Deborah Suchecki
Peter Meerlo
T. John Wu- 1Department of Psychobiology, Escola Paulista de Medicina, Universidade Federal de São Paulo, São Paulo, Brazil
- 2Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, Netherlands
- 3Department of Gynecologic Surgery and Obstetrics, Uniformed Services University of the Health Sciences, Bethesda, MD, United States
Editorial on the Research Topic
The bidirectional relationship between sleep and neuroendocrinology
Sleep is a behavior implicated in numerous functions, from immunological competence to learning and memory (1–3). The activity of many neuroendocrine systems is dependent on the sleep-wake rhythm; sleep stimulates the release of anabolic hormones (1, 4, 5) and inhibits the secretion of catabolic ones, such as glucocorticoids (1, 6), whereas waking has the opposite effects. Conversely, peripheral hormones and neuropeptides modulate sleep under both basal and stressful conditions (7–9), indicating a complex bidirectional relationship between endocrine and sleep-wake regulations. Chronic impairment of sleep or reduction of sleep time may both be a cause and a consequence of disturbed endocrine activity, and together they can have profound effects on brain functions, cognition, and emotional regulation, both in humans (10, 11) and rodents (12–15).
This Research Topic of Frontiers in Endocrinology – Neuroendocrine Session – presents six original papers investigating the relationship between sleep and (neuro)endocrine influence on metabolic, immunological and cognitive functions. The study by Ma et al. explores the role of orexins in fear conditioning-induced sleep impairment employing anatomical, functional and pharmacologic techniques. They demonstrated that mice exposed to fear conditioning displayed impairment of both REM and NREM sleep and greater activation of orexin pathway to the ventrolateral preoptic area (VLPO). Activation of this orexinergic pathway by optogenetic manipulation, as well as infusion of orexin-A into the VLPO, led to similar sleep impairments.
Due to a combination of biological (late chronotype), social (e.g., early school start time) and technological exposure (e.g., internet, social media) factors, adolescents tend to compensate for the weekdays’ sleep debt on weekends. The difference in sleep time between weekdays and weekends is defined as social jet leg (SJL) (16, 17). In an epidemiological study, SJL was shown to lead to increased body mass index, in individuals aged between 16 and 65 years (18). In their study on Brazilian adolescents of both sexes, aged 9 to 15 years, Pompeia et al. investigated the impact of SJL on these adolescents’ cardiometabolic health. They found that girls are especially vulnerable to the effects of SJL on altering cardiovascular and metabolic markers. In a cohort of 352 adolescents of both sexes, 16- to 19-year-olds, plasma and salivary inflammatory cytokines and metabolic-related hormones were related to sleep parameters, such as bedtime (before or after midnight), sleep duration and SJL. Greater sleep debt and SJL had a major impacts on these parameters, increasing the levels of pro-inflammatory markers, as well as adiponectin and leptin (Alqaderi et al.).
Pre-clinical and clinical studies indicate that sleep disturbances and poor sleep quality (19) increase plasma levels of corticosterone (20–23) or cortisol (24, 25). Sexual dimorphism in cortisol levels is a well-known biological phenomenon, with women displaying higher cortisol levels throughout the day (26) and in response to challenges (27, 28). Likewise, insomnia shows sex differences and greater incidence is reported in women than men (29). Mazgelyté et al. reported a positive correlation between poorer subjective sleep quality and higher hair cortisol levels in a group of peri- and postmenopausal women, suggesting that poor sleep quality is connected to chronically elevated cortisol levels. Moreover, dysregulation of sex hormones, as seen in peri- and postmenopausal women, seems to be related to poor sleep quality and the overall stress load as shown in the accumulation of cortisol in hair over a period of time. Indeed, middle aged women who underwent oophorectomy displayed worse objective and subjective sleep than age-matched ovary-intact women. Hormone replacement therapy mitigated the sleep effects in the women who underwent oopphorectomy. In addition, increased sleep latency and reduced sleep efficiency were implicated in impaired declarative memory and reduced volume of the anterolateral entorhinal cortex.
The last paper in this volume sought to set apart the role of nocturnal hypoxemia on glycosylated hemoglobin in sleep apnea patients. Obstructive sleep apnea (OSA) is a sleep breathing disorder leading to metabolic syndrome (30). In Mahmoud et al. study, glycosylated hemoglobin was associated with reduced time of oxygen saturation, but not with apnea-hypopnea index, in OSA patients. This result suggests that nocturnal hypoxemia might be a risk factor for the development or worsening of diabetes in OSA patients.
Together, the studies included in this Research Topic demonstrate that poor or inadequate sleep impacts metabolic, immunological and cognitive functions, irrespective of age and sex, although females appear to be at greater risk of sleep-induced symptoms of metabolic syndrome.
Author contributions
DS: Writing – original draft, Writing – review & editing. PM: Writing – original draft, Writing – review & editing. TW: Writing – original draft, Writing – review & editing.
Acknowledgments
DS is the recipient of a Research Fellowship from CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, project # 392608/2019-2).
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.
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References
1. Meerlo P, Sgoifo A, Suchecki D. Restricted and disrupted sleep: Effects on autonomic function, neuroendocrine stress systems and stress responsivity. Sleep Med Rev (2008) 12(3):197–210. doi: 10.1016/j.smrv.2007.07.007
2. Van Cauter E, Holmback U, Knutson K, Leproult R, Miller A, Nedeltcheva A, et al. Impact of sleep and sleep loss on neuroendocrine and metabolic function. Horm Res (2007) 67 Suppl 1:2–9. doi: 10.1159/000097543
3. Walker MP, Stickgold R. Sleep-dependent learning and memory consolidation. Neuron (2004) 44(1):121–33. doi: 10.1016/j.neuron.2004.08.031
4. Spiegel K, Leproult R, Van Cauter E. Impact of sleep debt on metabolic and endocrine function. Lancet (1999) 354(9188):1435–9. doi: 10.1016/S0140-6736(99)01376-8
5. Van Cauter E. Slow wave sleep and release of growth hormone. JAMA (2000) 284(21):2717–8. doi: 10.1001/jama.284.21.2717
6. Balbo M, Leproult R, Van Cauter E. Impact of sleep and its disturbances on hypothalamo-pituitary-adrenal axis activity. Int J Endocrinol (2010) 2010:759234. doi: 10.1155/2010/759234
7. García-Borreguero D, Wehr TA, Larrosa O, Granizo JJ, Hardwick D, Chrousos GP, et al. Glucocorticoid replacement is permissive for rapid eye movement sleep and sleep consolidation in patients with adrenal insufficiency. J Clin Endocrinol Metab (2000) 85(11):4201–6. doi: 10.1210/jcem.85.11.6965
8. Gronfier C, Brandenberger G. Ultradian rhythms in pituitary and adrenal hormones: their relations to sleep. Sleep Med Rev (1998) 2(1):17–29. doi: 10.1016/s1087-0792(98)90051-x
9. Adamantidis A, de Lecea L. Physiological arousal: a role for hypothalamic systems. Cell Mol Life Sci (2008) 65(10):1475–88. doi: 10.1007/s00018-008-7521-8
10. Armstrong JM, Ruttle PL, Klein MH, Essex MJ, Benca RM. Associations of child insomnia, sleep movement, and their persistence with mental health symptoms in childhood and adolescence. Sleep (2014) 37(5):901–9. doi: 10.5665/sleep.3656
11. Baum KT, Desai A, Field J, Miller LE, Rausch J, Beebe DW. Sleep restriction worsens mood and emotion regulation in adolescents. J Child Psychol Psychiatry (2014) 55(2):180–90. doi: 10.1111/jcpp.12125
12. da Silva Rocha-Lopes J, MaChado RB, Suchecki D. Chronic REM sleep restriction in juvenile male rats induces anxiety-like behavior and alters monoamine systems in the amygdala and hippocampus. Mol Neurobiol (2018) 55(4):2884–96. doi: 10.1007/s12035-017-0541-3
13. Novati A, Hulshof HJ, Koolhaas JM, Lucassen PJ, Meerlo P. Chronic sleep restriction causes a decrease in hippocampal volume in adolescent rats, which is not explained by changes in glucocorticoid levels or neurogenesis. Neuroscience (2011) 190:145–55. doi: 10.1016/j.neuroscience.2011.06.027
14. Simionato NM, da Silva Rocha-Lopes J, MaChado RB, Suchecki D. Chronic rapid eye movement sleep restriction during juvenility has long-term effects on anxiety-like behaviour and neurotransmission of male Wistar rats. Pharmacol Biochem Behav (2022) 217:173410. doi: 10.1016/j.pbb.2022.173410
15. Murack M, Chandrasegaram R, Smith KB, Ah-Yen EG, Rheaume É, Malette-Guyon É, et al. Chronic sleep disruption induces depression-like behavior in adolescent male and female mice and sensitization of the hypothalamic-pituitary-adrenal axis in adolescent female mice. Behav Brain Res (2021) 399:113001. doi: 10.1016/j.bbr.2020.113001
16. Randler C, Vollmer C, Kalb N, Itzek-Greulich H. Breakpoints of time in bed, midpoint of sleep, and social jetlag from infancy to early adulthood. Sleep Med (2019) 57:80–6. doi: 10.1016/j.sleep.2019.01.023
17. Wittmann M, Dinich J, Merrow M, Roenneberg T. Social jetlag: misalignment of biological and social time. Chronobiol Int (2006) 23(1-2):497–509. doi: 10.1080/07420520500545979
18. Roenneberg T, Allebrandt KV, Merrow M, Vetter C. Social jetlag and obesity. Curr Biol (2012) 22(10):939–43. doi: 10.1016/j.cub.2012.03.038
19. Joo EY, Yoon CW, Koo DL, Kim D, Hong SB. Adverse effects of 24 hours of sleep deprivation on cognition and stress hormones. J Clin Neurol (2012) 8(2):146–50. doi: 10.3988/jcn.2012.8.2.146
20. Andersen ML, Martins PJ, D’Almeida V, Bignotto M, Tufik S. Endocrinological and catecholaminergic alterations during sleep deprivation and recovery in male rats. J Sleep Res (2005) 14(1):83–90. doi: 10.1111/j.1365-2869.2004.00428.x
21. Barf RP, Van Dijk G, Scheurink AJ, Hoffmann K, Novati A, Hulshof HJ, et al. Metabolic consequences of chronic sleep restriction in rats: Changes in body weight regulation and energy expenditure. Physiol Behav (2012) 107(3):322–8. doi: 10.1016/j.physbeh.2012.09.005
22. Moraes DA, MaChado RB, Koban M, Hoffman GE, Suchecki D. The pituitary-adrenal response to paradoxical sleep deprivation is similar to a psychological stressor, whereas the hypothalamic response is unique. Front Endocrinol (Lausanne) (2022) 13:885909. doi: 10.3389/fendo.2022.885909
23. Buban KN, Shupe EA, Rothwell SW, Wu TJ. Sex differences in the hypothalamic-pituitary-adrenal axis response following a single or multiple days of sleep restriction. Stress (2020) 23:1–10. doi: 10.1080/10253890.2019.1710488
24. Leproult R, Copinschi G, Buxton O, Van Cauter E. Sleep loss results in an elevation of cortisol levels the next evening. Sleep (1997) 20(10):865–70.
25. Carvalhaes-Neto N, Ramos LR, Suchecki D, Tufik S, Huayllas MK, Kater CE. The effect of hospitalization on the sleep pattern and on cortisol secretion of healthy elderly. Exp Aging Res (2003) 29(4):425–36. doi: 10.1080/03610730303702
26. Gunn PJ, Middleton B, Davies SK, Revell VL, Skene DJ. Sex differences in the circadian profiles of melatonin and cortisol in plasma and urine matrices under constant routine conditions. Chronobiol Int (2016) 33(1):39–50. doi: 10.3109/07420528.2015.1112396
27. Seeman TE, Singer B, Wilkinson CW, McEwen B. Gender differences in age-related changes in HPA axis reactivity. Psychoneuroendocrinology (2001) 26(3):225–40.
28. Kudielka BM, Buske-Kirschbaum A, Hellhammer DH, Kirschbaum C. HPA axis responses to laboratory psychosocial stress in healthy elderly adults, younger adults, and children: impact of age and gender. Psychoneuroendocrinology (2004) 29(1):83–98. doi: 10.1016/s0306-4530(02)00146-4
29. Zeng LN, Zong QQ, Yang Y, Zhang L, Xiang YF, Ng CH, et al. Gender difference in the prevalence of insomnia: A meta-analysis of observational studies. Front Psychiatry (2020) 11:577429. doi: 10.3389/fpsyt.2020.577429
Keywords: sleep, orexin, social jetlag, metabolic syndrome, inflammation, estrogen, insomnia, sleep apnea
Citation: Suchecki D, Meerlo P and Wu TJ (2024) Editorial: The bidirectional relationship between sleep and neuroendocrinology. Front. Endocrinol. 15:1372967. doi: 10.3389/fendo.2024.1372967
Received: 19 January 2024; Accepted: 22 January 2024;
Published: 26 January 2024.
Edited and Reviewed by:
Hubert Vaudry, Université de Rouen, FranceCopyright © 2024 Suchecki, Meerlo and Wu. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Deborah Suchecki, ZGVib3JhaC5zdWNoZWNraTIxQHVuaWZlc3AuYnI=