years regarding the group mean difference with the baseline. Interestingly, after one night of recovery sleep, brain age was not different from baseline. We also demonstrated the associations between the change in brain age after total sleep deprivation and the sleep variables measured during the recovery night. By contrast, brain age was not significantly changed by either acute (3 h time-in-bed for one night) or chronic partial sleep restriction (5 h time-in-bed for five continuous nights). Together, the convergent findings indicate that acute total sleep loss changes brain morphology in an aging-like direction in young participants and that these changes are reversible by recovery sleep.SIGNIFICANCE STATEMENT Sleep is fundamental for humans to maintain normal physical and psychological functions. Experimental sleep deprivation is a variable-controlling approach to engaging the brain among different sleep conditions for investigating the responses of the brain to sleep loss. Here, we quantified the response of the brain to sleep deprivation by using the change of brain age predictable with brain morphologic features. In three independent datasets, we consistently found increased brain age after total sleep deprivation, which was associated with the change in sleep variables. Moreover, no significant change in brain age was found after partial sleep deprivation in another two datasets. Our study provides new evidence to explain the brainwide effect of sleep loss in an aging-like direction.

Keywords: T1 MRI; brain age; sleep deprivation.

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Figures

Figure 1.
Figure 1.
A schematic diagram showing the analytic steps.
Figure 2.
Figure 2.
The schematic demonstration of the study protocol for each dataset. A, The experimental protocol for the Somnosafe dataset. A, Adaption day; B1 and B2, the two baseline days; E1–E5, five-night chronic sleep deprivation (the experimental group received 5 h TIB per night, the control group had 8 h TIB per night). B, The experimental protocol for the CSR dataset. C, The experimental protocol for the NRU dataset. B, Baseline day. D, The experimental protocol for the UZH dataset. Here, R, recovery night following TSD. E, The experimental protocol for the Stockholm dataset. PSD for one night (3 h TIB).
Figure 3.
Figure 3.
The effect of total sleep deprivation on the brain age. A–C, The predicted brain age of each participant is represented by a blue diamond. The change in brain age between a pair of experimental conditions, corresponding to the x-axis, is represented by a red diamond. The x-axis label (left) corresponds to the experimental sequence. B, Baseline condition. Green circles represent the means. Gray bars represent 95% CI; *p < 0.05, statistically significant (p ≥ 0.05, n.s.) via the paired sample t test. The 0 enclosed by a red box indicates no change between any two conditions. A, Left, The predicted brain age across three experimental conditions in the Somnosafe dataset. Right, Pairwise comparison of brain age change (TSD – B, t(33) = 3.3847, p = 0.0019, mean difference = 0.9361 years; TSD – R, t(33) = 2.9255, p = 0.0062, mean difference = 0.8959 years; R–B, t(33) = 0.1580, p = 0.8754, mean difference = 0.0402 years). B, Left, The predicted brain age across two experimental conditions in the NRU dataset. Right, Pairwise comparison of brain age change (TSD – B, t(19) = 3.2133, p = 0.0046, mean difference = 2.1255 years). C, Left, The predicted brain age across three experimental conditions in the UZH dataset. Right, Pairwise comparison of brain age change (TSD – B: t(19) = 2.3645, p = 0.0289, mean difference = 1.0739 years; TSD – R, t(19) = 2.2394, p = 0.0373, mean difference = 0.9497 years; R – B, t(19) = 0.4715, p = 0.6426, mean difference = 0.1241 years). D, The similarity between the T statistic maps derived from the paired t test between the data collected after the night of total sleep deprivation and the data collected after the baseline night. Left, Results were based on the comparison of gray matter volume in the three datasets. The similarity was assessed by using Pearson's correlation coefficient r as shown in each cell. Bottom, The exemplar slices of the T statistic maps are shown for each dataset. Right, The results were based on the comparison of white matter volume.
Figure 4.
Figure 4.
The effect of partial sleep deprivation on the brain. A, Left, The predicted brain age across three experimental conditions in the CSR dataset. B, baseline condition. Right, Pairwise comparison of brain age change. No significant effect was detected (PSD – B, t(14) = 0.7444, p = 0.4689, mean difference = 0.2546 years; PSD – R, t(14) = 0.9675, p = 0.3497, mean difference = 0.2176 years; R – B, t(14) = 0.1497, p = 0.8831, mean difference = 0.0370 years). B, Left, The predicted brain age across two experimental conditions in the Stockholm dataset. Right, Pairwise comparison of brain age change. No significant effect was detected (PSD – B, t(40) = −1.6969, p = 0.0975, mean difference = −0.4773 years).
Figure 5.
Figure 5.
The associations between the change of brain age and sleep behavior in the Somnosafe dataset. A–C, Δbrainage refers to the change of brain age (TSD – baseline), which is normalized by the corresponding chronological age. The horizontal red (blue) arrow points to the increased (decreased) brain age after TSD. Pearson's correlation coefficient (r) and p value are shown. The least-squares reference line (red dashed) is used to show the linear tendency for the correlation. A, The association between the KSS change (ΔKSS, TSD – baseline) and Δbrainage. B, The association between the normalized WT (TSD/baseline) in the recovery night following TSD and Δbrainage (1) is enclosed in a red box, which indicates equal WT between two conditions. C, The association between the normalized N1 in the recovery night following TSD and Δbrainage. N1 refers to the time spent in stage N1 sleep during sleep period time.
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References

    1. Abel T, Havekes R, Saletin JM, Walker MP (2013) Sleep, plasticity and memory from molecules to whole-brain networks. Curr Biol 23:R774–R788. 10.1016/j.cub.2013.07.025 - DOI - PMC - PubMed
    1. Akerstedt T, Gillberg M (1990) Subjective and objective sleepiness in the active individual. Int J Neurosci 52:29–37. - PubMed
    1. Akerstedt T, Lekander M, Nilsonne G, Tamm S, d'Onofrio P, Kecklund G, Fischer H, Schwarz J, Petrovic P, Mansson KNT (2020) Gray matter volume correlates of sleepiness: a voxel-based morphometry study in younger and older adults. Nat Sci Sleep 12:289–298. 10.2147/NSS.S240493 - DOI - PMC - PubMed
    1. Alkadhi K, Zagaar M, Alhaider I, Salim S, Aleisa A (2013) Neurobiological consequences of sleep deprivation. Curr Neuropharmacol 11:231–249. 10.2174/1570159X11311030001 - DOI - PMC - PubMed
    1. Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38:95–113. 10.1016/j.neuroimage.2007.07.007 - DOI - PubMed

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