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Suppressing cardiac vagal modulation and changing sleep patterns in rats after chronic ischemic stroke injury

      Abstract

      Chronic autonomic function and sleep architecture changes in patients post-stroke are not well understood. Using wireless polysomnographic recordings, this study aimed to investigate the long-term effects on sleep patterns and autonomic function in free moving rats after middle cerebral artery occlusion (MCAO). The sleep pattern and heart rate variability (HRV) of Wistar-Kyoto rats (WKY) were analyzed. After 7–10 days, the rats were divided into two groups: an MCAO group (n=8) and a sham surgery group (n=8). Compared with shams, MCAO rats showed decreased accumulated quiet sleep (QS) time over 24 h during the 3rd week. The time percentage, duration and delta power of QS were also significantly decreased in the MCAO group during the dark period. Compared with baseline, there were significant increases in the parasympathetic-associated HRV measures in the sham group, including the total power (TP), high frequency power (HF) and lower frequency power (LF), throughout the post-operative weeks (primarily the 2nd and 3rd weeks), reflecting a developmental increase of parasympathetic modulation; the normalized LF and the LF–HF ratio were unaffected. In great contrast, however, most of the HRV measures in the MCAO group were not significantly changed. Therefore, this study showed that the long-term effects of ischemic stroke injury involve retardation of the establishment of parasympathetic enhancement and disturbance of the normal sleep–wake cycle.

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      References

        • Bassetti C.L.
        • Aldrich M.S.
        Sleep electroencephalogram changes in acute hemispheric stroke.
        Sleep Med. 2001; 2: 185-194
        • Bassi A.
        • Colivicchi F.
        • Santini M.
        • Caltagirone C.
        Cardiac autonomic dysfunction and functional outcome after ischaemic stroke.
        Eur. J. Neurol. 2007; 14: 917-922
        • Baumann C.R.
        • Kilic E.
        • Petit B.
        • Werth E.
        • Hermann D.M.
        • Tafti M.
        • Bassetti C.L.
        Sleep EEG changes after middle cerebral artery infarcts in mice: different effects of striatal and cortical lesions.
        Sleep. 2006; 29: 1339-1344
        • Chen S.T.
        • Hsu C.Y.
        • Hogan E.L.
        • Maricq H.
        • Balentine J.D.
        A model of focal ischemic stroke in the rat: reproducible extensive cortical infarction.
        Stroke. 1986; 17: 738-743
        • Chen C.Y.
        • Yang C.C.H.
        • Lin Y.Y.
        • 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
        • Dutsch M.
        • Burger M.
        • Dorfler C.
        • Schwab S.
        • Hilz M.J.
        Cardiovascular autonomic function in poststroke patients.
        Neurology. 2007; 69: 2249-2255
        • Erciyas A.H.
        • Topalkara K.
        • Topaktas S.
        • Akyuz A.
        • Dener S.
        Suppression of cardiac parasympathetic functions in patients with right hemispheric stroke.
        Eur. J. Neurol. 1999; 6: 685-690
        • Hermann D.M.
        • Bassetti C.L.
        Sleep-related breathing and sleep–wake disturbances in ischemic stroke.
        Neurology. 2009; 73: 1313-1322
        • Huang S.S.
        • Tsai S.K.
        • Chih C.L.
        • Chiang L.Y.
        • Hsieh H.M.
        • Teng C.M.
        • Tsai M.C.
        Neuroprotective effect of hexasulfobutylated C60 on rats subjected to focal cerebral ischemia.
        Free Radic. Biol. Med. 2001; 30: 643-649
        • Hunter A.J.
        • Mackay K.B.
        • Rogers D.C.
        To what extent have functional studies of ischaemia in animals been useful in the assessment of potential neuroprotective agents?.
        Trends Pharmacol. Sci. 1998; 19: 59-66
        • Jouvet M.
        Neurophysiology of the states of sleep.
        Physiol. Rev. 1967; 47: 117-177
        • Korpelainen J.T.
        • Sotaniemi K.A.
        • Huikuri H.V.
        • Myllyla V.V.
        Circadian rhythm of heart rate variability is reversibly abolished in ischemic stroke.
        Stroke. 1997; 28: 2150-2154
        • Korpelainen J.T.
        • Sotaniemi K.A.
        • Myllyla V.V.
        Autonomic nervous system disorders in stroke.
        Clin. Auton. Res. 1999; 9: 325-333
        • Kuo T.B.J.
        • Chan S.H.H.
        Continuous, on-line, real-time spectral analysis of systemic arterial pressure signals.
        Am. J. Physiol. 1993; 264: H2208-H2213
        • Kuo T.B.J.
        • 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.
        • Li C.L.
        • Chen C.F.
        • Chou P.
        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.
        • Shaw F.Z.
        • Lai C.W.
        • Yang C.C.H.
        Sleep-related sympathovagal imbalance in SHR.
        Am. J. Physiol. Heart Circ. Physiol. 2004; 286: H1170-H1176
        • Kuo T.B.J.
        • Shaw F.Z.
        • Lai C.J.
        • Lai C.W.
        • Yang C.C.H.
        Changes in sleep patterns in spontaneously hypertensive rats.
        Sleep. 2004; 27: 406-412
        • Kuo T.B.J.
        • Lai C.J.
        • Huang Y.T.
        • 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.
        • Yang C.C.H.
        Asymmetry in sympathetic and vagal activities during sleep–wake transitions.
        Sleep. 2008; 31: 311-320
        • Kuriyama N.
        • Mizuno T.
        • Niwa F.
        • Watanabe Y.
        • Nakagawa M.
        Autonomic nervous dysfunction during acute cerebral infarction.
        Neurol. Res. 2009; 32: 821-827
        • Leppavuori A.
        • Pohjasvaara T.
        • Vataja R.
        • Kaste M.
        • Erkinjuntti T.
        Insomnia in ischemic stroke patients.
        Cerebrovasc. Dis. 2002; 14: 90-97
        • Li J.Y.
        • Kuo T.B.J.
        • Hsieh S.S.
        • Yang C.C.H.
        Changes in electroencephalogram and heart rate during treadmill exercise in the rat.
        Neurosci. Lett. 2008; 434: 175-178
        • Malliani A.
        • Pagani M.
        • Lombardi F.
        • Cerutti S.
        Cardiovascular neural regulation explored in the frequency domain.
        Circulation. 1991; 84: 482-492
        • Micieli G.
        • Cavallini A.
        The autonomic nervous system and ischemic stroke: a reciprocal interdependence.
        Clin. Auton. Res. 2008; 18: 308-317
        • Min J.
        • Farooq M.U.
        • Greenberg E.
        • Aloka F.
        • Bhatt A.
        • Kassab M.
        • Morgan J.P.
        • Majid A.
        Cardiac dysfunction after left permanent cerebral focal ischemia: the brain and heart connection.
        Stroke. 2009; 40: 2560-2563
        • Muller C.
        • Achermann P.
        • Bischof M.
        • Nirkko A.C.
        • Roth C.
        • Bassetti C.L.
        Visual and spectral analysis of sleep EEG in acute hemispheric stroke.
        Eur. Neurol. 2002; 48: 164-171
        • Nagai R.
        • Nagata S.
        • Fukuya F.
        • Higaki J.
        • Rakugi H.
        • Ogihara T.
        Changes in autonomic activity and baroreflex sensitivity with the hypertension process and age in rats.
        Clin. Exp. Pharmacol. Physiol. 2003; 30: 419-425
        • Robinson T.G.
        • James M.
        • Youde J.
        • Panerai R.
        • Potter J.
        Cardiac baroreceptor sensitivity is impaired after acute stroke.
        Stroke. 1997; 28: 1671-1676
        • Saleh T.M.
        • Cribb A.E.
        • Connell B.J.
        Estrogen-induced recovery of autonomic function after middle cerebral artery occlusion in male rats.
        Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001; 281: R1531-R1539
        • Sterr A.
        • Herron K.
        • Dijk D.J.
        • Ellis J.
        Time to wake-up: sleep problems and daytime sleepiness in long-term stroke survivors.
        Brain Inj. 2008; 22: 575-579
        • Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology
        Heart rate variability: standards of measurement, physiological interpretation and clinical use.
        Circulation. 1996; 93: 1043-1065
        • Terzoudi A.
        • Vorvolakos T.
        • Heliopoulos I.
        • Livaditis M.
        • Vadikolias K.
        • Piperidou H.
        Sleep architecture in stroke and relation to outcome.
        Eur. Neurol. 2009; 61: 16-22
        • Tokgozoglu S.L.
        • Batur M.K.
        • Top uoglu M.A.
        • Saribas O.
        • Kes S.
        • Oto A.
        Effects of stroke localization on cardiac autonomic balance and sudden death.
        Stroke. 1999; 30: 1307-1311
        • Vock J.
        • Achermann P.
        • Bischof M.
        • Milanova M.
        • Muller C.
        • Nirkko A.
        • Roth C.
        • Bassetti C.L.
        Evolution of sleep and sleep EEG after hemispheric stroke.
        J. Sleep Res. 2002; 11: 331-338
        • Winward C.
        • Sackley C.
        • Metha Z.
        • Rothwell P.M.
        A population-based study of the prevalence of fatigue after transient ischemic attack and minor stroke.
        Stroke. 2009; 40: 757-761
        • Zemaityte D.
        • Varoneckas G.
        • Sokolov E.
        Heart rhythm control during sleep.
        Psychophysiology. 1984; 21: 279-289