Hypoxia Differentially Affects Healthy Men and Women During a Daytime Nap With a Dose-Response Relationship: a Randomized, Cross-Over Pilot Study

Alain Riveros-Rivera, Thomas Penzel, Hanns-Christian Gunga, Oliver Opatz, Friedemann Paul, Lars Klug, Michael Boschmann, Anja Mähler, Alain Riveros-Rivera, Thomas Penzel, Hanns-Christian Gunga, Oliver Opatz, Friedemann Paul, Lars Klug, Michael Boschmann, Anja Mähler

Abstract

Context: The use of daytime napping as a countermeasure in sleep disturbances has been recommended but its physiological evaluation at high altitude is limited. Objective: To evaluate the neuroendocrine response to hypoxic stress during a daytime nap and its cognitive impact. Design, Subject, and Setting: Randomized, single-blind, three period cross-over pilot study conducted with 15 healthy lowlander subjects (8 women) with a mean (SD) age of 29(6) years (Clinicaltrials identifier: NCT04146857, https://ichgcp.net/clinical-trials-registry/NCT04146857?cond=napping&draw=3&rank=12). Interventions: Volunteers underwent a polysomnography, hematological and cognitive evaluation around a 90 min midday nap, being allocated to a randomized sequence of three conditions: normobaric normoxia (NN), normobaric hypoxia at FiO2 14.7% (NH15) and 12.5% (NH13), with a washout period of 1 week between conditions. Results: Primary outcome was the interbeat period measured by the RR interval with electrocardiogram. Compared to normobaric normoxia, RR during napping was shortened by 57 and 206 ms under NH15 and NH13 conditions, respectively (p < 0.001). Sympathetic predominance was evident by heart rate variability analysis and increased epinephrine levels. Concomitantly, there were significant changes in endocrine parameters such as erythropoietin (∼6 UI/L) and cortisol (∼100 nmol/L) (NH13 vs. NN, p < 0.001). Cognitive evaluation revealed changes in the color-word Stroop test. Additionally, although sleep efficiency was preserved, polysomnography showed lesser deep sleep and REM sleep, and periodic breathing, predominantly in men. Conclusion: Although napping in simulated altitude does not appear to significantly affect cognitive performance, sex-dependent changes in cardiac autonomic modulation and respiratory pattern should be considered before napping is prescribed as a countermeasure.

Keywords: autonomic nervous system; high altitude (low air pressure); hypoxia; napping; physiological stress; sleep.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2022 Riveros-Rivera, Penzel, Gunga, Opatz, Paul, Klug, Boschmann and Mähler.

Figures

FIGURE 1
FIGURE 1
CONSORT 2010 flow diagram (A) and study protocol (B).
FIGURE 2
FIGURE 2
Correlations of after nap stress hormone levels (EPO, cortisol, norepinephrine) with HRV parameters measured after, during and after the nap. Positive correlations are displayed in light gray and negative correlations in dark gray. Circle size and intensity are proportional to the correlation coefficients. *p < 0.05 (Pearson’s r).
FIGURE 3
FIGURE 3
Peripheral oxygen saturation (SpO2) (A) and cortisol (B) and erythropoietin (EPO) (C) concentrations after a 90 min nap under normoxic (NN) and hypoxic conditions (NH15: FiO2 14.7, NH13: FiO2 12.5) in healthy men (n = 7) and women (n = 8). Data as mean ± SEM. *p < 0.05, **p < 0.001 (Linear Mixed Model). Frequency of high concentration of epinephrine and dopamine (D). Missing data due to blood specimen damage during processing.
FIGURE 4
FIGURE 4
Apnea-Hypopnea Index (AHI) (A) and Periodic Breathing Index (PBI) (B) during a 90 min nap under normoxic (NN) and hypoxic conditions (NH15: FiO2 14.7, NH13: FiO2 12.5) in healthy men (n = 7) and women (n = 8).

References

    1. Aquino Lemos V., Antunes H. K. M., Santos R. V. T., Lira F. S., Tufik S., Mello M. T. (2012). High Altitude Exposure Impairs Sleep Patterns, Mood, and Cognitive Functions. Psychophysiol 49, 1298–1306. 10.1111/j.1469-8986.2012.01411.x
    1. Berry C. C., Moore P., Dimsdale J. E. (2006). Assessing the Trade-Offs between Crossover and Parallel Group Designs in Sleep Research. J. Sleep Res. 15, 348–357. 10.1111/j.1365-2869.2006.00546.x
    1. Bird J. D., Kalker A., Rimke A. N., Chan J. S., Chan G., Saran G., et al. (2021). Severity of central Sleep Apnea Does Not Affect Sleeping Oxygen Saturation during Ascent to High Altitude. J. Appl. Physiol. 131, 1432–1443. 10.1152/japplphysiol.00363.2021
    1. Bloch K. E., Buenzli J. C., Latshang T. D., Ulrich S. (2015). Sleep at High Altitude: Guesses and Facts. J. Appl. Physiol. 119, 1466–1480. 10.1152/japplphysiol.00448.2015
    1. Boos C. J., Vincent E., Mellor A., O’Hara J., Newman C., Cruttenden R., et al. (2017). The Effect of Sex on Heart Rate Variability at High Altitude. Med. Sci. Sports Exerc. 49, 2562–2569. 10.1249/MSS.0000000000001384
    1. Boudreau P., Yeh W. H., Dumont G. A., Boivin D. B. (2012). A Circadian Rhythm in Heart Rate Variability Contributes to the Increased Cardiac Sympathovagal Response to Awakening in the Morning. Chronobiology Int. 29, 757–768. 10.3109/07420528.2012.674592
    1. Boukhris O., Trabelsi K., Ammar A., Abdessalem R., Hsouna H., Glenn J. M., et al. (2020). A 90 Min Daytime Nap Opportunity Is Better Than 40 Min for Cognitive and Physical Performance. Ijerph 17, 4650. 10.3390/ijerph17134650
    1. Camargo G., Sampayo A. M., Peña Galindo A., Escobedo F. J., Carriazo F., Feged-Rivadeneira A. (2020). Exploring the Dynamics of Migration, Armed Conflict, Urbanization, and Anthropogenic Change in Colombia. PLoS One 15, e0242266. 10.1371/journal.pone.0242266
    1. Caravita S., Faini A., Lombardi C., Valentini M., Gregorini F., Rossi J., et al. (2015). Sex and Acetazolamide Effects on Chemoreflex and Periodic Breathing during Sleep at Altitude. Chest 147, 120–131. 10.1378/chest.14-0317
    1. Cellini N., Torre J., Stegagno L., Sarlo M. (2018). Cardiac Autonomic Activity during Daytime Nap in Young Adults. J. Sleep Res. 27, 159–164. 10.1111/jsr.12539
    1. Chapleau M. W., Sabharwal R. (2011). Methods of Assessing Vagus Nerve Activity and Reflexes. Heart Fail. Rev. 16, 109–127. 10.1007/s10741-010-9174-6
    1. Coste O., Beers P., Bogdan A., Charbuy H., Touitou Y. (2005). Hypoxic Alterations of Cortisol Circadian Rhythm in Man after Simulation of a Long Duration Flight. Steroids 70, 803–810. 10.1016/j.steroids.2005.05.003
    1. Cousins J. N., Leong R. L. F., Jamaluddin S. A., Ng A. S. C., Ong J. L., Chee M. W. L. (2021). Splitting Sleep between the Night and a Daytime Nap Reduces Homeostatic Sleep Pressure and Enhances Long-Term Memory. Sci. Rep. 11, 5275. 10.1038/s41598-021-84625-8
    1. Cousins J. N., Wong K. F., Raghunath B. L., Look C., Chee M. W. L. (2019). The Long-Term Memory Benefits of a Daytime Nap Compared with Cramming. Sleep 42. 10.1093/sleep/zsy207
    1. Cristancho E., Riveros A., Sánchez A., Peñuela O., Böning D. (2016). Diurnal Changes of Arterial Oxygen Saturation and Erythropoietin Concentration in Male and Female Highlanders. Physiol. Rep. 4, e12901. 10.14814/phy2.12901
    1. Dimai H. P., Ramschak-Schwarzer S., Leb G. (2000). Altitude Hypoxia: Effects on Selected Endocrinological Parameters. Wien. Med. Wochenschr. 150, 178–181.
    1. Dutheil F., Danini B., Bagheri R., Fantini M. L., Pereira B., Moustafa F., et al. (2021). Effects of a Short Daytime Nap on the Cognitive Performance: A Systematic Review and Meta-Analysis. Ijerph 18, 10212. 10.3390/ijerph181910212
    1. Elmenhorst E.-M., Rooney D., Benderoth S., Wittkowski M., Wenzel J., Aeschbach D. (2022). Sleep-Induced Hypoxia under Flight Conditions: Implications and Countermeasures for Long-Haul Flight Crews and Passengers. Nss Vol. 14, 193–205. 10.2147/NSS.S339196
    1. Faraut B., Andrillon T., Vecchierini M.-F., Leger D. (2017). Napping: A Public Health Issue. From Epidemiological to Laboratory Studies. Sleep Med. Rev. 35, 85–100. 10.1016/j.smrv.2016.09.002
    1. Fekedulegn D., Andrew M. E., Shi M., Violanti J. M., Knox S., Innes K. E. (2020). Actigraphy-Based Assessment of Sleep Parameters. Ann. Work Expo. Heal. 64, 350–367. 10.1093/annweh/wxaa007
    1. Ferrini R. L., Barrett-Connor E. (1998). Sex Hormones and Age: a Cross-Sectional Study of Testosterone and Estradiol and Their Bioavailable Fractions in Community-Dwelling Men. Am. J. Epidemiol. 147, 750–754. 10.1093/oxfordjournals.aje.a009519
    1. Fultz N. E., Bonmassar G., Setsompop K., Stickgold R. A., Rosen B. R., Polimeni J. R., et al. (2019). Coupled Electrophysiological, Hemodynamic, and Cerebrospinal Fluid Oscillations in Human Sleep. Science 366, 628–631. 10.1126/science.aax5440
    1. Gaiduk M., Perea J. J., Seepold R., Martinez Madrid N., Penzel T., Glos M., et al. (2022). Estimation of Sleep Stages Analyzing Respiratory and Movement Signals. IEEE J. Biomed. Health Inform. 26, 505–514. 10.1109/JBHI.2021.3099295
    1. Gargaglioni L. H., Marques D. A., Patrone L. G. A. (2019). Sex Differences in Breathing. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 238, 110543. 10.1016/j.cbpa.2019.110543
    1. Gerber M., Lang C., Lemola S., Colledge F., Kalak N., Holsboer-Trachsler E., et al. (2016). Validation of the German Version of the Insomnia Severity index in Adolescents, Young Adults and Adult Workers: Results from Three Cross-Sectional Studies. BMC Psychiatry 16, 174. 10.1186/s12888-016-0876-8
    1. Harris P. A., Taylor R., Thielke R., Payne J., Gonzalez N., Conde J. G. (2009). Research Electronic Data Capture (REDCap)-A Metadata-Driven Methodology and Workflow Process for Providing Translational Research Informatics Support. J. Biomed. Inform. 42, 377–381. 10.1016/j.jbi.2008.08.010
    1. Hauer M. E., Fussell E., Mueller V., Burkett M., Call M., Abel K., et al. (2020). Sea-level Rise and Human Migration. Nat. Rev. Earth Environ. 1, 28–39. 10.1038/s43017-019-0002-9
    1. Heart rate variability (1996). Standards of Measurement, Physiological Interpretation, and Clinical Use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Eur. Heart J. 17, 354–381.
    1. Herzig D., Eser P., Omlin X., Riener R., Wilhelm M., Achermann P. (2018). Reproducibility of Heart Rate Variability Is Parameter and Sleep Stage Dependent. Front. Physiol. 8, 1–10. 10.3389/fphys.2017.01100
    1. Hill C. M., Bucks R. S., Cellini N., Motamedi S., Carroll A., Heathcote K., et al. (2018). Cardiac Autonomic Activity during Sleep in High-Altitude Resident Children Compared with lowland Residents. Sleep 41. 10.1093/sleep/zsy181
    1. Horiuchi M., Oda S., Uno T., Endo J., Handa Y., Fukuoka Y. (2017). Effects of Short-Term Acclimatization at the Summit of Mt. Fuji (3776 M) on Sleep Efficacy, Cardiovascular Responses, and Ventilatory Responses. High Alt. Med. Biol. 18, 171–178. 10.1089/ham.2016.0162
    1. Hoshikawa M., Uchida S., Sugo T., Kumai Y., Hanai Y., Kawahara T. (20072005–2011). Changes in Sleep Quality of Athletes under Normobaric Hypoxia Equivalent to 2,000-m Altitude: a Polysomnographic Study. J. Appl. Physiol. 103, 2005–2011. 10.1152/japplphysiol.00315.2007
    1. Hughes B. H., Brinton J. T., Ingram D. G., Halbower A. C. (2017). The Impact of Altitude on Sleep-Disordered Breathing in Children Dwelling at High Altitude: A Crossover Study. Sleep 40. 10.1093/sleep/zsx120
    1. Humphreys S., Deyermond R., Bali I., Stevenson M., Fee J. P. H. (2005). The Effect of High Altitude Commercial Air Travel on Oxygen Saturation. Anaesthesia 60, 458–460. 10.1111/j.1365-2044.2005.04124.x
    1. IATA (2020). Annual Review. 76th Annual General Meeting. Amsterdam-Netherlands Available at: .
    1. Insalaco G., Salvaggio A., Pomidori L., Cogo A., Romano S. (2016). Heart Rate Variability during Sleep at High Altitude: Effect of Periodic Breathing. Sleep Breath 20, 197–204. 10.1007/s11325-015-1205-z
    1. Jiang F., Kobayashi T., Ichihashi T., Nomura S. (2018). Effect of a Relatively Long Afternoon Nap on Autonomous Nervous Activity, Sleep Architecture, and Subjective Sleep Quality. IEEJ Trans. Elec Electron. Eng. 13, 1357–1361. 10.1002/tee.22702
    1. Ju J.-D., Zhang C., Sgambati F. P., Lopez L. M., Pham L. V., Schwartz A. R., et al. (2021). Acute Altitude Acclimatization in Young Healthy Volunteers: Nocturnal Oxygenation Increases over Time, whereas Periodic Breathing Persists. High Alt. Med. Biol. 22, 14–23. 10.1089/ham.2020.0009
    1. Julious S. A. (2005). Sample Size of 12 Per Group Rule of Thumb for a Pilot Study. Pharmaceut. Statist. 4, 287–291. 10.1002/pst.185
    1. Keenan D. M., Pichler Hefti J., Veldhuis J. D., Von Wolff M. (2020). Regulation and Adaptation of Endocrine Axes at High Altitude. Am. J. Physiology-Endocrinology Metab. 318, E297–E309. 10.1152/ajpendo.00243.2019
    1. Klug L., Mähler A., Rakova N., Mai K., Schulz-Menger J., Rahn G., et al. (2018). Normobaric Hypoxic Conditioning in Men with Metabolic Syndrome. Physiol. Rep. 6, e13949. 10.14814/phy2.13949
    1. Lastella M., Halson S. L., Vitale J. A., Memon A. R., Vincent G. E. (2021). To Nap or Not to Nap? A Systematic Review Evaluating Napping Behavior in Athletes and the Impact on Various Measures of Athletic Performance. Nss Vol. 13, 841–862. 10.2147/NSS.S315556
    1. Latshang T. D., Lo Cascio C. M., Stöwhas A.-C., Grimm M., Stadelmann K., Tesler N., et al. (20131976). Are Nocturnal Breathing, Sleep, and Cognitive Performance Impaired at Moderate Altitude (1,630-2,590 M)? Sleep 36, 1969–1976. 10.5665/sleep.3242
    1. Lee Y. J., Lee J. Y., Cho J. H., Choi J. H. (2022). Interrater Reliability of Sleep Stage Scoring: a Meta-Analysis. J. Clin. Sleep Med. 18, 193–202. 10.5664/jcsm.9538
    1. Lerchbaum E., Schwetz V., Rabe T., Giuliani A., Obermayer-Pietsch B. (2014). Hyperandrogenemia in Polycystic Ovary Syndrome: Exploration of the Role of Free Testosterone and Androstenedione in Metabolic Phenotype. PLoS One 9, e108263. 10.1371/journal.pone.0108263
    1. Leuenberger U., Gleeson K., Wroblewski K., Prophet S., Zelis R., Zwillich C., et al. (1991). Norepinephrine Clearance Is Increased during Acute Hypoxemia in Humans. Am. J. Physiology-Heart Circulatory Physiol. 261, H1659–H1664. 10.1152/ajpheart.1991.261.5.H1659
    1. Littlejohn E. L., Fedorchak S., Boychuk C. R. (2020). Sex-steroid-dependent Plasticity of Brain-Stem Autonomic Circuits. Am. J. Physiology-Regulatory, Integr. Comp. Physiol. 319, R60–R68. 10.1152/ajpregu.00357.2019
    1. Loh S., Lamond N., Dorrian J., Roach G., Dawson D. (2004). The Validity of Psychomotor Vigilance Tasks of Less Than 10-minute Duration. Behav. Res. Methods Instr. Comput. 36, 339–346. 10.3758/bf03195580
    1. Lombardi C., Meriggi P., Agostoni P., Faini A., Bilo G., Revera M., et al. (2013). High-altitude Hypoxia and Periodic Breathing during Sleep: Gender-Related Differences. J. Sleep Res. 22, 322–330. 10.1111/jsr.12012
    1. MacDonald E. A., Rose R. A., Quinn T. A. (2020). Neurohumoral Control of Sinoatrial Node Activity and Heart Rate: Insight from Experimental Models and Findings from Humans. Front. Physiol. 11, 170. 10.3389/fphys.2020.00170
    1. Mackenzie R. W. A., Watt P. W., Maxwell N. S. (2008). Acute Normobaric Hypoxia Stimulates Erythropoietin Release. High Alt. Med. Biol. 9, 28–37. 10.1089/ham.2007.1043
    1. Mähler A., Balogh A., Csizmadia I., Klug L., Kleinewietfeld M., Steiniger J., et al. (2018). Metabolic, Mental and Immunological Effects of Normoxic and Hypoxic Training in Multiple Sclerosis Patients: A Pilot Study. Front. Immunol. 9, 2819. 10.3389/fimmu.2018.02819
    1. Malik M., Bigger J. T., Camm A. J., Kleiger R. E., Malliani A., Moss A. J., et al. (1996). Heart Rate Variability: Standards of Measurement, Physiological Interpretation, and Clinical Use. Eur. Heart J. 17, 354–381. 10.1093/oxfordjournals.eurheartj.a014868
    1. Manzar M. D., Sethi M., Hussain M. E. (2012). Humidity and Sleep: a Review on thermal Aspect. Biol. Rhythm Res. 43, 439–457. 10.1080/09291016.2011.597621
    1. McDevitt E. A., Sattari N., Duggan K. A., Cellini N., Whitehurst L. N., Perera C., et al. (2018). The Impact of Frequent Napping and Nap Practice on Sleep-dependent Memory in Humans. Sci. Rep. 8, 15053. 10.1038/s41598-018-33209-0
    1. McMorris T., Hale B. J., Barwood M., Costello J., Corbett J. (2017). Effect of Acute Hypoxia on Cognition: A Systematic Review and Meta-Regression Analysis. Neurosci. Biobehavioral Rev. 74, 225–232. 10.1016/j.neubiorev.2017.01.019
    1. Millet G. P., Faiss R., Pialoux V. (2012). Point: Counterpoint: Hypobaric Hypoxia Induces/does Not Induce Different Responses from Normobaric Hypoxia. J. Appl. Physiol. 112, 1783–1784. 10.1152/japplphysiol.00067.2012
    1. Milner C. E., Cote K. A. (2009). Benefits of Napping in Healthy Adults: Impact of Nap Length, Time of Day, Age, and Experience with Napping. J. Sleep Res. 18, 272–281. 10.1111/j.1365-2869.2008.00718.x
    1. Mohd Azmi N. A. S., Juliana N., Azmani S., Mohd Effendy N., Abu I. F., Mohd Fahmi Teng N. I., et al. (2021). Cortisol on Circadian Rhythm and its Effect on Cardiovascular System. Ijerph 18, 676. 10.3390/ijerph18020676
    1. Mounier R., Brugniaux J. V. (2012). Counterpoint: Hypobaric Hypoxia Does Not Induce Different Responses from Normobaric Hypoxia. J. Appl. Physiol. 112, 1784–1786. 10.1152/japplphysiol.00067.2012a
    1. Mueller S. T., Piper B. J. (2014). The Psychology Experiment Building Language (PEBL) and PEBL Test Battery. J. Neurosci. Methods 222, 250–259. 10.1016/j.jneumeth.2013.10.024
    1. Mugele H., Oliver S. J., Gagnon D., Lawley J. S. (2021). Integrative Crosstalk between Hypoxia and the Cold: Old Data and New Opportunities. Exp. Physiol. 106, 350–358. 10.1113/EP088512
    1. Muhm J. M., Signal T. L., Rock P. B., Jones S. P., O'Keeffe K. M., Weaver M. R., et al. (2009). Sleep at Simulated 2438 M: Effects on Oxygenation, Sleep Quality, and Postsleep Performance. Aviat. Space Environ. Med. 80, 691–697. 10.3357/asem.2327.2009
    1. Nunan D., Sandercock G. R. H., Brodie D. A. (2010). A Quantitative Systematic Review of normal Values for Short-Term Heart Rate Variability in Healthy Adults. PACE - Pacing Clin. Electrophysiol. 33, 1407–1417. 10.1111/j.1540-8159.2010.02841.x
    1. Okamoto-Mizuno K., Mizuno K. (2012). Effects of thermal Environment on Sleep and Circadian Rhythm. J. Physiol. Anthropol. 31, 14. 10.1186/1880-6805-31-14
    1. Panjwani U., Thakur L., Anand J. P., Malhotra A. S., Banerjee P. K. (2006). Effect of Simulated Ascent to 3500 Meter on Neuro-Endocrine Functions. Indian J. Physiol. Pharmacol. 50, 250–256.
    1. Phillips J. B., Hørning D., Funke M. E. (2015). Cognitive and Perceptual Deficits of Normobaric Hypoxia and the Time Course to Performance Recovery. Aerospace Med. Hum. Perform. 86, 357–365. 10.3357/amhp.3925.2015
    1. Pramsohler S., Schilz R., Patzak A., Rausch L., Netzer N. C. (2019). Periodic Breathing in Healthy Young Adults in Normobaric Hypoxia Equivalent to 3500 M, 4500 M, and 5500 M Altitude. Sleep Breath 23, 703–709. 10.1007/s11325-019-01829-z
    1. Qian L., Ru T., Chen Q., Li Y., Zhou Y., Zhou G. (2020). Effects of Bright Light and an Afternoon Nap on Task Performance Depend on the Cognitive Domain. J. Sleep Res. 30, e13242. 10.1111/jsr.13242
    1. Rowell L. B., Johnson D. G., Chase P. B., Comess K. A., Seals D. R. (1989). Hypoxemia Raises Muscle Sympathetic Activity but Not Norepinephrine in Resting Humans. J. Appl. Physiol. 66, 1736–1743. 10.1152/jappl.1989.66.4.1736
    1. Schaedler T., Santos J. S., Vincenzi R. A., Pereira S. I. R., Louzada F. M. (2018). Executive Functioning Is Preserved in Healthy Young Adults under Acute Sleep Restriction. Sleep Sci. (Sao Paulo, Brazil) 11, 152–159. 10.5935/1984-0063.20180029
    1. Schulz A., Richter S., Ferreira de Sá D. S., Vögele C., Schächinger H. (2020). Cortisol Rapidly Increases Baroreflex Sensitivity of Heart Rate Control, but Does Not Affect Cardiac Modulation of Startle. Physiol. Behav. 215, 112792. 10.1016/j.physbeh.2019.112792
    1. Silber M. H., Ancoli-Israel S., Bonnet M. H., Chokroverty S., Grigg-Damberger M. M., Hirshkowitz M., et al. (2007). The Visual Scoring of Sleep in Adults. J. Clin. Sleep Med. 03, 121–131. 10.5664/jcsm.26814
    1. Simka M., Latacz P., Czaja J. (2018). Possible Role of Glymphatic System of the Brain in the Pathogenesis of High-Altitude Cerebral Edema. High Alt. Med. Biol. 19, 394–397. 10.1089/ham.2018.0066
    1. Souissi W., Hammouda O., Ayachi M., Ammar A., Khcharem A., de Marco G., et al. (2020). Partial Sleep Deprivation Affects Endurance Performance and Psychophysiological Responses during 12-minute Self-Paced Running Exercise. Physiol. Behav. 227, 113165. 10.1016/j.physbeh.2020.113165
    1. Steier J., Cade N., Walker B., Moxham J., Jolley C. (2017). Observational Study of Neural Respiratory Drive during Sleep at High Altitude. High Alt. Med. Biol. 18, 242–248. 10.1089/ham.2016.0097
    1. Suzuki M., Taniguchi T., Furihata R., Yoshita K., Arai Y., Yoshiike N., et al. (2019). Seasonal Changes in Sleep Duration and Sleep Problems: A Prospective Study in Japanese Community Residents. PLoS One 14, e0215345. 10.1371/journal.pone.0215345
    1. Tarvainen M. P., Niskanen J.-P., Lipponen J. A., Ranta-Aho P. O., Karjalainen P. A. (2014). Kubios HRV - Heart Rate Variability Analysis Software. Comput. Methods Programs Biomed. 113, 210–220. 10.1016/j.cmpb.2013.07.024
    1. Tobaldini, E E., Pecis M., Montano N. (2015). Effects of Acute and Chronic Sleep Deprivation on Cardiovascular Regulation. Arch. Ital. Biol. 152, 103–110. 10.12871/000298292014235
    1. Tseng C.-H., Lin F.-C., Chao H.-S., Tsai H.-C., Shiao G.-M., Chang S.-C. (2015). Impact of Rapid Ascent to High Altitude on Sleep. Sleep Breath 19, 819–826. 10.1007/s11325-014-1093-7
    1. Van Dongen H. P. A., Maislin G., Mullington J. M., Dinges D. F. (2003). The Cumulative Cost of Additional Wakefulness: Dose-Response Effects on Neurobehavioral Functions and Sleep Physiology from Chronic Sleep Restriction and Total Sleep Deprivation. Sleep 26, 117–126. 10.1093/sleep/26.2.117
    1. Voderholzer U., Piosczyk H., Holz J., Feige B., Loessl B., Kopasz M., et al. (2012). The Impact of Increasing Sleep Restriction on Cortisol and Daytime Sleepiness in Adolescents. Neurosci. Lett. 507, 161–166. 10.1016/j.neulet.2011.12.014
    1. Weibel J., Lin Y.-S., Landolt H.-P., Garbazza C., Kolodyazhniy V., Kistler J., et al. (2020). Caffeine-dependent Changes of Sleep-Wake Regulation: Evidence for Adaptation after Repeated Intake. Prog. Neuro-Psychopharmacology Biol. Psychiatry 99, 109851. 10.1016/j.pnpbp.2019.109851
    1. Wu H., Stone W., Hsi X., Zhuang J., Huang L., Yin Y., et al. (2010). Effects of Different Sleep Restriction Protocols on Sleep Architecture and Daytime Vigilance in Healthy Men. Physiol. Res. 59, 821–829. 10.33549/physiolres.931895
    1. Wurtman R. J. (2002). Stress and the Adrenocortical Control of Epinephrine Synthesis. Metabolism 51, 11–14. 10.1053/meta.2002.33185
    1. Xie L., Kang H., Xu Q., Chen M. J., Liao Y., Thiyagarajan M., et al. (2013). Sleep Drives Metabolite Clearance from the Adult Brain. Science 342, 373–377. 10.1126/science.1241224
    1. Yih M. L., Lin F.-C., Chao H.-S., Tsai H.-C., Chang S.-C. (2017). Effects of Rapid Ascent on the Heart Rate Variability of Individuals with and without Acute Mountain Sickness. Eur. J. Appl. Physiol. 117, 757–766. 10.1007/s00421-017-3555-7
    1. Zera T., Moraes D. J. A., da Silva M. P., Fisher J. P., Paton J. F. R. (2019). The Logic of Carotid Body Connectivity to the Brain. Physiology 34, 264–282. 10.1152/physiol.00057.2018

Source: PubMed

3
Se inscrever