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[Preprint]. 2024 Apr 16:2023.10.11.561858.
doi: 10.1101/2023.10.11.561858.

Adolescent chronic sleep restriction promotes alcohol drinking in adulthood: evidence from epidemiological and preclinical data

Oluwatomisin O Faniyan  1   2   3 , Daniele Marcotulli  4 , Reyila Simayi  1   5   3 , Federico Del Gallo  5   3 , Sara De Carlo  1   5   3 , Eleonora Ficiarà  5   3 , Doretta Caramaschi  6 , Rebecca Richmond  7 , Daniela Franchini  8 , Michele Bellesi  8   2   3 , Roberto Ciccocioppo  5   3 , Luisa de Vivo  5   3
Affiliations

Adolescent chronic sleep restriction promotes alcohol drinking in adulthood: evidence from epidemiological and preclinical data

Oluwatomisin O Faniyan et al. bioRxiv. .

Abstract

Epidemiological investigations have indicated that insufficient sleep is prevalent among adolescents, posing a globally underestimated health risk. Sleep fragmentation and sleep loss during adolescence have been linked to concurrent emotional dysregulation and an increase in impulsive, risk-taking behaviors, including a higher likelihood of substance abuse. Among the most widely used substances, alcohol stands as the primary risk factor for deaths and disability among individuals aged 15-49 worldwide. While the association between sleep loss and alcohol consumption during adolescence is well documented, the extent to which prior exposure to sleep loss in adolescence contributes to heightened alcohol use later in adulthood remains less clearly delineated. Here, we analyzed longitudinal epidemiological data spanning 9 years, from adolescence to adulthood, including 5497 participants of the Avon Longitudinal Study of Parents And Children cohort. Sleep and alcohol measures collected from interviews and questionnaires at 15 and 24 years of age were analyzed with multivariable linear regression and a cross-lagged autoregressive path model. Additionally, we employed a controlled preclinical experimental setting to investigate the causal relationship underlying the associations found in the human study and to assess comorbid behavioral alterations. Preclinical data were collected by sleep restricting Marchigian Sardinian alcohol preferring rats (msP, n=40) during adolescence and measuring voluntary alcohol drinking concurrently and in adulthood. Polysomnography was used to validate the efficacy of the sleep restriction procedure. Behavioral tests were used to assess anxiety, risky behavior, and despair. In humans, after adjusting for covariates, we found a cross-sectional association between all sleep parameters and alcohol consumption at 15 years of age but not at 24 years. Notably, alcohol consumption (Alcohol Use Disorder Identification Test for Consumption) at 24 years was predicted by insufficient sleep at 15 years whilst alcohol drinking at 15 years could not predict sleep problems at 24. In msP rats, adolescent chronic sleep restriction escalated alcohol consumption and led to increased propensity for risk-taking behavior in adolescence and adulthood. Our findings demonstrate that adolescent insufficient sleep causally contributes to higher adult alcohol consumption, potentially by promoting risky behavior.

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Figures

Figure 1.
Figure 1.. Cross-lagged panel model evaluating the cross-sectional and longitudinal association between sleep and alcohol.
Significant paths and relative estimates are in bold.
Figure 2.
Figure 2.. Experimental design, polysomnography, and alcohol and water consumption.
A) Experimental design for adolescent chronic sleep restriction (CSR) and yoked control (YC) groups. Each white rectangle represents 1 day of 6-hour bar rotation (Ctrl); each red rectangle represents 1 day of 20-hour bar rotation (CSR); yellow-gray rectangles represent recovery days during which rats could drink water and ethanol. CSR = chronic sleep restriction; YC = yoked controls; Ctrl = control; T1 and T2 indicate batteries of behavioral tests. B) Time spent in each physiological state, expressed as % of a 24-hour baseline, for the CSR group. Repeated measure ANOVA was performed on raw data (minutes), for NREM sleep Fday(1.789, 7.155)=13.11 p=0.0045; for REM sleep, Fday(2.23,10.25)=39.35 p<0.0001; for wake Fday(1.57, 7.21)=18.29 p=0.002. Dunnett’s multiple comparisons post hoc tests against baseline. C) Time spent in each physiological state, expressed as % of a 24-hour baseline, for the YC group. CSR = chronic sleep restriction; YC = yoked controls; Ctrl = control; rec = recovery. * p<0.05, ** p<0.01, *** p<0.001, **** p<0.0001. D) alcohol intake across the 6 cycles of sleep restriction, measured 30 minutes after presenting the 2 bottles (water and 10% ethanol). LME model Fgroup(1,38)=16.24 p=0.0003. Post hoc Šídák’s multiple comparisons test, cycle 3 adjusted p=0.0003, cycle 4 p=0.0027. E) average ethanol consumption, measured 30 minutes after bottle presentation, over 7 days of intermittent (1 day on, 1 day off) 2-bottle choice in adulthood, Mann Whitney test p=0.46. F) alcohol intake across the 6 cycles of sleep restriction, measured 10 hours after presenting the 2 bottles (water and 10% ethanol). LME model Fgroup(1,36)=15.59 p=0.0004. Post hoc Šídák’s multiple comparisons test, adjusted p value for cycle 2 p=0.0326, cycle 3 p=0.0155, and cycle 4 p=0.0078. G) average ethanol consumption, measured 10 hours after bottle presentation, over 7 days of intermittent (1 day on, 1 day off) 2-bottle choice in adulthood, Mann Whitney test p=0.03. H) water intake across the 6 cycles of sleep restriction, measured 30 minutes after presenting the bottles. LME model Fgroup(1,38)=0.55, p=0.46. I) water intake across the 6 cycles of sleep restriction, measured 10 hours after presenting the bottles. LME model Fgroup(1,38)=1.95, p=0.17. J) and K) average water consumption, measured 30 minutes (J) and 10 hours (K) after bottle presentation, over 7 days of intermittent (1 day on, 1 day off) 2-bottle choice in adulthood, Mann Whitney test p=0.91 and p=0.77. CSR group in red (N=22), YC group in blue (N=18). ns= not significant, * p<0.05, ** p<0.01, *** p<0.001.
Figure 3.
Figure 3.. Behavioral tests.
A) Open field test. Left, open field test shows a decline in total distance traveled from adolescence to adulthood in the YC group (N=18) but not in the CSR group (N=22). Two-way ANOVA found a main effect of age Fage(1,37)=6.976 p=0.012, and an interaction between age and group Fgroup × age(1,37)=4.35 p=0.043, which were confirmed by Šídák’s multiple comparisons post hoc tests, adolescent p=0.43, adult p=0.049, YC adolescent vs adult p=0.0053, CSR adolescent vs adult p=0.9. Right, time spent in the center of the open field. Two-way ANOVA found only an effect of age Fage(1,37)=17.30 p=0.0002, confirmed by Šídák’s multiple comparisons post hoc tests: YC p=0.057, CSR p=0.0015. B) Light-dark box. We found a trend towards shorter latency to enter the light box and longer time spent in the light box in CSR (N=9) relative to YC (N=10). p value for Mann-Whitney test displayed. C) Novelty Suppressed Feeding test. Left, food consumption in the arena, two-way repeated measure (rm) ANOVA Fgroup(1,37)=3.16 p=0.083, Fage(1,37)=3.04 p=0.089, Fage × group(1,37)=0.36 p=0.54. Right, food consumption in home-cage, two-way rmANOVA Fage(1,37)=56.37 p<0.0001, Fgroup(1,37)=0.2 p=0.6, Fage × group(1,37)=0.55 p=0.46, Šídák’s post hoc test for YC and CSR p<0.0001. D) Novelty Suppressed Feeding test. Left, latency to eat in the arena, two-way rmANOVA Fgroup(1,37)=13.35 p=0.0008, Fage(1,37)=0.01 p=0.9, Fage × group(1,37)=0.05 p=0.8. Šídák’s multiple comparisons post hoc tests, adolescent p=0.047, adult p=0.018. Right, latency to eat in the home cage, two-way rmANOVA Fgroup(1,37)=0.66 p=0.42, Fage(1,37)=5.74 p=0.022, Fage × group(1,37)=0.22 p=0.64. E) food consumption over a period of 24 hour, two-way rmANOVA Fgroup(1,13)=0.18 p=0.67, Fage(1,13)=165,9 p<0.0001, Fage × group(1,13)=3.5 p=0.083, Šídák’s post hoc test for YC (N=8) and CSR (N=7) p<0.0001. F) Measures of body weight during adolescence (left) and young adulthood (right), CSR N=22, YC N=18, Mann-Whitney p=0.22. G) Forced swim test. Right, time spent immobile, Mann-Whitney p=0.43. Left, latency to immobility Mann-Whitney p=0.48. YC= yoke controls; CSR= chronic sleep restriction; NSFT= novelty suppressed feeding test; ns= not significant, * p<0.05, ** p<0.01, ****p<0.0001. H Positive correlation between alcohol consumption and ambulatory distance in adult rats (N total=39; ρ=0.37 p=0.022). I) Correlation between the amount of alcohol consumed at 30 minutes and the latency to approach food in the arena in CSR adult rats (N=18; ρ=−0.59, p=0.01) and YC (N=16; ρ=0.49 p=0.054). J) and K) Longitudinal correlation between adolescent alcohol consumption and adult performance in the novelty suppressed feeding test (NSFT) (N= 34; ρ=−0.45 p=0.008 at 30 minutes left, ρ=−0.44 p=0.01 at 10 hours right). ρ= Spearman’s coefficient. For correlations with the latencies at the NSFT, rats that did not engage in food consumption during the test were removed from the analysis. YC=yoke controls; CSR = chronic sleep restriction.
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