Animal Models

Noise-induced sleep disruption increases weight gain and decreases energy metabolism in female rats

Subjects

Abstract

Background/objectives

Inadequate sleep increases obesity and environmental noise contributes to poor sleep. However, women may be more vulnerable to noise and hence more susceptible to sleep disruption-induced weight gain than men. In male rats, exposure to environmental (i.e. ambient) noise disrupts sleep and increases feeding and weight gain. However, the effects of environmental noise on sleep and weight gain in female rats are unknown. Thus, this study was designed to determine whether noise exposure would disturb sleep, increase feeding and weight gain and alter the length of the estrous cycle in female rats.

Subjects/methods

Female rats (12 weeks old) were exposed to noise for 17d (8 h/d during the light period) to determine the effects of noise on weight gain and food intake. In a separate set of females, estrous cycle phase and length, EEG, EMG, spontaneous physical activity and energy expenditure were recorded continuously for 27d during baseline (control, 9d), noise exposure (8 h/d, 9d) and recovery (9d) from sleep disruption.

Results

Noise exposure significantly increased weight gain and food intake compared to females that slept undisturbed. Noise also significantly increased wakefulness, reduced sleep and resulted in rebound sleep during the recovery period. Total energy expenditure was significantly lower during both noise exposure and recovery due to lower energy expenditure during spontaneous physical activity and sleep. Notably, noise did not alter the estrous cycle length.

Conclusions

As previously observed in male rats, noise exposure disrupted sleep and increased weight gain in females but did not alter the length of the estrous cycle. This is the first demonstration of weight gain in female rats during sleep disruption. We conclude that the sleep disruption caused by exposure to environmental noise is a significant tool for determining how sleep loss contributes to obesity in females.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. 1.

    Ford ES, Cunningham TJ, Croft JB. Trends in self-reported sleep duration among US adults from 1985 to 2012. Sleep. 2015;38:829–32.

    PubMed  PubMed Central  Article  Google Scholar 

  2. 2.

    Itani O, Jike M, Watanabe N, Kaneita Y. Short sleep duration and health outcomes: a systematic review, meta-analysis, and meta-regression. Sleep Med. 2017;32:246–56.

    PubMed  Article  Google Scholar 

  3. 3.

    Basner M, McGuire S. WHO environmental noise guidelines for the European region: a systematic review on environmental noise and effects on sleep. Int J Environ Res Public Health. 2018;15:519–64

    PubMed Central  Article  Google Scholar 

  4. 4.

    Oftedal B, Krog NH, Pyko A, Eriksson C, Graff-Iversen S, Haugen M, et al. Road traffic noise and markers of obesity—a population-based study. Environ Res. 2015;138:144–53.

    CAS  PubMed  Article  Google Scholar 

  5. 5.

    Herzog N, Jauch-Chara K, Hyzy F, Richter A, Friedrich A, Benedict C, et al. Selective slow wave sleep but not rapid eye movement sleep suppression impairs morning glucose tolerance in healthy men. Psychoneuroendocrinology. 2013;38:2075–82.

    CAS  PubMed  Article  Google Scholar 

  6. 6.

    Roosli M, Mohler E, Frei P, Vienneau D. Noise-related sleep disturbances: does gender matter? Noise Health. 2014;16:197–204.

    PubMed  Article  Google Scholar 

  7. 7.

    Lyytikainen P, Rahkonen O, Lahelma E, Lallukka T. Association of sleep duration with weight and weight gain: a prospective follow-up study. J Sleep Res. 2011;20:298–302.

    PubMed  Article  Google Scholar 

  8. 8.

    Markwald RR, Melanson EL, Smith MR, Higgins J, Perreault L, Eckel RH, et al. Impact of insufficient sleep on total daily energy expenditure, food intake, and weight gain. Proc Natl Acad Sci USA. 2013;110:5695–700.

    CAS  PubMed  Article  Google Scholar 

  9. 9.

    Spaeth AM, Dinges DF, Goel N. Effects of experimental sleep restriction on weight gain, caloric intake, and meal timing in healthy adults. Sleep. 2013;36:981–90.

    PubMed  PubMed Central  Article  Google Scholar 

  10. 10.

    Bosy-Westphal A, Hinrichs S, Jauch-Chara K, Hitze B, Later W, Wilms B, et al. Influence of partial sleep deprivation on energy balance and insulin sensitivity in healthy women. Obes Facts. 2008;1:266–73.

    PubMed  PubMed Central  Article  Google Scholar 

  11. 11.

    Spaeth AM, Dinges DF, Goel N. Resting metabolic rate varies by race and by sleep duration. Obesity (Silver Spring). 2015;23:2349–56.

    Article  Google Scholar 

  12. 12.

    Shechter A, Rising R, Albu JB, St-Onge MP. Experimental sleep curtailment causes wake-dependent increases in 24-h energy expenditure as measured by whole-room indirect calorimetry. Am J Clin Nutr. 2013;98:1433–9.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  13. 13.

    Shechter A, Rising R, Wolfe S, Albu JB, St-Onge MP. Postprandial thermogenesis and substrate oxidation are unaffected by sleep restriction. Int J Obes (Lond). 2014;38:1153–8.

    CAS  Article  Google Scholar 

  14. 14.

    Andersen ML, Ribeiro DA, Alvarenga TA, Silva A, Araujo P, Zager A, et al. Are endogenous sex hormones related to DNA damage in paradoxically sleep-deprived female rats? Horm Behav. 2010;57:216–21.

    CAS  PubMed  Article  Google Scholar 

  15. 15.

    de Oliveira RA, Cunha GM, Borges KD, de Bruin GS, dos Santos-Filho EA, Viana GS, et al. The effect of venlafaxine on behaviour, body weight and striatal monoamine levels on sleep-deprived female rats. Pharmacol Biochem Behav. 2004;79:499–506.

    PubMed  Article  Google Scholar 

  16. 16.

    Hajali V, Sheibani V, Esmaeili-Mahani S, Shabani M. Female rats are more susceptible to the deleterious effects of paradoxical sleep deprivation on cognitive performance. Behav Brain Res. 2012;228:311–8.

    PubMed  Article  Google Scholar 

  17. 17.

    Everson CA, Bergmann BM, Rechtschaffen A. Sleep deprivation in the rat: III. Total sleep deprivation. Sleep. 1989;12:13–21.

    CAS  PubMed  Article  Google Scholar 

  18. 18.

    Longuski PA, Cudillo CA, Stern JJ. Brief communication effects of estradiol on feeding and locomotion in REM deprived rats. Physiol Behav. 1976;16:97–9.

    CAS  PubMed  Article  Google Scholar 

  19. 19.

    Schwierin B, Borbely AA, Tobler I. Sleep homeostasis in the female rat during the estrous cycle. Brain Res. 1998;811:96–104.

    CAS  PubMed  Article  Google Scholar 

  20. 20.

    Fang J, Fishbein W. Sex differences in paradoxical sleep: influences of estrus cycle and ovariectomy. Brain Res. 1996;734:275–85.

    CAS  PubMed  Article  Google Scholar 

  21. 21.

    Colvin GB, Whitmoyer DI, Lisk RD, Walter DO, Sawyer CH. Changes in sleep-wakefulness in female rats during circadian and estrous cycles. Brain Res. 1968;7:173–81.

    CAS  PubMed  Article  Google Scholar 

  22. 22.

    Giles ED, Jackman MR, Johnson GC, Schedin PJ, Houser JL, MacLean PS. Effect of the estrous cycle and surgical ovariectomy on energy balance, fuel utilization, and physical activity in lean and obese female rats. Am J Physiol Regul Integr Comp Physiol. 2010;299:R1634–42.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. 23.

    Anantharaman-Barr HG, Decombaz J. The effect of wheel running and the estrous cycle on energy expenditure in female rats. Physiol Behav. 1989;46:259–63.

    CAS  PubMed  Article  Google Scholar 

  24. 24.

    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.

    CAS  PubMed  Article  Google Scholar 

  25. 25.

    Andersen ML, Antunes IB, Silva A, Alvarenga TA, Baracat EC, Tufik S. Effects of sleep loss on sleep architecture in Wistar rats: gender-specific rebound sleep. Prog Neuropsychopharmacol Biol Psychiatry. 2008;32:975–83.

    CAS  PubMed  Article  Google Scholar 

  26. 26.

    Cordeira J, Kolluru SS, Rosenblatt H, Kry J, Strecker RE, McCarley RW. Learning and memory are impaired in the object recognition task during metestrus/diestrus and after sleep deprivation. Behav Brain Res. 2018;339:124–9.

    PubMed  Article  Google Scholar 

  27. 27.

    Parrish JB, Teske JA. Acute partial sleep deprivation due to environmental noise increases weight gain by reducing energy expenditure in rodents. Obesity (Silver Spring). 2017;25:141–6.

    Article  Google Scholar 

  28. 28.

    Mavanji V, Teske JA, Billington CJ, Kotz CM. Partial sleep deprivation by environmental noise increases food intake and body weight in obesity resistant rats. Obesity (Silver Spring). 2013;21:1396–405.

    Article  Google Scholar 

  29. 29.

    DePorter DP, Coborn JE, Teske JA. Partial sleep deprivation reduces the efficacy of orexin-A to stimulate physical activity and energy expenditure. Obesity (Silver Spring). 2017;25:1716–22.

    CAS  Article  Google Scholar 

  30. 30.

    Mavanji V, Teske JA, Billington CJ, Kotz CM. Elevated sleep quality and orexin receptor mRNA in obesity-resistant rats. Int J Obes (Lond). 2010;34:1576–88.

    CAS  Article  Google Scholar 

  31. 31.

    Borbely AA, Tobler I, Hanagasioglu M. Effect of sleep deprivation on sleep and EEG power spectra in the rat. Behav Brain Res. 1984;14:171–82.

    CAS  PubMed  Article  Google Scholar 

  32. 32.

    Sinton CM, Kovakkattu D, Friese RS. Validation of a novel method to interrupt sleep in the mouse. J Neurosci Methods. 2009;184:71–8.

    PubMed  Article  Google Scholar 

  33. 33.

    Coborn JE, DePorter DP, Mavanji V, Sinton CM, Kotz CM, Billington CJ, et al. Role of orexin-A in the ventrolateral preoptic area on components of total energy expenditure. Int J Obes (Lond). 2017;41:1256–62.

    CAS  Article  Google Scholar 

  34. 34.

    Mavanji V, Perez-Leighton CE, Kotz CM, Billington CJ, Parthasarathy S, Sinton CM, et al. Promotion of wakefulness and energy expenditure by orexin-A in the ventrolateral preoptic area. Sleep. 2015;38:1361–70.

    PubMed  PubMed Central  Article  Google Scholar 

  35. 35.

    Anita MM. The phases of the oestrous cycle in the adult white rat. J Exp Biol. 1951;28:576–84.

    Google Scholar 

  36. 36.

    Benjamini YHY. Controlling the false discovery rate: a practical and powerful approach to multiple hypothesis testing. J R Stat Soc Ser B. 1995;57:289–300.

    Google Scholar 

  37. 37.

    Parker GC, McKee ME, Bishop C, Coscina DV. Whole-body metabolism varies across the estrous cycle in Sprague−Dawley rats. Physiol Behav. 2001;74:399–403.

    CAS  PubMed  Article  Google Scholar 

  38. 38.

    Brobeck JR, Wheatland M, Strominger JL. Variations in regulation of energy exchange associated with estrus, diestrus and pseudopregnancy in rats. Endocrinology. 1947;40:65–72.

    CAS  PubMed  Article  Google Scholar 

  39. 39.

    Oshima I, Morishita H, Omura K, Saito S. Changes in hypothalamic LH-RH content and blood levels of LH-RH, gonadotropin and estradiol during the preovulatory stage of rat estrous cycle. Endocrinol Jpn. 1978;25:607–11.

    CAS  PubMed  Article  Google Scholar 

  40. 40.

    Silveyra P, Catalano PN, Lux-Lantos V, Libertun C. Impact of proestrous milieu on expression of orexin receptors and prepro-orexin in rat hypothalamus and hypophysis: actions of Cetrorelix and Nembutal. Am J Physiol Endocrinol Metab. 2007;292:E820–8.

    CAS  PubMed  Article  Google Scholar 

  41. 41.

    Colvin GB, Whitmoyer DI, Sawyer CH. Circadian sleep-wakefulness patterns in rats after ovariectomy and treatment with estrogen. Exp Neurol. 1969;25:616–25.

    CAS  PubMed  Article  Google Scholar 

  42. 42.

    Kawashima S, Shinoda A. Spontaneous activity of neonatally estrogenized female rats. Endocrinol Jpn. 1968;15:305–12.

    CAS  PubMed  Article  Google Scholar 

  43. 43.

    Hagan JJ, Leslie RA, Patel S, Evans ML, Wattam TA, Holmes S, et al. Orexin A activates locus coeruleus cell firing and increases arousal in the rat. Proc Natl Acad Sci USA. 1999;96:10911–6.

    CAS  PubMed  Article  Google Scholar 

  44. 44.

    Kiwaki K, Kotz CM, Wang C, Lanningham-Foster L, Levine JA. Orexin A (hypocretin 1) injected into hypothalamic paraventricular nucleus and spontaneous physical activity in rats. Am J Physiol Endocrinol Metab. 2004;286:E551–9.

    CAS  PubMed  Article  Google Scholar 

  45. 45.

    Nichols J, Gardner RL. Effect of damage to the zona pellucida on development of preimplantation embryos in the mouse. Hum Reprod. 1989;4:180–7.

    CAS  PubMed  Article  Google Scholar 

  46. 46.

    Schwartz MD, Mong JA. Estradiol suppresses recovery of REM sleep following sleep deprivation in ovariectomized female rats. Physiol Behav. 2011;104:962–71.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  47. 47.

    Williams NI, Berga SL, Cameron JL. Synergism between psychosocial and metabolic stressors: impact on reproductive function in cynomolgus monkeys. Am J Physiol Endocrinol Metab. 2007;293:E270–6.

    CAS  PubMed  Article  Google Scholar 

  48. 48.

    Luo E, Stephens SB, Chaing S, Munaganuru N, Kauffman AS, Breen KM. Corticosterone blocks ovarian cyclicity and the LH surge via decreased kisspeptin neuron activation in female mice. Endocrinology. 2016;157:1187–99.

    CAS  PubMed  Article  Google Scholar 

  49. 49.

    Wagenmaker ER, Moenter SM. Exposure to acute psychosocial stress disrupts the luteinizing hormone surge independent of estrous cycle alterations in female mice. Endocrinology. 2017;158:2593–602.

    PubMed  PubMed Central  Article  Google Scholar 

  50. 50.

    Basner M, Samel A, Isermann U. Aircraft noise effects on sleep: application of the results of a large polysomnographic field study. J Acoust Soc Am. 2006;119(5 Pt 1):2772–84.

    PubMed  Article  Google Scholar 

  51. 51.

    Reutrakul S, Van Cauter E. Sleep influences on obesity, insulin resistance, and risk of type 2 diabetes. Metabolism. 2018;84:56–66.

    CAS  Article  Google Scholar 

  52. 52.

    Koban M, Swinson KL. Chronic REM-sleep deprivation of rats elevates metabolic rate and increases UCP1 gene expression in brown adipose tissue. Am J Physiol Endocrinol Metab. 2005;289:E68–74.

    CAS  PubMed  Article  Google Scholar 

  53. 53.

    Martins PJ, Marques MS, Tufik S, D’Almeida V. Orexin activation precedes increased NPY expression, hyperphagia, and metabolic changes in response to sleep deprivation. Am J Physiol Endocrinol Metab. 2010;298:E726–34.

    CAS  PubMed  Article  Google Scholar 

  54. 54.

    Richard D. Effects of ovarian hormones on energy balance and brown adipose tissue thermogenesis. Am J Physiol. 1986;250(2 Pt 2):R245–9.

    CAS  PubMed  Google Scholar 

  55. 55.

    Wade GN, Zucker I. Modulation of food intake and locomotor activity in female rats by diencephalic hormone implants. J Comp Physiol Psychol. 1970;72:328–36.

    CAS  PubMed  Article  Google Scholar 

  56. 56.

    Rodrigues NR, Macedo GE, Martins IK, Gomes KK, de Carvalho NR, Posser T, et al. Short-term sleep deprivation with exposure to nocturnal light alters mitochondrial bioenergetics in Drosophila. Free Radic Biol Med. 2018;120:395–406.

    CAS  PubMed  Article  Google Scholar 

  57. 57.

    Rangtell FH, Schmidt F, Wurfel J, Karamchedu S, Andersson P, Vogel H, et al. Morning enzymatic activity of DPP-4 is differentially altered by sleep loss in women and men. Diabetes Care. 2018;41:e10–e1.

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgements

Funding for the publication was supported by the National Institutes of Health NS099468–01A1 (JAT), a CONICYT grant Fondecyt Regular 1150274 (CEP-L), and the USDA ARZT-1372540-R23–131 (JAT).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jennifer A. Teske.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Coborn, J.E., Lessie, R.E., Sinton, C.M. et al. Noise-induced sleep disruption increases weight gain and decreases energy metabolism in female rats. Int J Obes 43, 1759–1768 (2019). https://doi.org/10.1038/s41366-018-0293-9

Download citation

Further reading

Search