Users Online: 393

Home Print this page Email this page Small font sizeDefault font sizeIncrease font size

Home | About us | Editorial board | Search | Ahead of print | Current issue | Archives | Submit article | Instructions | Subscribe | Contacts | Login 
     

   Table of Contents      
REVIEW ARTICLE
Year : 2021  |  Volume : 11  |  Issue : 1  |  Page : 17-26

Sleep and Gonadotrophin Hormones


1 Department of Pharmacology, JSS College of Pharmacy, JSS Academy of Higher Education & Research, Mysuru, India
2 Department of Pharmacology, JSS College of Pharmacy, JSS Academy of Higher Education & Research, Mysuru,Centre for Experimental Pharmacology and Toxicology, Central Animal Facility, JSS Academy of Higher Education & Research, Mysuru, India
3 Department of Physiology, Saveetha Medical College & Hospital, Thandalam, Chennai, India
4 Department of Traditional Food & Sensory Science, CSIR − Central Food Technological Research Institute (CFTRI), Mysuru, India
5 Centre for Biodiversity Research, Dhofar University, Salalah, Oman
6 Department of Food Science and Nutrition, CAMS, Sultan Qaboos University, Muscat, Oman
7 Department of Biochemistry, Panimalar Medical College Hospital and Research Institute, Chennai, India
8 Department of Biochemistry, Saveetha Dental College, Saveetha Institute of Medical and Technical Sciences, Saveetha University, Chennai, India
9 Department of Biomedical Sciences, School of Medicine, Nazarbayev University, Nur-Sultan City, Kazakhstan
10 Research and Policy Department, World Innovation Summit for Health (WISH), Foundation, Doha, Qatar

Date of Submission07-May-2020
Date of Decision30-Oct-2020
Date of Acceptance20-Nov-2020
Date of Web Publication12-Feb-2021

Correspondence Address:
MBA M. Walid Qoronfleh
Research and Policy Department, World Innovation Summit for Health (WISH), Qatar Foundation, P.O. Box 5825, Doha
Qatar
PhD, MBA Saravana Babu Chidambaram
Research and Policy Department, World Innovation Summit for Health (WISH), Qatar Foundation, P.O. Box 5825, Doha
India
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijnpnd.ijnpnd_97_20

Rights and Permissions
   Abstract 


Sleep plays a key role in neuroendocrine functioning and glucose metabolism. Currently existing data reveal that restriction of sleep duration results in adverse health effects. Sleep plays an imperative role in endocrine systems. Sleep causes the episodic secretion of gonadotrophin through modulation of neurotransmitters activity. Research on the significance of sex and gonadotrophic hormone in causing sleep disparities and its effects on cognition among men and women is gaining increased awareness. Epidemiologic, preclinical, and clinical studies have reported that sleep deprivation causes alteration of metabolic endocrine functions, including reduced glucose tolerance, insulin sensitivity, and leptin levels with increased cortisol and ghrelin levels. Men with lesser levels of testosterone and women with elevated levels of progesterone are more susceptible to the effects of sleep restriction on cognition and emotion processing tasks. The present integrative review highlights the effects of sleep deprivation on sex and gonadotrophin hormones and its link to cognitive function.

Keywords: Cognition, gonadotrophin hormones, sleep, sleep disorders


How to cite this article:
Shivalingaiah SB, Tuladhar S, Mahalakshmi AM, Muthukumar P, Yannam SK, Rashan L, Essa MM, Mohan SK, Veeraraghavan VP, Bolla SR, Chidambaram SB, Qoronfleh MW. Sleep and Gonadotrophin Hormones. Int J Nutr Pharmacol Neurol Dis 2021;11:17-26

How to cite this URL:
Shivalingaiah SB, Tuladhar S, Mahalakshmi AM, Muthukumar P, Yannam SK, Rashan L, Essa MM, Mohan SK, Veeraraghavan VP, Bolla SR, Chidambaram SB, Qoronfleh MW. Sleep and Gonadotrophin Hormones. Int J Nutr Pharmacol Neurol Dis [serial online] 2021 [cited 2021 May 8];11:17-26. Available from: https://www.ijnpnd.com/text.asp?2021/11/1/17/309287




   Introduction Top


Sleep is described as a reversible quiescent state of the body, phenotypically characterized by disengagement from the environment, postural recumbence, behavioral dormancy, and closed eyes. Sleep also plays an important role in thermoregulation, homeostatic control over endocrine cascades, preserving the functions of vital organs via toxins clearance, memory encoding, and consolidation. According to National Sleep Foundation, USA, 7 to 8 hour sleep is essential for maintaining good health.[1] Sleep is divided into two stages, rapid eye movement sleep (REM) and non-rapid eye movement sleep (NREM). The stages of sleep alternate throughout the night in a roughly 90 min cycle.[2],[3] During REM sleep, the brain will be active pertaining to the wake stage, although notable differences with respect to the regional patterns of activation have been reported in humans. The sleep cycle consists of 20 to 25% of REM sleep occurring in four to six discrete episodes.[4] NREM sleep comprises of 75% of total sleep time and consists of progressively deeper stages of sleep. N1 (stage 1), the lightest stage of sleep, between being awake and asleep, is also referred to as somnolence or drowsy sleep. In this stage, the muscles are quite active, and the eyes roll around slowly. The brain waves during stage 1 mainly shift from beta and gamma (frequency of 12–30 Hz and 25–100 Hz, respectively), to more synchronize but slower alpha waves (frequency of 8–13 Hz). N2 (stage 2) is the first unequivocal stage in which muscle activity is completely decreased. Brain waves during stage 2 are mainly in the theta wave range and characterized by two distinguishing phenomena: sleep spindles (also known as sigma waves) and K-complexes. N3 (stages 3 and 4) is a deep or slow-wave sleep and characterizes around 15 to 20% of total sleep time. During stage 3, brain waves are mainly in the delta wave range (with a frequency of around 0.5–4 Hz).[5]

Sleep deprivation (SD) is a common problem in modern society because of the change of lifestyle, screen time, and shift work. SD is a risk factor that contributes to the progression of several diseases by altering the behavioral, hormonal, and neurochemical pathways.[6],[7],[8] SD impairs brain functions and contributes significantly to the wear and tear of the physiological homeostasis.[9] It causes metabolic endocrinal dysfunctions, which, in turn, causes a reduction in body weight and increased food intake, an increase in anxiety, and a decrease in motor and cognitive performances.[10] Induction of SD for a period of 4 days in experimental rats is reported to cause a decrease in estrogen and testosterone and an increase in progesterone, prolactin, corticosterone, and catecholamine levels.[11] SD alters hypothalamic (suprachiasmatic nucleus) and pituitary (anterior) functions that, in turn, is linked to hormonal (including gonadotropin hormones), that is, hypothalamic–pituitary–gonadal axis (HPG)[12] and behavioral changes[13] [Figure 1]. Mounting evidences demonstrate a casual role of gonadotropin systems in Alzheimer disease and cognitive performance.[14],[15] Thus, it is evident that the vicious cycle between sleep–HPG axis–hormones affects cognitive functions.[16] This review is an attempt to summarize literatures reporting the adverse effects of sleep loss/SD on sex and gonadotropin hormones and associated cognitive function.
Figure 1 The synthesis of melatonin, thyroid-stimulating hormone (TSH), and cortisol, depending on circadian rhythm. The expression of cortisol, a steroid hormone produced in the adrenal gland, is tightly regulated by circadian rhythms in various mammals, including humans. The primary rhythm of this cycle is controlled by the suprachiasmatic nucleus (SCN), located in the hypothalamus. The secretion pattern of cortisol is coordinated by the hypothalamic–pituitary–adrenal (HPA) axis and the hippocampus. This HPA axis receives input from the SCN, from which it controls corticotrophin-releasing hormone (CRH) release in the paraventricular nucleus. From there, adrenocorticotrophic hormone (ACTH) is released from the corticotropes in the anterior pituitary by stimulating corticotrophin-releasing hormone (CRH). In normal individuals, cortisol levels fall to low or even undetectable levels around midnight, followed by peak expression around at 08:30

Click here to view


Sleep Disorders

A wide range of physiological and psychological factors causes dysregulation in the circadian regulation of sleep leading to impairment in daytime functioning.[17] The International Classification of Sleep Disorders differentiates several categories of sleep disorders, of which the most common include insomnia, narcolepsy, sleep-related breathing disorders (e.g., obstructive sleep apnea [OSA]), circadian rhythm disorders (e.g., delayed sleep phase disorder [DSPD]), advanced sleep phase disorder (ASPD), and sleep-related movement disorders (e.g., restless legs syndrome [RLS], periodic limb movement disorder [PLMD]).[11]

Sleep apnea

OSA, a disorder characterized by breathing disruption during sleep caused by airway occlusion. Sleep apnea increases in postmenopausal women, it has been suggested that gonadal hormones, particularly progesterone, might protect women from sleep-disordered breathing during the reproductive years.[18],[19] Several studies indicate that female hormones have a significant impact on the upper airway dilator muscle activity during sleep with a peak activity during the luteal phase, lower activity during the follicular phase, and lowest activity among postmenopausal women.[20] Estrogen has a beneficial role in preventing the development of OSA along with attenuating the associated comorbidities. It is possible that estrogen-mediated activation of p38 MAP kinase may inhibit HIF-1α to attenuate lung inflammation, which may inhibit the activation of vagal C fibers to attenuate bronchoconstriction and prevent obstruction during sleep. OSA is shown as a risk factor for erectile and sexual dysfunction in men. But, till date, there is no direct report showing the interaction between testosterone and OSA. However, testosterone replacement therapy is shown to worsen OSA in few reports.[21]

Insomnia

Insomnia, the inability to sleep with sufficient opportunity, is more prevalent in women than men. In women, insomnia may result from multifactorial issues, including hormonal changes associated with the menstrual cycle, pregnancy, postpartum, hot flashes associated with menopause, oral contraceptive use, psychiatric complaints (anxiety and depression), undiagnosed sleep disorders such as apnea, and/or lifestyle and environmental factors. In particular, hormonal changes during the late luteal phase of the menstrual cycle, third trimester of pregnancy, and menopause are strongly associated with women’s reports of insomnia.[22] Insomnia is comorbid with other disorders that are more prevalent in women, such as anxiety and depression, and exhibits a substantial sex disparity in women and men with bipolar disorder and stable coronary artery disease. In general, research suggests that women more frequently report subjective complaints of insomnia, yet show better sleep than men when evaluated on objective measures of sleep.[20] Low doses of testosterone are reported to affect sleep quality, whereas high doses affect sleep patterns and duration in men.[23]

Restless legs syndrome

RLS, also known as Willis–Ekbom disease, is a sensory-motor syndrome disorder that causes uncomfortable (painful) tingling and tugging sensations in the legs (or overwhelming urge to move the legs at rest.[24] It is less common but possible to have RLS symptoms in the arms, face, torso, and genital regions. More than 80% of people with RLS also experience a condition known as PLMD.[25] PLMD is characterized by involuntary leg twitching or jerking movements during sleep that typically occur every 15 to 40 seconds, sometimes throughout the night. The symptoms cause repeated awakening and severely disrupted sleep. RLS occurs in both men and women, although the incidence is about twice as high in women and has greater prevalence in pregnant women, who exhibit RLS at rates of between 11 and 23%.[26]

The putative causes for RLS include low levels of iron and/or dysfunction in basal ganglia circuits that use the neurotransmitter dopamine. RLS may also be related to chronic conditions such as kidney failure, diabetes, and peripheral neuropathy. The movement disorders appear to be more prevalent in women than men, presumably due to higher rates of anemia and increased risks associated with pregnancy in women. Increased estradiol levels during pregnancy are linked to RLS in women.[27] In the case of men, RLS is shown to be linked to erectile dysfunction,[28] which may be due to decreased testosterone levels. However, the biological link between RLS and testosterone has not been clarified yet.

Narcolepsy

Narcolepsy is a sleep disorder that is characterized by drowsiness during the day, sleep attacks, sleep paralysis, hallucinations, and, for some, sudden loss of muscle control (cataplexy). Narcolepsy with cataplexy has a known cause, related to a loss of cells in the brain that secrete hypocretin (also called orexin), which is important in the regulation of regulation wakefulness.[29] The International Classification of Sleep Disorders classifies narcolepsy into three types: narcolepsy with cataplexy, narcolepsy without cataplexy, and secondary narcolepsy. The major clinical manifestations of narcolepsy include narcoleptic sleep attacks (100%), cataplexy (60–70%), sleep paralysis (25–50%), hypnagogic hallucinations (20–40%), disturbed night sleep (70–80%), and automatic behavior (20–40%). In addition to the major manifestations, patients with narcolepsy may also have four important comorbid conditions, sleep apnea, periodic limb movements in sleep, REM behavior disorder (RBD), and nocturnal eating disorder.[30] No clear preclinical or clinical reports are available on the effects of estrogen and testosterone on narcolepsy.

Circadian rhythm disorders

Circadian misalignment occurs when the internal circadian clock is not properly aligned with the external environment, including light-dark, sleep-wake, and fasting feeding cycles.[31],[32] This condition can occur acutely with jet lag or on a chronic basis with shift work, delayed sleep phase, or advanced sleep phase disorders. Night shift work is an example of severe circadian misalignment, as workers are awake, active, and eating during their biological night and trying to sleep and fast during their biological day.[33]

Circadian rhythm sleep disorders include DSPD, ASPD, and non-24-hour (free-running type) sleep–wake disorder, as well as problems related to jet lag and shift work.[34] DSPD is the most common circadian rhythm disorder and results in a preferred sleep phase that may be delayed until after midnight and lasting until late morning. ASPD, which is more common in elderly patients, results in an advanced sleep phase such that individuals fall asleep in the early evening and wake in the early morning hours.[32] Non-24-hour sleep–wake disorder causes an individual to fall asleep approximately 1 to 2 hours later each consecutive day (hence, corresponding to a circadian cycle of 25–26 h).[35]

The evidence for hormonal involvement in circadian rhythm disorders is based on a large degree of differences noted in male and female circadian biology. Women spend more time in bed and sleep longer but report a poorer sleep quality than men. Several studies show that women exhibit phase-advanced rhythms (e.g., temperature and melatonin) such that circadian timing is shifted earlier in women than in men; hence, women tend to sleep longer than men.[9] The fact that women experience fluctuating levels of hormones throughout their reproductive lifespan has been proposed as a mechanism by which sleep and circadian disorders may occur more frequently in women than men.[36] Lastly, across both sexes, hormonal rhythms appear to be significantly delayed in patients with DSPD, and such circadian misalignments may adversely affect metabolic and hormonal factors such as circulating glucose and insulin levels.[37]

Sleep and Endocrine System

Sleep has an electrophysiological component and an endocrine component, that is, a distinct pattern of hormone secretion.[4] Both the electrophysiological and the hormonal components interact bidirectionally. The secretion of growth hormone (GH), prolactin, and thyrotropin (TSH) is increased during sleep, whereas the secretion of adrenocorticotrophic hormone and cortisol is decreased.[38] GH-releasing hormone is the main stimulatory neuropeptide that regulates GH release from the pituitary. Exogenous GH-releasing hormone stimulates sleep, especially, NREM sleep.[39]

The two major pathways by which sleep affects the release of hormones are the hypothalamic–pituitary axis and the autonomous nervous system. The release of hormones from the pituitary gland controls the secretion of other hormones from the peripheral endocrine glands that are markedly influenced by sleep. Modulation of pituitary-dependent hormonal release is partly mediated by hypothalamic-releasing and/or hypothalamic-inhibiting factors controlling pituitary function.[35] Physiologically hypothalamus and pituitary systems directly influence the hormone secretion from the gonadal organs (HPG axis) in both men and women.[38] SD is reported to derange the HPG axis and, which, in turn, forms the reasons for the altered hormonal secretion in sleep loss.[16]

During deep sleep, physiologically there will be a decrease in sympathetic drive and an increase in parasympathetic activity. Most of the endocrine organs are sensitive to the changes in sympathovagal balance.[40] Sleep loss is associated with an elevation of sympathovagal balance, with a higher sympathetic but lower parasympathetic tone. Well-documented examples are pancreatic insulin secretion and the release of leptin by the fat cells. In general, the endocrine alterations occurred during the sleepless night(s) were completely reversed during recovery sleep.[41]

The Mechanisms of Sleep Influence on Endocrine

The circadian influence on the endocrine begins from the photoreceptors of the retina. Light information from the retina is sent to the suprachiasmatic nucleus [SCN] of hypothalamus through the retinohypothalamic tract [Figure 2]. SCN is the pacemaker of the circadian rhythmicity by the endogenous stimuli of dark and light from the environment to the eye. Melatonin is produced by the pineal gland by the sympathetic fibers that travel from SCN to the paraventricular nucleus and then to thoracic spinal receptors that are located in SCN, Gonadotropin-Releasing Hormone (GnRH) neurons and TSH neurons of the hypothalamus, and pars tuberalis of the pituitary. The levels of melatonin receptors are also located in the ovaries. Melatonin attenuated oxidative stress in ovaries and improved the fertility of aged mice.[42] Nurses working in the night shift were found to have lesser levels of melatonin,[43] which would have an effect on their reproductive functions. Melatonin suppressed GnRH in cholestatic rats[44] but in a study on zebrafish, continuous dark conditions resulted in higher melatonin levels in the brain and ovary tissue, and melatonin was found to suppress gonadotropin inhibiting hormone.[45] These contradictory results warrant further research on the sleep, melatonin, and its possible implications in reproductive function.
Figure 2 Schematic representation of differences between the site of action of estrogenic and androgenic hormones on the suprachiasmatic nucleus (SCN). Testosterone can be aromatized into estradiol and thus may have dual androgenic/ estrogenic impacts on the system. The SCN regulates circadian timing in physiology and behavior by sending outputs to the neuroendocrine systems (reproduced from Mong et al., 2011, The Journal of Neuroscience)

Click here to view


Another possible mechanism is the circadian influence on lipid metabolism.[46] Sex steroids are made of lipids, so the circadian variances can influence the sex hormone synthesis.

Sleep and Hormones of Reproduction and Cognition

Long-term irregularities in the circadian clock increase the risk of sleep, metabolic, endocrine, psychological, and reproductive disorders.[47],[48] These disorders can further increase the risk of cardiovascular diseases[49] and certain cancers.[50]

Sleep disturbances can affect reproductive health and contribute to fertility disorders,[51] but the mechanism is not yet clearly elucidated. Different mechanisms are hypothesized from the studies of circadian clock influence on the reproductive hormones. The circadian clock regulates the cholesterol synthesis[52] that is required for steroidogenesis of sex hormones. These are again produced by the influence of gonadotropic hormones that are also influenced by the circadian clock. Thus, the circadian clock has a dual influence on the precursor required for steroidogenesis and regulate their release by influencing the GnRH. The SCN, the pacemaker of the circadian rhythm, also has receptors for these steroid hormones and plays a crucial role in the feedback mechanism of the steroid sex hormones and gonadotropins forming an important HPG axis. In a study on zebrafish in an ovarian cycle, the continuous dark condition resulted in increased melatonin and decreased gonadotropin inhibiting hormone and facilitated maturation of more oocytes, whereas in continuous light exposed fish, melatonin is reduced and gonadotropin inhibiting hormone is increased suppressing gonadotropins, and there were fewer mature oocytes, which indicates the role of melatonin in HPG axis.[45] Melatonin is produced from the pineal gland by the influence of the SCN-generated circadian rhythms by exposure to light and dark cycles.[53]

Women with normal cycles also demonstrate decreases in luteinizing hormone (LH) pulse frequency during sleep, most prominently in the early follicular phase. Sleep-related LH pulses were more likely to be associated with brief awakenings compared to REM and slow-wave sleep.[54] Differences in LH pulse frequency inhibitions were found in healthy women and polycystic ovary syndrome (PCOS) women but not due to the influence of the circadian clock.[55] Higher LH and higher body core temperature were associated with poor sleep quality.[56] A positive correlation of follicle stimulating hormone (FSH) levels with a longer duration of sleep was documented.[39] Menstrual cycle disturbances were reported in shift workers.[57] During the transition period of menopause, a more rapid rate of FSH change was associated with sleep complaints.[58],[59] The alterations in the sleep resulting in the altered melatonin levels influence the GnRH and thus the LH and FSH.

LH surge at the starting of the active period of the day under the influence of the SCN circadian clock is well known in rodents.[60] SCN signals GnRH-releasing system that results in the LH surge. In animal studies, SD resulted in low testosterone production, which is due to SD stress resulting in HPG axis disruption. Stress results in increased corticosteroid production by the adrenal gland that results in less testosterone production by Leydig cells.[61] Men with OSA had decreased LH and testosterone compared to healthy young men. Thus, it inferred that OSA resulted in decreased pituitary–gonad function. But this could be also due to the age and obesity of the OSA sample.[62]

Human studies have not yet confirmed a clear circadian link of the reproductive cycle. However, mutations of circadian genes resulting in miscarriage were reported[63] that is prevalent in flight attendants,[64] and circadian cyclical components in gonads suggest a possible link between conception and sleep disturbance. Disruption of the HPG axis has been seen in many animal studies. This disruption can also influence neurobehavioral modifications. Estrogen reduction in aging associated with cognitive deficits and loss of spine density in the prefrontal cortex and hippocampus is reported.[65],[66] Increase of LH and FSH is found in aging. Recently, increased peripheral LH and FSH have been found to correlate with amyloid beta, decline in cognition, and neurodegeneration.[67],[68] Further studies are needed to confirm the role of LH on CNS-related pathology.

Testosterone

Testosterone is mainly secreted during sleep. It is believed that the levels of testosterone keep on changing with the lowest concentrations during daytime and the highest at wake time.[69] Clinical studies in healthy men have shown that SD alters the circulation of androgens in blood.[10],[23],[70] A clinical study has shown that 5 hours of SD in healthy men reduced the testosterone levels in blood.[71] Shift workers were also reported to have lower levels of testosterone that were associated with disturbed sleep pattern.[72] The decrease in testosterone levels was associated with fatigue and alertness.[73] Also, it was reported that the decrease in the levels of testosterone due to SD could be attributed to the inhibition of Leydig cell steroidogenesis.[74] SD inhibits HPG axis that stimulates the release of corticosteroids. An increase in the corticosteroids activates hypothalamus–pituitary–adrenal axis that resulted in a decrease in testosterone levels.[75] Preclinical studies reported that SD altered the androgens and reduced the levels of testosterone.[76],[77],[78] Further, it was reported that SD affected the testosterone levels in both young and elderly. However, the effect was more prominent in elderly, suggesting an age-dependent effect.[77] It was also found that restoration of sleep after SD did not restore the levels of testosterone to baseline, thereby indicating that SD might cause a long-term effect of hormonal imbalance, at least testosterone.[79] The timing of SD also played a crucial role in lowering testosterone levels. SD in the early part of the night did not affect the testosterone levels, while early awakening and wakefulness in the second part of the night reduced testosterone levels.[80] Epidemiological studies showed that lower levels of testosterone were associated with cognitive deficits in elderly men.[81] Testosterone deprivation was found to reduce the spine density in the hippocampal region, modulated learning, and memory,[82] and increased the levels of anxiety in rats.[83] Lower levels of testosterone were associated with a higher risk of Alzheimer disease.[84] Preclinical and clinical studies reported that the decline in testosterone triggered the deposition of amyloid beta.[85],[86] Testosterone supplementation was reported to improve the cognitive functions in healthy elderly men.[87],[88] Animal studies also showed that exogenous administration of testosterone improved the spatial and working memory in rats.[89],[90],[91] These data revealed that decrease in the testosterone levels followed by SD is responsible for the cognitive dysfunction.

Progesterone

Progesterone regulates the process of the uterine lining and it is essential for implantation and maintenance of pregnancy. Low levels of progesterone might be an index of luteal phase dysfunction. Four-day SD in rats showed higher levels of progesterone.[92],[93] The increase in the levels of progesterone was correlated with an increase in corticosterone, indicating that SD activated hypothalamus–pituitary–adrenal axis that, in turn, might be responsible for fluctuations in progesterone levels.[93],[94] Persengiev et al.[95] showed that chronic SD in rats increases the plasma progesterone levels as well as the release of melatonin suggesting an interaction between the steroid hormones. Increased levels of progesterone were reported to alter mood and cognition.[96],[97] Progesterone potentiates emotional memory and exogenous administration of progesterone was found to increase the activity of the right amygdala of healthy women, thereby affecting memory processing in other regions of the brain.[98],[99]

Thyroid-stimulating hormone

Sleep has an inhibitory effect on the production of thyroid-stimulating hormone (TSH) secreted from the pituitary.[100] In a few preclinical and clinical studies, it was found that acute SD increased the levels of TSH and free T4 and T3.[101],[102] However, chronic sleep restriction in healthy female subjects resulted in lower levels of TSH and T4.[103] Further, chronic SD in rats also showed a progressive decline in TSH levels[104] suggesting that sleep loss can interfere with the synthesis and secretion of the hormones. Alterations in the level of TSH were found to affect mood and cognitive functions. Wahlin et al.[105] reported that the decline in the cognitive performance of adults is associated with lower levels of TSH. The decrease in the levels of TSH was found to contribute to the progression of Alzheimer disease.[106],[107] Further, normalizing the levels of TSH was found to improve the cognitive functions.[108]

Estradiol

SD modulates hormone release by altering the hormonal–neurochemical mechanism.[109] Estradiol is the pri­mary estrogen regulating the activities of FSH and LH. Sleep has been found to be critical for the secretion of estradiol. Gruchala et al.[110] reported that women having better sleep hygiene had higher levels of estradiol. In a clinical study, it was observed that SD increased the levels of estradiol.[111] Higher levels of estradiol were observed in women with an altered sleep cycle and sleep quality.[53] Decreased levels of estradiol resulted in a complex interaction between gonadal hormones and neuronal signaling processes.[112] Reduced level of estradiol contributes to stress effects. In women, reduced level of estradiol was associated with depression, anxiety, panic disorders, and reduced levels of cognitive dysfunction.[87] Estradiols were shown to possess neuroprotective effects[113] and was also shown to affect cognitive function. Reduced levels resulted in impairment of hippocampal synaptic plasticity in rats.[114] Accumulating evidences from both clinical and preclinical experiments indicated that estradiol might further affect memory and the learning processes. Because long-term potentiation (LTP) is generally an accepted electrophysiological model for the assessment of memory, it might be useful to probe the functional variations generated by altering the levels of estradiol. The abovementioned method was observed to be particularly effective because the induction of LTP is dependent on N-methyl-D-aspartate (NMDA) receptor activation that, in turn, is further increased by treatment with estradiol.[115],[116]


   Conclusion Top


The current review contributes to understanding the role of gonadotrophin hormones of both sexes in normal sleep phenomena, the individual vulnerability to sleep loss, and the associated comorbidities. Existing literature has shown that gonadotrophin hormones play a vital in regulating the hypothalamic activity of aging and hippocampal neuronal homeostasis. The gonadotrophins might thus represent a potential strategy for sleep-related health problems. A novel observation of the current review signifies the role of female sex hormones and phases of the menstrual cycle in sleep loss. SD prolongs the estrous cycle and increases the testosterone levels in the brain hippocampus. Gonadotrophin releasing hormone is abundantly expressed in the female hippocampus and increases the estrogen and testosterone levels. Gonadotrophins are therefore anticipated to enhance LTP. Progesterone emerged as a strong predictor of performance in women, highlighting the luteal phase of the menstrual cycle as a vulnerability period for emotional processing deficits, following SD. Among the men and women, the influences are varied with regard to the role of gonadotrophin and sex hormones in sleep and circadian rhythms on the quality of sleep.

Acknowledgment

The authors sincerely acknowledge their respective management and authorities for providing the required infrastructure for this review preparation. The language and technical editing support provided by The Editing Refinery, MD, USA is highly acknowledged.

Financial support and sponsorship

Nil.

Conflicts of interest

The authors reported no conflicts of interest.



 
   References Top

1.
National Sleep Foundation. 2015. Available from: https://www.sleepfoundation.org/ [Accessed on 25/12/2019].  Back to cited text no. 1
    
2.
Bhat A, Pires AS, Tan V, Babu Chidambaram S, Guillemin GJ. Effects of sleep deprivation on the tryptophan metabolism. Int J Tryptophan Res 2020;13:1178646920970902.  Back to cited text no. 2
    
3.
Colten HR, Altevogt BM. Sleep Disorders and Sleep Deprivation: An Unmet Public Health Problem. Washington, DC: National Academies Press (US); 2006 pp. 33-54.  Back to cited text no. 3
    
4.
Gil-Lozano M, Hunter PM, Behan L-A, Gladanac B, Casper RF, Brubaker PL. Short-term sleep deprivation with nocturnal light exposure alters time-dependent glucagon-like peptide-1 and insulin secretion in male volunteers. Am J Physiol Endocrinol Metab 2016;310:E41-50.  Back to cited text no. 4
    
5.
Fogel S, Martin N, Lafortune M et al. NREM sleep oscillations and brain plasticity in aging. Front Neurol 2012;3:176.  Back to cited text no. 5
    
6.
Bishir M, Bhat A, Essa MM, Ekpo O, Ihunwo AO, Veeraraghavan VP et al. Sleep deprivation and neurological disorders. BioMed Res Int 2020;2020:1-19.  Back to cited text no. 6
    
7.
Andersen ML, Martins PJF, D’Almeida V, Santos RF, Bignotto M, Tufik S. Effects of paradoxical sleep deprivation on blood parameters associated with cardiovascular risk in aged rats. Exp Gerontol 2004;39:817-24.  Back to cited text no. 7
    
8.
Ayas NT, White DP, Manson JE et al. A prospective study of sleep duration and coronary heart disease in women. Arch Intern Med 2003;163:205-9.  Back to cited text no. 8
    
9.
Kim TW, Jeong J-H, Hong S-C. The impact of sleep and circadian disturbance on hormones and metabolism. Int J Endocrinol 2015;2015:591729.  Back to cited text no. 9
    
10.
Benedito MA, Camarini R. Rapid eye movement sleep deprivation induces an increase in acetylcholinesterase activity in discrete rat brain regions. Braz J Med Biol Res 2001 34:103-9.  Back to cited text no. 10
    
11.
Deurveilher S, Rusak B, Semba K. Estradiol and progesterone modulate spontaneous sleep patterns and recovery from sleep deprivation in ovariectomized rats. Sleep 2009;32:865-77.  Back to cited text no. 11
    
12.
Mohammadi H, Rezaei M, Faghihi F, Khazaie H. Hypothalamic-pituitary-gonadal activity in paradoxical and psychophysiological insomnia. J Med Signals Sens 2019;9:59-67.  Back to cited text no. 12
[PUBMED]  [Full text]  
13.
Klumpers UMH, Veltman DJ, van Tol M-J et al. Neurophysiological effects of sleep deprivation in healthy adults, a pilot study. PLoS One 2015;10:e0116906.  Back to cited text no. 13
    
14.
Gurvich C, Hoy K, Thomas N, Kulkarni J. Sex differences and the influence of sex hormones on cognition through adulthood and the aging process. Brain Sci 2018;8:163.  Back to cited text no. 14
    
15.
Maggi R. Physiology of gonadotropin-releasing hormone (GNRH): beyond the control of reproductive functions. MOJ Anat Physiol 2016;2:150-4.  Back to cited text no. 15
    
16.
Hagewoud R, Bultsma LJ, Barf RP, Koolhaas JM, Meerlo P. Sleep deprivation impairs contextual fear conditioning and attenuates subsequent behavioural, endocrine and neuronal responses. J Sleep Res 2011;20:259-66.  Back to cited text no. 16
    
17.
Chokroverty S. Overview of sleep & sleep disorders. Indian J Med Res 2010;131:126-40.  Back to cited text no. 17
[PUBMED]  [Full text]  
18.
Sahithi AST, Muthu T, Saraswathy R. Migraine: Update and future perspectives. Int J Nutr Pharmacol Neurol Dis 2020;10:179.  Back to cited text no. 18
  [Full text]  
19.
Entzian P, Linnemann K, Schlaak M, Zabel P. Obstructive sleep apnea syndrome and circadian rhythms of hormones and cytokines. Am J Respir Crit Care Med 1996;153:1080-6.  Back to cited text no. 19
    
20.
Jehan S, Masters-Isarilov A, Salifu I et al. Sleep disorders in postmenopausal women. J Sleep Disord Ther 2015;4:1000212.  Back to cited text no. 20
    
21.
Liu PY, Yee B, Wishart SM et al. The short-term effects of high-dose testosterone on sleep, breathing, and function in older men. J Clin Endocrinol Metab 2003;88:3605-13.  Back to cited text no. 21
    
22.
Pavlova MK, Latreille V. Sleep disorders. Am J Med 2019;132:292-9.  Back to cited text no. 22
    
23.
Wittert G. The relationship between sleep disorders and testosterone in men. Asian J Androl 2014;16:262-5.  Back to cited text no. 23
[PUBMED]  [Full text]  
24.
Guo S, Huang J, Jiang H et al. Restless legs syndrome: from pathophysiology to clinical diagnosis and management. Front Aging Neurosci 2017;9:171.  Back to cited text no. 24
    
25.
Medic G, Wille M, Hemels ME. Short- and long-term health consequences of sleep disruption. Nat Sci Sleep 2017;9:151-61.  Back to cited text no. 25
    
26.
Eichling PS, Sahni J. Menopause related sleep disorders. J Clin Sleep Med 2005;1:291-300.  Back to cited text no. 26
    
27.
Dzaja A, Wehrle R, Lancel M, Pollmächer T. Elevated estradiol plasma levels in women with restless legs during pregnancy. Sleep 2009;32:169-74.  Back to cited text no. 27
    
28.
Cho JW, Duffy JF. Sleep, sleep disorders, and sexual dysfunction. World J Mens Health 2019;37:261-75.  Back to cited text no. 28
    
29.
Akintomide GS, Rickards H. Narcolepsy: a review. Neuropsychiatr Dis Treat 2011;7:507-18.  Back to cited text no. 29
    
30.
Kiley JP, Twery MJ, Gibbons GH. The National Center on Sleep Disorders Research—progress and promise. Sleep 2019;42:zsz105.  Back to cited text no. 30
    
31.
Kumaravel P, Subash S, Seethalakshmi KS, Murugan N, Yuvarajan R, Subramanian P. Monosodium glutamate modulates the circadian rhythms of biochemical variables and behavioral activity in rats under constant light. Int J Nutr Pharmacol Neurol Dis 2012;2:251.  Back to cited text no. 31
  [Full text]  
32.
Czeisler CA, Klerman EB. Circadian and sleep-dependent regulation of hormone release in humans. Recent Prog Horm Res 1999;54:97-130.  Back to cited text no. 32
    
33.
Copinschi G, Cauter EV. Effects of ageing on modulation of hormonal secretions by sleep and circadian rhythmicity. Horm Res 1995;43:20-24.  Back to cited text no. 33
    
34.
Leproult R, Van Cauter E. Role of sleep and sleep loss in hormonal release and metabolism. Endocr Dev 2010;17:11-21.  Back to cited text no. 34
    
35.
Kische H, Ewert R, Fietze I et al. Sex Hormones and sleep in men and women from the general population: a cross-sectional observational study. J Clin Endocrinol Metab 2016;101:3968-77.  Back to cited text no. 35
    
36.
Challet E. Keeping circadian time with hormones. Diabetes Obesity Metab 2015;17:76-83.  Back to cited text no. 36
    
37.
Mong JA, Baker FC, Mahoney MM et al. Sleep, rhythms, and the endocrine brain: influence of sex and gonadal hormones. J Neurosci 2011;31:16107-16.  Back to cited text no. 37
    
38.
Gómez‐González B, Domínguez‐Salazar E, Hurtado‐Alvarado G et al. Role of sleep in the regulation of the immune system and the pituitary hormones. Ann N Y Acad Sci 2012;1261:97-106.  Back to cited text no. 38
    
39.
Touzet S, Rabilloud M, Boehringer H, Barranco E, Ecochard R. Relationship between sleep and secretion of gonadotropin and ovarian hormones in women with normal cycles. Fertil Steril 2002;77:738-44.  Back to cited text no. 39
    
40.
Trinder J, Kleiman J, Carrington M et al. Autonomic activity during human sleep as a function of time and sleep stage. J Sleep Res 2001;10:253-64.  Back to cited text no. 40
    
41.
Lanfranco F, Motta G, Minetto MA et al. Neuroendocrine alterations in obese patients with sleep apnea syndrome. Int J Endocrinol 2010;2010:e474518.  Back to cited text no. 41
    
42.
Song C, Peng W, Yin S et al. Melatonin improves age-induced fertility decline and attenuates ovarian mitochondrial oxidative stress in mice. Sci Rep 2016;6:1-15.  Back to cited text no. 42
    
43.
Razavi P, Devore EE, Bajaj A et al. Shift work, chronotype, and melatonin rhythm in nurses. Cancer Epidemiol Biomarkers Prev 2019;28:1177-86.  Back to cited text no. 43
    
44.
McMillin M, DeMorrow S, Glaser S et al. Melatonin inhibits hypothalamic gonadotropin-releasing hormone release and reduces biliary hyperplasia and fibrosis in cholestatic rats. Am J Physiol Gastrointest Liver Physiol 2017;313:G410-8.  Back to cited text no. 44
    
45.
Yumnamcha T, Khan ZA, Rajiv C et al. Interaction of melatonin and gonadotropin-inhibitory hormone on the zebrafish brain-pituitary-reproductive axis. Mol Reprod Dev 2017;84:389-400.  Back to cited text no. 45
    
46.
Gooley JJ. Circadian regulation of lipid metabolism. Proc Nutr Soc 2016;75:440-50.  Back to cited text no. 46
    
47.
Priya S, Mahalakshmi AM, Tuladhar S, Ray B, Sushmitha BS, Shivashree S et al. Sleep and Body Fluids. Int J Nutr Pharmacol Neurol Dis 2020;10:65.  Back to cited text no. 47
  [Full text]  
48.
Khan S, Nabi G, Yao L et al. Health risks associated with genetic alterations in internal clock system by external factors. Int J Biol Sci 2018;14:791-8.  Back to cited text no. 48
    
49.
Nagai M, Hoshide S, Kario K. Sleep duration as a risk factor for cardiovascular disease- a review of the recent literature. Curr Cardiol Rev 2010;6:54-61.  Back to cited text no. 49
    
50.
Chen Y, Tan F, Wei L et al. Sleep duration and the risk of cancer: a systematic review and meta-analysis including dose–response relationship. BMC Cancer 2018;18:1149.  Back to cited text no. 50
    
51.
Kloss JD, Perlis ML, Zamzow JA, Culnan EJ, Gracia CR. Sleep, sleep disturbance, and fertility in women. Sleep Med Rev 2015;22:78-87.  Back to cited text no. 51
    
52.
Urlep Z, Rozman D. The interplay between circadian system, cholesterol synthesis, and steroidogenesis affects various aspects of female reproduction. Front Endocrinol 2013;4:111  Back to cited text no. 52
    
53.
Schwartz MD, Wotus C, Liu T et al. Dissociation of circadian and light inhibition of melatonin release through forced desynchronization in the rat. Proc Natl Acad Sci USA 2009;106:17540-5.  Back to cited text no. 53
    
54.
Hall JE, Sullivan JP, Richardson GS. Brief wake episodes modulate sleep-inhibited luteinizing hormone secretion in the early follicular phase. J Clin Endocrinol Metab 2005;90:2050-5.  Back to cited text no. 54
    
55.
Lu C, Hutchens EG, Farhy LS, Bonner HG, Suratt PM, McCartney CR. Influence of sleep stage on lh pulse initiation in the normal late follicular phase and in polycystic ovary syndrome. Neuroendocrinology 2018;107:60-72.  Back to cited text no. 55
    
56.
Murphy PJ, Campbell SS. Sex hormones, sleep, and core body temperature in older postmenopausal women. Sleep 2007;30:1788-94.  Back to cited text no. 56
    
57.
Stocker LJ, Macklon NS, Cheong YC, Bewley SJ. Influence of shift work on early reproductive outcomes: a systematic review and meta-analysis. Obstet Gynecol 2014;124:99-110.  Back to cited text no. 57
    
58.
Sowers MF, Zheng H, Kravitz HM et al. Sex steroid hormone profiles are related to sleep measures from polysomnography and the Pittsburgh Sleep Quality Index. Sleep 2008;31:1339-49.  Back to cited text no. 58
    
59.
Baker FC, de Zambotti M, Colrain IM, Bei B. Sleep problems during the menopausal transition: prevalence, impact, and management challenges. Nat Sci Sleep 2018;10:73-95.  Back to cited text no. 59
    
60.
Williams III WP, Kriegsfeld LJ. Circadian control of neuroendocrine circuits regulating female reproductive function. Front Endocrinol 2012;3:60.  Back to cited text no. 60
    
61.
Sapolsky RM. Stress-induced suppression of testicular function in the wild baboon: role of glucocorticoids. Endocrinology 1985;116:2273-8.  Back to cited text no. 61
    
62.
Luboshitzky R, Lavie L, Shen-Orr Z, Herer P. Altered luteinizing hormone and testosterone secretion in middle-aged obese men with obstructive sleep apnea. Obes Res 2005;13:780-6.  Back to cited text no. 62
    
63.
Hodžić A, Lavtar P, Ristanović M, Novaković I, Dotlić J, Peterlin B. Genetic variation in the CLOCK gene is associated with idiopathic recurrent spontaneous abortion. PLoS One 2018;13:e0196345.  Back to cited text no. 63
    
64.
Grajewski B, Whelan EA, Lawson CC et al. Miscarriage among flight attendants. Epidemiology 2015;26:192-203.  Back to cited text no. 64
    
65.
Bloss EB, Puri R, Yuk F et al. Morphological and molecular changes in aging rat prelimbic prefrontal cortical synapses. Neurobiol Aging 2013;34:200-10.  Back to cited text no. 65
    
66.
Wallace M, Luine V, Arellanos A, Frankfurt M. Ovariectomized rats show decreased recognition memory and spine density in the hippocampus and prefrontal cortex. Brain Res 2006;1126:176-82.  Back to cited text no. 66
    
67.
Short RA, O’Brien PC, Graff-Radford NR, Bowen RL. Elevated gonadotropin levels in patients with Alzheimer disease. Mayo Clin Proc 2001;76:906-9.  Back to cited text no. 67
    
68.
Verdile G, Laws SM, Henley D et al. Associations between gonadotropins, testosterone and β amyloid in men at risk of Alzheimer’s disease. Mol Psychiatry 2014;19:69-75.  Back to cited text no. 68
    
69.
Long N, Nguyen L, Stevermer J. PURLs: it’s time to reconsider early-morning testosterone tests. J Fam Pract 2015;64:418-9.  Back to cited text no. 69
    
70.
Abu-Samak MS, Mohammad BA, Abu-Taha MI, Hasoun LZ, Awwad SH. Associations between sleep deprivation and salivary testosterone levels in male university students: a prospective cohort study. Am J Mens Health 2018;12:411-9.  Back to cited text no. 70
    
71.
Leproult R, Cauter EV. Effect of 1 week of sleep restriction on testosterone levels in young healthy men. JAMA 2011;305:2173-4.  Back to cited text no. 71
    
72.
Axelsson J, Akerstedt T, Kecklund G, Lindqvist A, Attefors R. Hormonal changes in satisfied and dissatisfied shift workers across a shift cycle. J Appl Physiol 2003;95:2099-105.  Back to cited text no. 72
    
73.
Horstman AM, Dillon EL, Urban RJ, Sheffield-Moore M. The role of androgens and estrogens on healthy aging and longevity. J Gerontol A Biol Sci Med Sci 2012;67:1140-52.  Back to cited text no. 73
    
74.
Lee DS, Choi JB, Sohn DW. Impact of sleep deprivation on the hypothalamic-pituitary-gonadal axis and erectile tissue. J Sex Med 2019;16:5-16.  Back to cited text no. 74
    
75.
Choi JH, Lee SH, Bae JH et al. Effect of sleep deprivation on the male reproductive system in rats. J Korean Med Sci 2016;31:1624-30.  Back to cited text no. 75
    
76.
Andersen ML, Bignotto M, Machado RB, Tufik S. Does paradoxical sleep deprivation and cocaine induce penile erection and ejaculation in old rats? Addict Biol 2002;7:285-90.  Back to cited text no. 76
    
77.
Oh MM, Kim JW, Jin MH, Kim JJ, Moon DG. Influence of paradoxical sleep deprivation and sleep recovery on testosterone level in rats of different ages. Asian J Androl 2012;14:330-4.  Back to cited text no. 77
    
78.
Suchecki D, Tufik S. Social stability attenuates the stress in the modified multiple platform method for paradoxical sleep deprivation in the rat. Physiol Behav 2000;68:309-16.  Back to cited text no. 78
    
79.
Andersen ML, Martins PJF, D’Almeida V, Bignotto M, Tufik S. Endocrinological and catecholaminergic alterations during sleep deprivation and recovery in male rats. J Sleep Res 2005;14:83-90.  Back to cited text no. 79
    
80.
Schmid SM, Hallschmid M, Jauch-Chara K, Lehnert H, Schultes B. Sleep timing may modulate the effect of sleep loss on testosterone. Clin Endocrinol 2012;77:749-54.  Back to cited text no. 80
    
81.
Moffat SD, Zonderman AB, Metter EJ, Blackman MR, Harman SM, Resnick SM. Longitudinal assessment of serum free testosterone concentration predicts memory performance and cognitive status in elderly men. J Clin Endocrinol Metab 2002;87:5001-7.  Back to cited text no. 81
    
82.
Bussiere JR, Beer TM, Neiss MB, Janowsky JS. Androgen deprivation impairs memory in older men. Behav Neurosci 2005;119:1429-37.  Back to cited text no. 82
    
83.
Frye CA, Seliga AM. Testosterone increases analgesia, anxiolysis, and cognitive performance of male rats. Cogn Affect Behav Neurosci 2001;1:371-81.  Back to cited text no. 83
    
84.
Hogervorst E, Bandelow S. The controversy over levels of sex steroids in cases with Alzheimer’s disease. J Neuroendocrinol 2004;16:93-4.  Back to cited text no. 84
    
85.
Almeida OP, Waterreus A, Spry N, Flicker L, Martins RN. One year follow-up study of the association between chemical castration, sex hormones, beta-amyloid, memory and depression in men. Psychoneuroendocrinology 2004;29:1071-81.  Back to cited text no. 85
    
86.
Ramsden M, Nyborg AC, Murphy MP et al. Androgens modulate beta-amyloid levels in male rat brain. J Neurochem 2003;87:1052-5.  Back to cited text no. 86
    
87.
Cherrier MM, Matsumoto AM, Amory JK et al. The role of aromatization in testosterone supplementation: effects on cognition in older men. Neurology 2005;64:290-6.  Back to cited text no. 87
    
88.
Cherrier MM, Asthana S, Plymate S et al. Testosterone supplementation improves spatial and verbal memory in healthy older men. Neurology 2001;57:80-88.  Back to cited text no. 88
    
89.
Bimonte-Nelson HA, Singleton RS, Nelson ME et al. Testosterone, but not nonaromatizable dihydrotestosterone, improves working memory and alters nerve growth factor levels in aged male rats. Exp Neurol 2003;181:301-12.  Back to cited text no. 89
    
90.
Spritzer MD, Daviau ED, Coneeny MK, Engelman SM, Prince WT, Rodriguez-Wisdom KN. Effects of testosterone on spatial learning and memory in adult male rats. Horm Behav 2011;59:484-96.  Back to cited text no. 90
    
91.
Wagner BA, Braddick VC, Batson CG, Cullen BH, Miller LE, Spritzer MD. Effects of testosterone dose on spatial memory among castrated adult male rats. Psychoneuroendocrinology 2018;89:120-30.  Back to cited text no. 91
    
92.
Banga PV, Patil CY, Deshmukh GA, Chandaliya KC, Baig MS, Doifode SM. Biosynthesis, mechanism of action, and clinical mportance of neuroactive steroids: Pearls from literature. Int J Nutr Pharmacol Neurol Dis 2013;3:77.  Back to cited text no. 92
  [Full text]  
93.
Antunes IB, Andersen ML, Baracat EC, Tufik S. The effects of paradoxical sleep deprivation on estrous cycles of the female rats. Horm Behav 2006;49:433-40.  Back to cited text no. 93
    
94.
Andersen ML, Bignotto M, Tufik S. Influence of paradoxical sleep deprivation and cocaine on development of spontaneous penile reflexes in rats of different ages. Brain Res 2003;968:130-8.  Back to cited text no. 94
    
95.
Persengiev S, Kanchev L, Vezenkova G. Circadian patterns of melatonin, corticosterone, and progesterone in male rats subjected to chronic stress: effect of constant illumination. J Pineal Res 1991;11:57-62.  Back to cited text no. 95
    
96.
Brett M, Baxendale S. Motherhood and memory: a review. Psychoneuroendocrinology 2001;26:339-62.  Back to cited text no. 96
    
97.
Steiner M, Dunn E, Born L. Hormones and mood: from menarche to menopause and beyond. J Affect Disord 2003;74:67-83.  Back to cited text no. 97
    
98.
van Wingen G, van Broekhoven F, Verkes RJ et al. How progesterone impairs memory for biologically salient stimuli in healthy young women. J Neurosci 2007;27:11416-23.  Back to cited text no. 98
    
99.
van Wingen GA, van Broekhoven F, Verkes RJ et al. Progesterone selectively increases amygdala reactivity in women. Mol Psychiatry 2008;13:325-33.  Back to cited text no. 99
    
100.
Parker DC, Rossman LG, Pekary AE, Hershman JM. Effect of 64-hour sleep deprivation on the circadian waveform of thyrotropin (TSH): further evidence of sleep-related inhibition of TSH release. J Clin Endocrinol Metab 1987;64:157-61.  Back to cited text no. 100
    
101.
Brabant G, Prank K, Ranft U et al. Physiological regulation of circadian and pulsatile thyrotropin secretion in normal man and woman. J Clin Endocrinol Metab 1990;70:403-9.  Back to cited text no. 101
    
102.
Kuhs H, Farber D, Tolle R. Serum prolactin, growth hormone, total corticoids, thyroid hormones and thyrotropine during serial therapeutic sleep deprivation. Biol Psychiatry 1996;39:857-64.  Back to cited text no. 102
    
103.
Kessler L, Nedeltcheva A, Imperial J, Penev PD. Changes in serum TSH and free T4 during human sleep restriction. Sleep 2010;33:1115-8.  Back to cited text no. 103
    
104.
Everson CA, Nowak TS. Hypothalamic thyrotropin-releasing hormone mRNA responses to hypothyroxinemia induced by sleep deprivation. Am J Physiol Endocrinol Metab 2002;283:E85-93.  Back to cited text no. 104
    
105.
Wahlin A, Bunce D, Wahlin T-BR. Longitudinal evidence of the impact of normal thyroid stimulating hormone variations on cognitive functioning in very old age. Psychoneuroendocrinology 2005;30:625-37.  Back to cited text no. 105
    
106.
de Jong FJ, Masaki K, Chen H et al. Thyroid function, the risk of dementia and neuropathologic changes: the Honolulu-Asia aging study. Neurobiol Aging 2009;30:600-6.  Back to cited text no. 106
    
107.
Kalmijn S, Mehta KM, Pols HA, Hofman A, Drexhage HA, Breteler MM. Subclinical hyperthyroidism and the risk of dementia. The Rotterdam study. Clin Endocrinol 2000;53:733-7.  Back to cited text no. 107
    
108.
Wekking EM, Appelhof BC, Fliers E et al. Cognitive functioning and well-being in euthyroid patients on thyroxine replacement therapy for primary hypothyroidism. Eur J Endocrinol 2005;153:747-53.  Back to cited text no. 108
    
109.
Andersen ML, Alvarenga TAF, Guindalini C et al. Paradoxical sleep deprivation influences sexual behavior in female rats. J Sexual Med 2009;6:2162-72.  Back to cited text no. 109
    
110.
Merklinger-Gruchala A, Ellison PT, Lipson SF, Thune I, Jasienska G. Low estradiol levels in women of reproductive age having low sleep variation. Eur J Cancer Prev 2008;17:467-72.  Back to cited text no. 110
    
111.
Baumgartner A, Dietzel M, Saletu B et al. Influence of partial sleep deprivation on the secretion of thyrotropin, thyroid hormones, growth hormone, prolactin, luteinizing hormone, follicle stimulating hormone, and estradiol in healthy young women. Psychiatry Res 1993;48:153-78.  Back to cited text no. 111
    
112.
Viau V. Functional cross-talk between the hypothalamic-pituitary-gonadal and −adrenal axes. J Neuroendocrinol 2002;14:506-13.  Back to cited text no. 112
    
113.
Pike CJ, Carroll JC, Rosario ER, Barron AM. Protective actions of sex steroid hormones in Alzheimer’s disease. Front Neuroendocrinol 2009;30:239-58.  Back to cited text no. 113
    
114.
Simonyan KV, Chavushyan VA. Protective effects of hydroponic Teucrium polium on hippocampal neurodegeneration in ovariectomized rats. BMC Complement Altern Med 2016;16:415.  Back to cited text no. 114
    
115.
Hajali V, Sheibani V, Mahani SE et al. Ovariectomy does not exacerbate the negative effects of sleep deprivation on synaptic plasticity in rats. Physiol Behav 2015;144:73-81.  Back to cited text no. 115
    
116.
Woolley CS, McEwen BS. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol 1993;336:293-306.  Back to cited text no. 116
    


    Figures

  [Figure 1], [Figure 2]



 

Top
 
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

 
  In this article
    Abstract
   Introduction
   Conclusion
    References
    Article Figures

 Article Access Statistics
    Viewed998    
    Printed18    
    Emailed0    
    PDF Downloaded34    
    Comments [Add]    

Recommend this journal