Elsevier

Sleep Medicine

Volume 2, Issue 3, May 2001, Pages 185-194
Sleep Medicine

Original article
Sleep electroencephalogram changes in acute hemispheric stroke

https://doi.org/10.1016/S1389-9457(00)00071-XGet rights and content

Abstract

Background/objective: Since reports of the effects of cerebral hemispheric stroke on sleep architecture are rare and contradictory, we prospectively studied 24 patients with first acute supratentorial, extra-thalamic stroke.

Methods: We assessed stroke severity, topography, and volume (on brain MRI). Sleep electroencephalogram recordings were performed a mean of 12 days after stroke onset, and scored for sleep stages over the healthy hemisphere. Sleep spindles and sawtooth waves were analyzed over both hemispheres. Data were compared with those of 17 age and gender-matched patients with normal brain imaging.

Results: Compared to controls, stroke patients had lower total sleep time (P<0.01), lower sleep efficiency (P=0.02), and reduced amounts of NREM sleep stages 2–4 (P=0.02). Sleep spindles and sawtooth waves were often bilaterally reduced in patients with stroke volumes >25 ml. Abnormalities of REM sleep were more common in sleep studies performed within 3 days after stroke onset. Compared to patients with poor outcome, those with good outcome had higher sleep efficiency (P<0.01), more sleep time (P=0.02), and more NREM sleep stage 2 (P<0.01).

Conclusion: Acute hemispheric stroke is accompanied by sleep EEG changes over the healthy hemisphere that correlate with stroke severity. These findings support the hypothesis that the cerebral hemispheres participate in the control of sleep.

Introduction

Since the first EEG recording in sleep, sleep is no longer considered a passive state but the result of an active brain process. For several decades sleep was thought to depend mainly on brainstem mechanisms and to occur homogeneously over the cerebral hemispheres. Several recent observations, however, suggest a role of the forebrain in sleep regulation and the existence of focal differences in the EEG correlates of sleep over the cerebral hemispheres. First, there are regional differences in sleep EEG spectra at the macro EEG level with state-related and frequency-specific differences [1], [2]. Second, intracellular recordings indicate that discrete neuronal populations contribute to sleep generation [3]. The reticular nucleus of the thalamus is the pace-maker of sleep spindles, the cerebral cortex may be essential for generation of K complexes and <1 Hz delta activity [4], and thalamo-cortico-thalamic networks for that of >1 Hz delta activity [5]. On the other hand, the generation of rapid eye movements (REM) sleep depends upon the integrity of the medio-lateral, ponto-mesencephalic tegmentum [6], [7]. Third, ablation of the frontal cortex in the cat leads to reduction of both REM and non-rapid eye movements sleep (NREM) sleep [8]. Fourth, functional neuroimaging (e.g. positron emission tomography) (PET)) has shown topographic differences in the activity level of distinct hemispheric areas during NREM and REM sleep [9], [10], [11].

Until now most reports of the effects of brain injury on sleep have concentrated on sleep EEG changes following brainstem or thalamic lesions [12], [13], [14], [15]. In hemispheric stroke, Cress and Gibbs observed in 1948 a reduction of sleep spindles over the affected hemisphere [16]. In the 1970s, Hachinski et al. [17] reported a reduction of both sleep spindles and slow wave sleep in patients with large strokes and poor clinical outcome. A reduction of REM sleep has been described in patients with severe hemispheric lesions [18]. However, the effects of side and topography of the lesion on sleep architecture have rarely been analyzed and when they have, the results have been contradictory [18], [19].

Studies on sleep EEG changes following hemispheric stroke reported to date suffer important limitations. First, neither sleep apnea, present in at least 50% of stroke patients [20], [21], [22], nor periodic limb movements were assessed in most studies, although both may affect sleep architecture. Second, data on clinical severity and radiological extension of stroke were usually absent or limited. Third, control groups often consisted of non-hospitalized persons, and hospitalization for acute illness may induce profound sleep EEG changes [23]. Fourth, a systematic assessment of sleep microstructure has not been performed [17], [24], [25].

Nonetheless, the evidence concerning the role of the forebrain in sleep regulation suggests that the study of changes in the macro and microstructure of sleep following focal brain damage (e.g. stroke) may contribute as experiments of nature to a better understanding of regional aspects of sleep EEG generation. To assess the relationship between sleep EEG and stroke severity, topography and outcome, we analysed the macro and microstructure of sleep in a consecutive series of 24 patients with acute hemispheric, extra-thalamic stroke.

Section snippets

Patients

Over a period of 40 weeks we assessed by means of conventional polysomnography 24 consecutive patients (eight women, 16 men), with a mean age±SE of 62.1±2.2 years (range: 26–78) admitted to the Neurology Department of the University of Michigan Hospitals because of a first acute hemispheric stroke documented by brain CT or MRI. The study protocol was approved by the Institutional Review Board of the University of Michigan Medical Center.

Stroke assessment

Patients were assessed clinically by one of the authors

Results

There were 13 left-sided and 11 right-sided strokes. The mean±SE score of the scandinavian stroke scale (SSS) was 36.7±3.4 (range 12–56). Eight patients had a severe stroke (SSS<30). Stroke volume ranged from 0.3 to 122 ml (mean±SE=20.2±6.5 ml). A presumed stroke etiology was identified in 17 (71%) of 24 patients.

Outcome at hospital discharge was good (independent) in 16 (66%) of 24 patients. As expected, there was a significant difference in SSS (P<0.001) between patients with good and bad

Discussion

In this study, sleep macro and microstructure was assessed in 24 consecutive patients with, MRI-proven acute extra-thalamic hemispheric stroke. We found that acute hemispheric stroke is associated with a severe reduction in sleep efficiency, with reduced amounts of both NREM and REM sleep, compared to published norms [29]. However, the presence of sleep architecture changes in our control population indicates that the observed sleep EEG changes can be attributed only partially to brain damage.

Acknowledgements

We thank Douglas Quint, for reviewing the neuroradiological data used in this study and Ken Morton for his valuable help in scoring of the PSGs. Ronald Chervin, gave helpful comments in the initial phase of this research. This paper was supported by the Swiss National Science Foundaton, Grant No. 32.49.853.96.

References (40)

  • M. Steriade et al.

    Coalescence of sleep rhythms and their chronology in corticothalamic networks

    SOL

    (1998)
  • F. Amzica et al.

    The K-complex: its slow (<1 Hz) rhythmicity and relation to delta waves

    Neurology

    (1997)
  • J.M. Siegel

    Brainstem mechanisms generating REM sleep

  • N. Hofle et al.

    Regional cerebral blood flow changes as a function of delta and spindle activity during slow wave sleep in humans

    J. Neurosci.

    (1997)
  • A.R. Braun et al.

    Regional cerebral blood flow throughout the sleep-wake cycle. An H215O study

    Brain

    (1997)
  • P. Maquet et al.

    Functional neuroanatomy of human rapid-eye-movement sleep and dreaming

    Nature

    (1996)
  • O.N. Markand et al.

    Sleep abnormalities in patients with brainstem lesions

    Neurology

    (1976)
  • A. Autret et al.

    A syndrome of REM and Non-REM sleep reduction and lateral gaze paresis after medial tegmental pontine stroke

    Arch. Neurol.

    (1988)
  • C. Bassetti et al.

    Hypersomnia following thalamic stroke

    Ann Neurol

    (1996)
  • C.H. Cress et al.

    Electroencephalographic asymmetry during sleep

    Dis Nerv Syst

    (1948)
  • Cited by (81)

    • Measuring Sleep, Wakefulness, and Circadian Functions in Neurologic Disorders

      2021, Sleep Medicine Clinics
      Citation Excerpt :

      Thalamic strokes predominantly reduce sleep spindles and deeper NREM sleep stages.6,9,22,23 Indeed, a reduction in sleep spindles after thalamic and supratentorial strokes24,25 may occur as a function of lesion size.19 Moreover, spindle power reduction in the peri-infarct area acutely after stroke is accompanied by a temporarily increased spindle power over the contralesional hemisphere.

    • Sleep architectural dysfunction and undiagnosed obstructive sleep apnea after chronic ischemic stroke

      2021, Sleep Medicine
      Citation Excerpt :

      This suggests that OSA alone is unlikely to be mediating the reductions to SWS observed in our stroke sample. Despite preliminary exploratory evidence indicating an effect of acute stroke topography and lesion volumes on sleep architecture [25,26], we found no significant differences in hemispheric sleep architecture between stroke patients' ipsilesional and contralesional hemispheres. Furthermore, we observed no difference in the degree of periventricular or deep white matter hyperintensities between stroke patients and controls.

    View all citing articles on Scopus

    This paper is dedicated to the memory of Dr Aldrich, who recently passed away.

    View full text