Rui Costa1; David Costa1; José Pestana2
INTRODUCTION: REM sleep deprivation increases unstimulated erections in rats, and total sleep deprivation increases erections during audiovisual sexual stimulation in men, but the effects of sleep problems on human unstimulated sexual arousal are unknown.
OBJECTIVE: We examined the associations of subjective sleep quality with unstimulated sexual arousal, satisfaction with sex life, and sexual frequency and desire over the past month.
METHODS: 275 Portuguese (169 women) reported their anxiety, sexual arousal and sexual desire during a resting state, and completed the Pittsburgh Sleep Quality Index, the sexual satisfaction subscale of the LiSat scale, the Desire dimensions of the Female Sexual Function Index (women only) and International Index of Erectile Function (men only). They additionally reported how many days in the past month they engaged in penile-vaginal intercourse, noncoital sex, and masturbation. Salivary testosterone (T) was assayed by luminescence immunoassays.
RESULTS: Poorer sleep quality correlated with greater unstimulated sexual arousal in men with higher T levels and in women with higher T levels not taking oral contraceptives. In women with lower T, poorer subjective sleep quality correlated with greater sexual dissatisfaction. In both sexes, sleep quality was uncorrelated with sexual desire and sexual frequency over the past month.
DISCUSSION: Consistently with other studies in humans and animals, the findings are congruent with the notion that lack of sleep can increase sexual arousal, but not sexual frequency. T might play a role in the sexual arousal caused by lack of appropriate sleep.
Keywords: Sleep. Coitus. Sexual Dysfunctions, Psychological
Poor sleep quality has been related to sexual difficulties1-9, but case studies suggest that chronic insomnias sometimes increase sexual desire and arousal10. In fact, there is accumulating research suggesting that lack of sleep can increase sexual arousal in humans and animals. The present study aimed at better understanding this intriguing phenomenon in men and women.
In male rats, REM sleep deprivation increased spontaneous erections and ejaculations, that is, without the presence of females11,12, but effects on copulation were found to be mixed with REM sleep deprivation either increasing or reducing copulatory behavior11,13-16. In one study, both REM sleep deprivation and general sleep restriction lowered sperm viability, but increased inducible nitric oxide synthase13, which can enhance erections17,18. General sleep restriction did not interfere with copulation in male rats13. Increased genital excitation and sexual behavior were also observed in male cats deprived of REM sleep19,20. In female rats, REM sleep deprivation either increased or reduced proceptivity and receptivity with lower progesterone levels possibly enhancing sexual responsiveness under conditions of REM sleep deprivation21,22.
In men with psychogenic erectile dysfunction, total sleep deprivation increased erections in response to audiovisual sexual stimuli23, and in a nonclinical male sample, both REM sleep deprivation and non-REM awakenings increased visual attention to images of women, but the non-REM awakenings implied REM deprivation24. In women, poorer subjective sleep quality over the past month correlated with greater increases in subjective sexual arousal during fantasy25. Moreover, in a study with women reporting daily sleep duration and sexual responses and behaviors in the next day, shorter sleep duration correlated with greater perceived genital arousal (lubrication) in the next day, but to lesser desire and less likelihood of having sex26. In contrast, others found that sleep disorders and shorter sleep duration are uncorrelated with coital frequency27,28. Taken together, all these findings in humans and animals suggest that lack of sleep can facilitate sexual arousal with unclear effects on sexual interactions.
Because animal studies show that lack of REM sleep increases spontaneous erections11,12, we tested the hypothesis that, in men and women, poorer subjective sleep quality over the past month correlates with greater unstimulated sexual arousal, that is, arousal in a resting state without external sexual stimulation. Because studies in humans and animals have yielded mixed findings regarding the effects of sleep deprivation on sexual interactions and motivation to pursue sexual activity, we additionally examined the associations of poorer subjective sleep quality with sexual desire and frequency over the past month, as well as with sexual satisfaction, with no a priori hypotheses.
Given that lack of sleep increases anxiety29 and moderate levels of anxiety may facilitate sexual arousal30-33, we examined if state anxiety explains the hypothesized relation between unstimulated sexual arousal and poorer subjective sleep quality.
Testosterone (T) administration to REM-sleep deprived male rats stimulated copulatory behavior34, and greater T rises were found to have a slight explanatory effect in the relationship between women’s poorer sleep quality and fantasy-induced sexual arousal25. Therefore, we hypothesized that the relation between unstimulated sexual arousal and severity of sleep problems is observed among those with higher T levels, but not among those with lower T levels.
Because oral contraceptives seem to facilitate REM sleep35,36, it is likely that sleep problems of oral contraceptive users involve less REM sleep disturbances; because specifically lack of REM sleep might increase unstimulated sexual arousal, we tested if unstimulated arousal and poorer subjective sleep quality are correlated, and if this association is moderated by T levels, in naturally cycling women and oral contraceptive users separately.
The study had the participation of 338 Portuguese from the Lisbon area. Exclusion criteria applied to those not reporting data on sleep quality (N = 2), describing their sexuality as totally or almost totally with the same sex (N = 18), taking psychotropic medications or having health conditions that could interfere with sexuality (except one participant complaining from chronic insomnia; N = 29), not reporting data on hormonal contraception (N = 6), and for whom there were no data on T (N = 8). The final sample consisted of 169 women and 106 men. The samples sizes were chosen, because they have adequate power (.80) to detect modest effect sizes: in the case of women until r2 = .045. In the case of men until r2 = .070. Descriptive statistics are depicted in Table 1.
The Pittsburgh Sleep Quality Index (PSQI)37 was used to measure subjective sleep quality. The PSQI has 19 items tapping seven components of sleep quality: overall subjective sleep quality, sleep latency, sleep duration, habitual sleep efficiency, sleep disturbances, use of sleeping medication, and daytime dysfunction. Higher scores indicate poorer sleep quality.
Unstimulated sexual arousal, desire, and anxiety, were measured by asking “In this precise moment, describe to what extent are you feeling sexual arousal, desire, and anxiety. Responses were given on a scale from 1 (absolutely nothing) to 7 (extremely)25,38. These questions were made shortly after participants having arrived to the laboratory, when they were in a resting state. In fact, these questions were meant to assess baseline psychological state before exposition to stimuli as part of a study not reported here. Baseline (unstimulated) desire and arousal measured with this scale were significantly increased by induction of a sexual fantasy25 and visualization of a romantic movie scene38, which supports their validity as measures of resting state.
Sexual satisfaction was measured with the respective single-item scale of the LiSat (Life Satisfaction) scale, which is rated on a scale ranging from 1 (very dissatisfying) to 6 (very satisfying)39. Several studies support the utilization of this measure in sexual assessment39-42.
Participants were asked about their frequency in days in the past month of penile-vaginal intercourse, masturbation, and noncoital sex without same day vaginal intercourse43. In addition, female sexual desire was assessed with the Desire subscale of the Female Sexual Function Index (FSFI)44, which has 2 items asking respondents to rate their level and frequency of sexual desire or interest over the past four weeks on a scale from 1 to 5. Male sexual desire was additionally measured with the Desire dimension of the International Index of Erectile Function (IIEF)45. This subscale is composed of 2 items asking respondents to rate their level and frequency of sexual desire in the preceding four weeks on a scale from 1 to 5.
For salivary T determination, approximately 1ml of saliva was collected into a polypropylene tube for each participant, and conserved at -20º. Afterwards, samples were centrifuged for ten minutes at 2245 g, and T was assayed with luminescence immunoassay kits from IBL-International (RE62031). Inter and intra-assay coefficients were 7.17% and 2.28%, respectively. All samples were collected in the afternoon (between 2 pm and 5 pm), because T collected during this time of the day has been more consistently related to behavioral variables46-48. We did not control for menstrual cycle, because it was shown not to meaningful affect correlations between T and behavioral and cogntive variables49,50. Because we wanted to test that the relation between unstimulated arousal and poorer sleep is moderated by T levels, we distributed the male and female samples in subgroups with higher and lower T levels based on a median split.
Upon arriving at the laboratory, participants provided written informed consent and reported to what extent they were feeling sexual arousal, sexual desire, and anxiety. Immediately afterwards, they provided a saliva sample for T determination. This procedure had the objective of assessing baseline T and psychological state before exhibition of experimental stimuli as part of a study not reported here (the stimuli consisted of an excerpt of romantic movie showing the initial emotional involvement between a man and woman, and of a short movie showing explicit sexual activity between a man and a woman). The saliva samples were collected before questionnaires being applied. After the experimental task, participants completed the battery of questionnaires including the questions of interest for the present study. Participants received course credits or a ten-euro shopping voucher. The advertisement of the experiment was done through the internet and directed at the general population. The study had the approval of the local Ethics Committee, and followed the Declaration of Helsinki principles.
Sleep problems correlated with greater T levels among naturally cycling women (r = .24, p = .051), but not in men (r = .06, p = .551) and women taking oral contraception (r = -.11, p = .280). Women taking oral contraception were more likely to have T below the median (57.7 % vs. 36.9 %, chi square = 6.90, p = .009).
As displayed in Table 2, unstimulated sexual arousal correlated with greater severity of sleep problems in women. When women were allocated to subgroups with higher and lower T levels, unstimulated arousal correlated with sleep problems only among women with higher T. We did a further allocation of the female sample into four subgroups according to T levels and oral contraception use (lower T and no contraceptive use, higher T and no contraceptive use, lower T and contraceptive use, higher T and contraceptive use). Sleep problems correlated with unstimulated arousal only in the subgroup with higher T and not taking oral contraception (see Table 4).
As depicted in Table 3, unstimulated sexual arousal correlated with greater severity of sleep problems in men. When the men were allocated to subgroups with higher and lower T levels, unstimulated arousal correlated with sleep problems only among men with higher T.
As depicted in Table 2, greater severity of sleep problems correlated with greater sexual dissatisfaction among the entire group of women, and in the female subgroup with lower T. For both sexes, severity of sleep problems was uncorrelated with unstimulated desire as well as with sexual frequency and desire over the past month (see Tables 2, 3 and 4).
In backward multiple regressions done for the subgroups of men with higher T levels and women with higher T levels taking oral contraception, severity of sleep problems was predicted by greater unstimulated arousal, but not by unstimulated anxiety, and age (see Tables 5 and 6).
The present study confirmed that poorer subjective sleep quality is related to greater unstimulated sexual arousal, and that this relation was mostly driven by men with higher T levels and women with higher T levels not taking oral contraception. These findings extend previous ones showing that 1) severity of women’s subjective sleep problems correlated with greater fantasy-induced subjective sexual arousal25, 2) perceived genital arousal was greater, when the duration of sleep was shorter in the previous night26, and 3) sleep deprivation in men increased erections in response to erotica23 and visual attention to images of women24. Our findings are also consistent with studies in male rats showing that unstimulated erections are facilitated by REM sleep deprivation11,12, a consequence of general sleep deprivation.
As predicted, severity of sleep problems correlated with unstimulated arousal only in the male and female groups with higher T levels. The facilitating role of T in increasing sexual arousal in rats and humans with lack of adequate sleep was previously reported25,34. In addition, enhanced dopaminergic activity appears to be a mechanism by which REM sleep deprivation increases sexual arousal14,51,52, and REM sleep is likely more disturbed in many people with sleep problems. Ferini-Strambi and colleagues proposed that sleep deprivation reduces psychological inhibitions23.
In addition, the relation between female unstimulated arousal and sleep quality was further moderated by oral contraception: we found that unstimulated arousal and poorer sleep quality correlated in naturally cycling women with higher T levels, but not in women taking oral contraceptives, even if they had higher T levels, which argues against the possibility that the decrements in T commonly observed in women taking oral contraception53 (and replicated in the present study) drive the relation between sleep quality and sexual arousal. There is evidence that oral contraception favors REM sleep35,36; therefore, it is possible that sleep problems in oral contraceptive users are less likely to reflect REM sleep disturbances, and thereby less likely to have a sexually arousing effect. Also, it has been found, that, in female rats, REM sleep deprivation either facilitates or inhibits proceptive and receptive sexual behavior, with lower progesterone possibly increasing sexual behavior under REM sleep deprivation21,22. This raises the possibility that the hormonal changes caused by the pill may attenuate or impede the enhancing effect of sleep deprivation on sexual arousal. Future research is needed to clarify this question. Future research might address the role of type and duration of contraception.
Poorer sleep quality was associated with female dissatisfaction with sex life, and this relation was largely driven by women with lower T levels, regardless of oral contraception. Whereas lack of adequate sleep correlated with greater unstimulated arousal when there were higher T levels, lack of adequate sleep correlated with greater dissatisfaction with sex life, when there were lower T levels. Research in men has highlighted a possible interrelationship between sleep problems, erectile dysfunction, and lower T54. Future research is needed to unveil which factors moderate the effects of sleep disturbances on sexual responsiveness; with the present knowledge, lower T levels appear to increase the risk of sexual difficulties related to sleep problems.
According to our findings, poorer sleep quality does not reflect on greater sexual desire nor on greater frequency of sexual activities. If anything, there were nonsignificant correlations between poorer sleep quality and lesser frequency of sexual interactions. In rats, the effects of REM sleep deprivation on copulation are mixed11,13-16,21,22. In a study of women, shorter sleep duration reduced desire and likelihood of having sex in the other day, despite facilitation of lubrication26, but others have found coital frequency to be uncorrelated with sleep disorders27 and shorter sleep duration28, which is consistent with our findings. It is likely that, even with increased sexual arousal, the tiredness that results from lack of sleep often interferes with intimacy, which might ultimately lead to sexual difficulties. Sleep problems have been related to erectile dysfunction and female sexual difficulties1-9,26.
Unstimulated state anxiety did not explain the relationship between sleep problems and unstimulated arousal. This is consistent with a previous study, in which state anxiety did not explain the association between poor sleep quality and sexual arousal in response to fantasy25.
In the naturally cycling female group, there was a significant direct correlation between higher T levels and poorer subjective sleep quality. The link between T and sleep quality in women remains understudied. In men, there is some evidence that lack of adequate sleep may cause T levels to diminish55,56. In the present study, T did not correlate with sleep problems in men, but this finding might be explained by the young age range of the present sample, as previous studies included older participants55,56.
Unstimulated sexual arousal was reported with participants having no external stimulation, but they might have been aroused by fantasy. In fact, severity of subjective sleep problems was previously correlated with greater fantasy-induced sexual arousal25. If sleep deprivation enhances spontaneous sexual responses, it is possible that, in humans, there is a concomitant increase in internally-generated sexual imagery. Also, it could be argued that the unstimulated participants were still aroused to some degree by events that had occurred before they arrived to the laboratory. If that is the case, then sexual stimuli can exert a more persistent effect in persons with poorer sleep quality, even when they are already not present. Research is warranted on this topic.
Our study revealed that unstimulated arousal was more consistently correlated with sleep quality than unstimulated desire. This is consistent with previous research showing that poorer subjective sleep quality correlated with greater fantasy-induced subjective sexual arousal, but not desire25, and that shorter sleep duration increased genital arousal, but not desire in the next day26. Desire and arousal may be contrasted as the former being a motivational state that drives the search for sexual activity, whereas the latter is a change in the physical and psychological state that prepares individuals for sexual activity57, which does not contradict models of sexual response in which arousal precedes desire. Although, these definitions are not commonly provided to research participants, it is rather possible that most understand them that way, even if there are difficulties for lay people to express it in words. Also, the differential relations of desire and arousal with sleep quality found in humans seem consistent with animal models showing that REM sleep deprivation can enhance spontaneous erections (without presence of females)11,12, but there are mixed findings regarding the effects on the pursuit of copulation, as indexed by reduced proceptive behavior in females21,22, and greater mount and intromission latency, or reduced mount and intromission frequency in males11,13-16.
Limitations of the present study include the lack of physiological measures of erection and vaginal vasocongestion, and the young, mostly non-cohabiting, sample. Also, the study was cross-sectional, and caution is needed regarding causal inferences. However, previous research shows that lack of appropriate sleep has an enhancing effect on sexual arousal11,12,23,24,26, and that T administration facilitates sexual behavior in REM-deprived rats34.
The findings are consistent with the notion that, in men and naturally cycling women, lack of adequate sleep facilitates unstimulated sexual arousal in those with higher T levels, but frequency of sexual interactions is not increased.
1. Amasyali AS, Taştaban E, Amasyali SY, Turan Y, Kazan E, Sari E, et al. Effects of low sleep quality on sexual function, in women with fibromyalgia. Int J Impot Res. 2016;28(2):46-9.
2. Andersen ML, Santos-Silva R, Bittencourt LR, Tufik S. Prevalence of erectile dysfunction complaints associated with sleep disturbances in Sao Paulo, Brazil: a population-based survey. Sleep Med. 2010;11(10):1019-24.
3. Charandabi SM, Rezaei N, Hakimi S, Khatami S, Valizadeh R, Azadi A. Sleep disturbances and sexual function among men aged 45-75 years in an urban area of Iran. Sleep Sci. 2016;9(1):29-34.
4. Chen KF, Liang SJ, Lin CL, Liao WC, Kao CH. Sleep disorders increase risk of subsequent erectile dysfunction in individuals without sleep apnea: a nationwide population-base cohort study. Sleep Med. 2016;17:64-8.
5. Cheng QS, Liu T, Huang HB, Peng YF, Jiang SC, Mei XB. Association between personal basic information, sleep quality, mental disorders and erectile function: a cross-sectional study among 334 Chinese outpatients. Andrologia. 2017;49(3):e12631.
6. Ghajarzadeh M, Jalilian R, Togha M, Azimi A, Hosseini P, Babaei N. Depression, poor sleep, and sexual dysfunction in migraineurs women. Int J Prev Med. 2014;5(9):1113-8.
7. Lin HH, Ho FM, Chen YF, Tseng CM, Ho CC, Chung WS. Increased risk of erectile dysfunction among patients with sleep disorders: a nationwide population-based cohort study. Int J Clin Pract. 2015;69(8):846-52.
8. Sasaki H, Yamasaki H, Ogawa K, Nanjo K, Kawamori R, Iwamoto Y, et al. Prevalence and risk factors for erectile dysfunction in Japanese diabetics. Diabetes Res Clin Pract. 2005;70(1):81-9.
9. Schnatz PF, Whitehurst SK, O’Sullivan DM. Sexual dysfunction, depression, and anxiety among patients of an inner-city menopause clinic. J Womens Health (Larchmt). 2010;19(10):1843-9.
10. Schenck CH, Arnulf I, Mahowald MW. Sleep and sex: what can go wrong? A review of the literature on sleep related disorders and abnormal sexual behaviors and experiences. Sleep. 2007;30(6):683-702.
11. Alvarenga TA, Andersen ML, Velázquez-Moctezuma J, Tufik S. Food restriction or sleep deprivation: which exerts a greater influence on the sexual behaviour of male rats? Behav Brain Res. 2009;202(2):266-71.
12. Andersen ML, Antunes IB, Tufik S. Effects of paradoxical sleep deprivation on genital reflexes in five rat strains. Horm Behav. 2006;49(2):173-80.
13. Alvarenga TA, Hirotsu C, Mazaro-Costa R, Tufik S, Andersen ML. Impairment of male reproductive function after sleep deprivation. Fertil Steril. 2015;103(5):1355-62.e1.
14. Damasceno F, Skinner GO, Cordeiro JF, Ferraz MR, Almeida OM. Sleep deprivation affects sexual behavior and tyrosine hydroxylase (TH) levels in sexually experienced male rats. Physiol Behav. 2008;94(3):405-11.
15. Ferraz MR, Ferraz MM, Santos R. How REM sleep deprivation and amantadine affects male rat sexual behavior. Pharmacol Biochem Behav. 2001;69(3-4):325-32.
16. Velazquez-Moctezuma J, Salazar ED, Retana-Marquez S. Effects of short- and long-term REM sleep deprivation on sexual behavior in male rats. Physiol Behav. 1996;59(2):277-81.
17. Ferrini MG, Gonzalez-Cadavid NF, Rajfer J. Aging related erectile dysfunction-potential mechanism to halt or delay its onset. Transl Androl Urol. 2017;6(1):20-7.
18. Yang S, Chen C, Li Y, Ren Z, Zhang Y, Wu G, et al. Saw palmetto extract enhances erectile responses by inhibition of phosphodiesterase 5 activity and increase in inducible nitric oxide synthase messenger ribonucleic acid expression in rat and rabbit corpus cavernosum. Urology. 2013;81(6):1380.e7-13.
19. Dement WC. Recent studies on the biological role of rapid eye movement sleep. Am J Psychiatry. 1965;122(4):404-8.
20. Vimont-Vicary P, Jouvet-Mounier D, Delorme F. EEG and behavioral effects of deprivation of paradoxical sleep in cats. Electroencephalogr Clin Neurophysiol. 1966;20(5):439-49.
21. Andersen ML, Alvarenga TA, Guindalini C, Perry JC, Silva A, Zager A, et al. Paradoxical sleep deprivation influences sexual behavior in female rats. J Sex Med. 2009;6(8):2162-72.
22. Velazquez-Moctezuma J, Monroy E, Beyer C, Canchola E. Effects of REM deprivation on the lordosis response induced by gonadal steroids in ovariectomized rats. Physiol Behav. 1984;32(1):91-4.
23. Ferini-Strambi L, Montorsi F, Iannaccone S, Guazzoni G, Zucconi M, Smirne S, et al. The impact of sleep deprivation on erotic erections. Eur Urol. 1996;30(1):50-3.
24. Zarcone V, de la Pena A, Dement WC. Heightened sexual interest and sleep disturbance. Percept Motor Skill. 1974;39(3):1135-41.
25. Costa RM, Oliveira TF. Poorer Subjective Sleep Quality Is Related to Higher Fantasy-Induced Sexual Arousal in Women of Reproductive Age. J Sex Marital Ther. 2016;42(8):740-8.
26. Kalmbach DA, Arnedt JT, Pillai V, Ciesla JA. The impact of sleep on female sexual response and behavior: a pilot study. J Sex Med. 2015;12(5):1221-32.
27. Okabe K, Mishima N. Frequency of marital intercourse among patients with psychiatric and psychosomatic disorders in Japan. J Sex Marital Ther. 2004;30(1):3-11.
28. Goh VH, Tong TY. Sleep, sex steroid hormones, sexual activities, and aging in Asian men. J Androl. 2010;31(2):131-7.
29. Vandekerckhove M, Cluydts R. The emotional brain and sleep: an intimate relationship. Sleep Med Rev. 2010;14(4):219-26.
30. Barlow DH, Sakheim DK, Beck JG. Anxiety increases sexual arousal. J Abnorm Psychol. 1983;92(1):49-54.
31. Bradford A, Meston CM. The impact of anxiety on sexual arousal in women. Behav Res Ther. 2006;44(8):1067-77.
32. Palace EM, Gorzalka BB. The enhancing effects of anxiety on arousal in sexually dysfunctional and functional women. J Abnorm Psychol. 1990;99(4):403-11.
33. Kalmbach DA, Kingsberg SA, Ciesla JA. How changes in depression and anxiety symptoms correspond to variations in female sexual response in a nonclinical sample of young women: a daily diary study. J Sex Med. 2014;11(12):2915-27.
34. Velazquez-Moctezuma J, Monroy E, Cruz ML. Facilitation of the effect testosterone on male sexual behavior in rats deprived of REM sleep. Behav Neural Biol. 1989;51(1):46-53.
35. Burdick RS, Hoffmann R, Armitage R. Short note: oral contraceptives and sleep in depressed and healthy women. Sleep. 2002;25(3):347-9.
36. Hachul H, Andersen ML, Bittencourt LR, Santos-Silva R, Conway SG, Tufik S. Does the reproductive cycle influence sleep patterns in women with sleep complaints? Climacteric. 2010;13(6):594-603.
37. Buysse DJ, Reynolds CF 3rd, Monk TH, Berman SR, Kupfer DJ. The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989;28(2):193-213.
38. Costa RM, Oliveira TF, Pestana J, Costa D. Self-transcendence is related to higher female sexual desire. Pers Indiv Differ. 2016;96:191-7.
39. Fugl-Meyer KS, Stothard D, Belger M, Toll A, Berglund O, Eliasson T, et al. The effect of tadalafil on psychosocial outcomes in Swedish men with erectile distress: a multicentre, non-randomised, open-label clinical study. Int J Clin Pract. 2006;60(11):1386-93.
40. Brody S, Costa RM. Satisfaction (sexual, life, relationship, and mental health) is associated directly with penile-vaginal intercourse, but inversely with other sexual behavior frequencies. J Sex Med. 2009;6(7):1947-54.
41. Moncada I, Micheltorena CF, Martínez-Sánchez EM, Gutiérrez JR. Evaluation of the psychometric properties of the life satisfaction checklist as a screening tool for erectile dysfunction. J Sex Med. 2008;5(1):83-91.
42. Oberg K, Sjögren Fugl-Meyer K. On Swedish women’s distressing sexual dysfunctions: some concomitant conditions and life satisfaction. J Sex Med. 2005;2(2):169-80.
43. Brody S, Preut R. Vaginal intercourse frequency and heart rate variability. J Sex Marital Ther. 2003;29(5):371-80.
44. Rosen R, Brown C, Heiman J, Leiblum S, Meston C, Shabsigh R, et al. The Female Sexual Function Index (FSFI): a multidimensional self-report instrument for the assessment of female sexual function. J Sex Marital Ther. 2000;26(2):191-208.
45. Rosen RC, Riley A, Wagner G, Osterloh IH, Kirkpatrick J, Mishra A. The international index of erectile function (IIEF): a multidimensional scale for assessment of erectile dysfunction. Urology. 1997;49(6):822-30.
46. Gray PB, Campbell BC, Marlowe FW, Lipson SF, Ellison PT. Social variables predict between-subject but not day-to-day variation in the testosterone of US men. Psychoneuroendocrinology. 2004;29(9):1153-62.
47. López HH, Hay AC, Conklin PH. Attractive men induce testosterone and cortisol release in women. Horm Behav. 2009;56(1):84-92.
48. Roney JR, Lukaszewski AW, Simmons ZL. Rapid endocrine responses of young men to social interactions with young women. Horm Behav. 2007;52(3):326-33.
49. Dabbs JM Jr. Salivary testosterone measurements: reliability across hours, days, and weeks. Physiol Behav. 1990;48(1):83-6.
50. Dabbs JM Jr, de La Rue D. Salivary testosterone measurements among women: relative magnitude of circadian and menstrual cycles. Horm Res. 1991;35(5):182-4.
51. Nunes Júnior GP, Tufik S, Nobrega JN. Autoradiographic analysis of D1 and D2 dopaminergic receptors in rat brain after paradoxical sleep deprivation. Brain Res Bull. 1994;34(5):453-6.
52. Volkow ND, Wang GJ, Telang F, Fowler JS, Logan J, Wong C, et al. Sleep deprivation decreases binding of [11C]raclopride to dopamine D2/D3 receptors in the human brain. J Neurosci. 2008;28(34):8454-61.
53. Zimmerman Y, Eijkemans MJ, Coelingh Bennink HJ, Blankenstein MA, Fauser BC. The effect of combined oral contraception on testosterone levels in healthy women: a systematic review and meta-analysis. Hum Reprod Update. 2014;20(1):76-105.
54. Soterio-Pires JH, Hirotsu C, Kim LJ, Bittencourt L, Tufik S, Andersen ML. The interaction between erectile dysfunction complaints and depression in men: a cross-sectional study about sleep, hormones and quality of life. Int J Impot Res. 2017;29(2):70-5.
55. Barrett-Connor E, Dam TT, Stone K, Harrison SL, Redline S, Orwoll E; Osteoporotic Fractures in Men Study Group. The association of testosterone levels with overall sleep quality, sleep architecture, and sleep-disordered breathing. J Clin Endocrinol Metab. 2008;93(7):2602-9.
56. Penev PD. Association between sleep and morning testosterone levels in older men. Sleep. 2007;30(4):427-32.
57. Ortigue S, Bianchi-Demicheli F. Interactions between human sexual arousal and sexual desire: a challenge for social neuroscience. Rev Med Suisse. 2007;3(104):809-13.
July 16 2017.
Accepted em October 31 2017.