Unstable sleep and higher sympathetic activity during late-sleep periods of rats: implication for late-sleep-related higher cardiovascular events
TERRY B. J. KUO
Sleep Research Center, National Yang-Ming University, Taipei, Taiwan
Institute of Brain Science, National Yang-Ming University, Taipei, Taiwan
Department of Education and Research, Taipei City Hospital, Taipei, Taiwan
Brain Research Center, National Yang-Ming University, Taipei, Taiwan
T.B.J.K. and C.-T.L. Contributed equally to this paper.
Search for more papers by this authorCHUN-TING LAI
Sleep Research Center, National Yang-Ming University, Taipei, Taiwan
Institute of Brain Science, National Yang-Ming University, Taipei, Taiwan
Department of Education and Research, Taipei City Hospital, Taipei, Taiwan
T.B.J.K. and C.-T.L. Contributed equally to this paper.
Search for more papers by this authorCHUN-YU CHEN
Sleep Research Center, National Yang-Ming University, Taipei, Taiwan
Institute of Brain Science, National Yang-Ming University, Taipei, Taiwan
Search for more papers by this authorGUO-SHE LEE
Sleep Research Center, National Yang-Ming University, Taipei, Taiwan
Institute of Brain Science, National Yang-Ming University, Taipei, Taiwan
Department of Education and Research, Taipei City Hospital, Taipei, Taiwan
Faculty of Medicine, National Yang-Ming University, Taipei, Taiwan
Search for more papers by this authorCHERYL C. H. YANG
Sleep Research Center, National Yang-Ming University, Taipei, Taiwan
Institute of Brain Science, National Yang-Ming University, Taipei, Taiwan
Department of Education and Research, Taipei City Hospital, Taipei, Taiwan
Brain Research Center, National Yang-Ming University, Taipei, Taiwan
Search for more papers by this authorTERRY B. J. KUO
Sleep Research Center, National Yang-Ming University, Taipei, Taiwan
Institute of Brain Science, National Yang-Ming University, Taipei, Taiwan
Department of Education and Research, Taipei City Hospital, Taipei, Taiwan
Brain Research Center, National Yang-Ming University, Taipei, Taiwan
T.B.J.K. and C.-T.L. Contributed equally to this paper.
Search for more papers by this authorCHUN-TING LAI
Sleep Research Center, National Yang-Ming University, Taipei, Taiwan
Institute of Brain Science, National Yang-Ming University, Taipei, Taiwan
Department of Education and Research, Taipei City Hospital, Taipei, Taiwan
T.B.J.K. and C.-T.L. Contributed equally to this paper.
Search for more papers by this authorCHUN-YU CHEN
Sleep Research Center, National Yang-Ming University, Taipei, Taiwan
Institute of Brain Science, National Yang-Ming University, Taipei, Taiwan
Search for more papers by this authorGUO-SHE LEE
Sleep Research Center, National Yang-Ming University, Taipei, Taiwan
Institute of Brain Science, National Yang-Ming University, Taipei, Taiwan
Department of Education and Research, Taipei City Hospital, Taipei, Taiwan
Faculty of Medicine, National Yang-Ming University, Taipei, Taiwan
Search for more papers by this authorCHERYL C. H. YANG
Sleep Research Center, National Yang-Ming University, Taipei, Taiwan
Institute of Brain Science, National Yang-Ming University, Taipei, Taiwan
Department of Education and Research, Taipei City Hospital, Taipei, Taiwan
Brain Research Center, National Yang-Ming University, Taipei, Taiwan
Search for more papers by this authorSummary
We proposed that the higher incidence of sleep fragmentation, sympathovagal imbalance and baroreceptor reflex impairment during quiet sleep may play a critical role in late-sleep-related cardiovascular events. Polysomnographic recording was performed through wireless transmission using freely moving Wistar–Kyoto rats over 24 h. The low-frequency power of arterial pressure variability was quantified to provide an index of vascular sympathetic activity. Spontaneous baroreflex sensitivity was assessed by slope of arterial pressure–RR linear regression. As compared with early-light period (Zeitgeber time 0–6 h), rats during the late-light period (Zeitgeber time 6–12 h) showed lower accumulated quiet sleep time and higher paradoxical sleep time; furthermore, during quiet sleep, the rats showed a lower δ% of electroencephalogram, more incidents of interruptions, higher σ% and higher β% of electroencephalogram, raised low-frequency power of arterial pressure variability value and lower baroreflex sensitivity parameters. During the light period, low-frequency power of arterial pressure variability during quiet sleep had a negative correlation with accumulated quiet sleep time and δ% of electroencephalogram, while it also had a positive correlation with σ% and β% of electroencephalogram and interruption events. However, late-sleep-related raised sympathetic activity and sleep fragmentation diminished when an α1-adrenoceptor antagonist was given to the rats. Our results suggest that the higher incidence of sleep fragmentation and sympathovagal imbalance during quiet sleep may play a critical role in late-sleep-related cardiovascular events. Such sleep fragmentation is coincident with an impairment of baroreflex sensitivity, and is mediated via α1-adernoceptors.
Supporting Information
Figure S1. Comparisons of duration of stage,number of stages, incidence of interruptions (event/min), deltapower percentage, theta power percentage and beta power percentageduring paradoxical sleep status using a 2-h window (left panel) anda 6-h window (right panel) among rats during light and dark(oblique line) periods over 24 h.
Figure S2. Comparisons of mean arterialpressure (MAP), R-R intervals (RR), low-frequency power (BLF) ofarterial pressure variability, normalized low-frequency power (LF%)and high-frequency power (HF) of heart rate variability duringparadoxical sleep status using a 2-h window (left panel) and a 6-hwindow (right panel) among rats during light and dark (obliqueline) periods over 24 h.
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| jsr1046_sm_Online-Supplementary-final.doc376 KB | Supporting info item |
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References
- Alfoldi, P., Franken, P., Tobler, I. and Borbely, A. A.Short light-dark cycles influence sleep stages and EEG power spectra in the rat. Behav. Brain Res., 1991, 43: 125–131.
- Argentino, C., Toni, D., Rasura, M. et al. Circadian variation in the frequency of ischemic stroke. Stroke, 1990, 21: 387–389.
- Bangash, M. F., Xie, A., Skatrud, J. B. et al. Cerebrovascular response to arousal from NREM and REM sleep. Sleep, 2008, 31: 321–327.
- Berteotti, C., Asti, V., Ferrari, V. et al. Central and baroreflex control of heart period during the wake-sleep cycle in spontaneously hypertensive rats. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2007, 293: R293–R298.
- Bjorvatn, B., Fagerland, S. and Ursin, R.EEG power densities (0.5-20 Hz) in different sleep-wake stages in rats. Physiol. Behav., 1998, 63: 413–417.
- Campbell, I. G. and Feinberg, I.Dissociation of delta EEG amplitude and incidence in rat NREM sleep. Brain Res. Bull., 1993, 30: 143–147.
- Catcheside, P. G., Chiong, S. C., Orr, R. S. et al. Acute cardiovascular responses to arousal from non-REM sleep during normoxia and hypoxia. Sleep, 2001, 24: 895–902.
- Catcheside, P. G., Chiong, S. C., Mercer, J., Saunders, N. A. and McEvoy, R. D.Noninvasive cardiovascular markers of acoustically induced arousal from non-rapid-eye-movement sleep. Sleep, 2002, 25: 797–804.
- Chen, C. Y., Yang, C. C. H., Lin, Y. Y. and Kuo, T. B. J.Locomotion-induced hippocampal theta is independent of visual information in rats during movement through a pipe. Behav. Brain Res., 2011, 216: 699–704.
- Goff, E. A., Nicholas, C. L., Simonds, A. K., Trinder, J. and Morrell, M. J.Differential effects of waking from non-rapid eye movement versus rapid eye movement sleep on cardiovascular activity. J. Sleep Res., 2010, 19: 201–206.
- Guilleminault, C., Pool, P., Motta, J. and Gillis, A. M.Sinus arrest during REM sleep in young adults. N. Engl. J. Med., 1984, 311: 1006–1010.
- Hu, K., Scheer, F. A., Laker, M., Smales, C. and Shea, S. A.Endogenous circadian rhythm in vasovagal response to head-up tilt. Circulation, 2011, 123: 961–970.
- Iellamo, F., Placidi, F., Marciani, M. G. et al. Baroreflex buffering of sympathetic activation during sleep: evidence from autonomic assessment of sleep macroarchitecture and microarchitecture. Hypertension, 2004, 43: 814–819.
- Kario, K., Pickering, T. G., Hoshide, S. et al. Morning blood pressure surge and hypertensive cerebrovascular disease: role of the alpha adrenergic sympathetic nervous system. Am. J. Hypertens, 2004, 17: 668–675.
- Kato, T., Montplaisir, J. Y. and Lavigne, G. J.Experimentally induced arousals during sleep: a cross-modality matching paradigm. J. Sleep Res., 2004, 13: 229–238.
- Kawano, Y.Diurnal blood pressure variation and related behavioral factors. Hypertens. Res., 2011, 34: 281–285.
- Kleinlogel, H.Effects of the selective alpha 1-adrenoceptor blocker prazosin on EEG sleep and waking stages in the rat. Neuropsychobiology, 1989, 21: 100–103.
- Kuo, T. B. J. and Yang, C. C. H.Sleep-related changes in cardiovascular neural regulation in spontaneously hypertensive rats. Circulation, 2005, 112: 849–854.
- Kuo, T. B. J., Lin, T., Yang, C. C. H. et al. Effect of aging on gender differences in neural control of heart rate. Am. J. Physiol., 1999, 277: H2233–H2239.
- Kuo, T. B. J., Lai, C. J., Huang, Y. T. and Yang, C. C. H.Regression analysis between heart rate variability and baroreflex-related vagus nerve activity in rats. J. Cardiovasc. Electrophysiol., 2005, 16: 864–869.
- Kuo, T. B. J., Shaw, F. Z., Lai, C. J. and Yang, C. C. H.Asymmetry in sympathetic and vagal activities during sleep-wake transitions. Sleep, 2008, 31: 311–320.
- Kuo, T. B. J., Chen, C. Y., Lai, C. T. et al. Sleep disturbance among spontaneously hypertensive rats is mediated by an α1-adrenergic mechanism. Am. J. Hypertension, 2012, in press.
- Legramante, J. M., Marciani, M. G., Placidi, F. et al. Sleep-related changes in baroreflex sensitivity and cardiovascular autonomic modulation. J. Hypertens, 2003, 21: 1555–1561.
- Li, Y., Thijs, L., Hansen, T. W. et al. Prognostic value of the morning blood pressure surge in 5645 subjects from 8 populations. Hypertension, 2010, 55: 1040–1048.
- Miki, K., Kato, M. and Kajii, S.Relationship between renal sympathetic nerve activity and arterial pressure during REM sleep in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2003, 284: R467–R473.
- Muller, J. E., Stone, P. H., Turi, Z. G. et al. Circadian variation in the frequency of onset of acute myocardial infarction. N. Engl. J. Med., 1985, 313: 1315–1322.
- Nelson, L. E., Lu, J., Guo, T. et al. The alpha2-adrenoceptor agonist dexmedetomidine converges on an endogenous sleep-promoting pathway to exert its sedative effects. Anesthesiology, 2003, 98: 428–436.
- Pellejero, T., Monti, J. M., Baglietto, J. et al. Effects of methoxamine and alpha-adrenoceptor antagonists, prazosin and yohimbine, on the sleep-wake cycle of the rat. Sleep, 1984, 7: 365–372.
- Rosenberg, R. S., Bergmann, B. M. and Rechtschaffen, A.Variations in slow wave activity during sleep in the rat. Physiol. Behav., 1976, 17: 931–938.
- Saper, C. B., Fuller, P. M., Pedersen, N. P., Lu, J. and Scammell, T. E.Sleep state switching. Neuron, 2010, 68: 1023–1042.
- Scheer, F. A., Hilton, M. F., Mantzoros, C. S. and Shea, S. A.Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc. Natl Acad. Sci. USA, 2009, 106: 4453–4458.
- Silvani, A., Bastianini, S., Berteotti, C. et al. Central and baroreflex control of heart period during the wake-sleep cycle in consomic rats with different genetic susceptibility to hypertension. Clin. Exp. Pharmacol. Physiol., 2010, 37: 322–327.
- Smolensky, M. H., Hermida, R. C., Castriotta, R. J. and Portaluppi, F.Role of sleep-wake cycle on blood pressure circadian rhythms and hypertension. Sleep Med., 2007, 8: 668–680.
- Somers, V. K., Dyken, M. E., Mark, A. L. and Abboud, F. M.Sympathetic-nerve activity during sleep in normal subjects. N. Engl. J. Med., 1993, 328: 303–307.
- Task Force of the European Society of Cardiology and the North American Society of Pacing, ElectrophysiologyHeart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation, 1996, 93: 1043–1065.
- Uchida, S., Maloney, T., March, J. D., Azari, R. and Feinberg, I.Sigma (12–15 Hz) and delta (0.3–3 Hz) EEG oscillate reciprocally within NREM sleep. Brain Res. Bull., 1991, 27: 93–96.
- Wolk, R., Gami, A. S., Garcia-Touchard, A. and Somers, V. K.Sleep and cardiovascular disease. Curr. Probl. Cardiol., 2005, 30: 625–662.
- Yang, C. C. H., Kuo, T. B. J. and Chan, S. H. H.Auto- and cross-spectral analysis of cardiovascular fluctuations during pentobarbital anesthesia in the rat. Am. J. Physiol., 1996, 270: H575–H582.
- Yang, C. C. H., Lai, C. W., Lai, H. Y. and Kuo, T. B. J.Relationship between electroencephalogram slow-wave magnitude and heart rate variability during sleep in humans. Neurosci. Lett., 2002, 329: 213–216.
- Yoshimoto, M., Yoshida, I. and Miki, K.Functional role of diverse changes in sympathetic nerve activity in regulating arterial pressure during REM sleep. Sleep, 2011, 34: 1093–1101.
- Zoccoli, G., Andreoli, E., Bojic, T. et al. Central and baroreflex control of heart rate during the wake-sleep cycle in rat. Sleep, 2001, 24: 753–758.
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