Sleep and brain lesions: a critical review of the literature and additional new cases

doi:10.1016/S0987-7053(01)00282-9

Neurophysiologie Clinique/Clinical Neurophysiology

Volume 31, Issue 6, December 2001, Pages 356-375

https://doi.org/10.1016/S0987-7053(01)00282-9 Get rights and content

Abstract

We present a comprehensive review of sleep studies performed in patients with brain lesions complemented by 16 additional personal selected cases and by discussion of the corresponding animal data. The reader is cautioned about the risk of establishing an erroneous correlation between abnormal sleep and a given disorder due to the important inter and intra variability of sleep parameters among individuals. Salient points are stressed : the high frequency of post-stroke sleep breathing disorders is becoming increasingly recognised and may, in the near future, change the way this condition is managed. Meso-diencephalic bilateral infarcts induce a variable degree of damage to both waking and non-REM sleep networks producing and abnormal waking and sometimes a stage 1 hypersomnia reduced by modafinil or bromocriptine, which can be considered as a syndrome of cathecholaminergic deficiency. Central pontine lesions induce REM and non-REM sleep insomnia with bilateral lateral gaze paralysis. Bulbar stroke leads to frequent sleep breathing disorders.

Polysomnography can help define the extent of involvement of various degenerative diseases. Fragmented sleep in Parkinson’s disease may be preceded by REM sleep behavioural disorders. Multiple system atrophies are characterised by important sleep disorganisation. Sleep waking disorganisation and a specific ocular REM pattern are often seen in supra-nuclear ophtalmoplegia. In Alzheimer patients, sleep perturbations parallel the mental deterioration and are possibly related to cholinergic deficiency. Fronto-temporal dementia may be associated with an important decrease in REM sleep. Few narcoleptic syndromes are reported to be associated with a tumour of the third ventricle or a multiple sclerosis or to follow a brain trauma ; all these cases raise the question whether this is a simple coincidence, a revelation of a latent narcolepsy or, as in non- DR16 /DQ5 patients, a genuine symptomatic narcolepsy.

Trypanosomiasis and the abnormal prion protein precociously alter sleep patterns. Polysomnography is a precious tool for evaluating brain function provided it is realised under optimal conditions in stable patients and interpreted with caution.

Several unpublished cases are presented: one case of pseudohypersomnia due to a bilateral thalamic infarct and corrected by modafinil, four probable late-onset autosomal recessive cerebellar ataxias without sleep pattern anomalies, six cases of fronto-temporal dementia with strong reduction in total sleep time and REMS percentage on the first polysomnographic night, one case of periodic hypersomnia associated with a Rathke’s cleft cyst and four cases of suspected symptomatic narcolepsy with a DR16-DQ5 haplotype, three of which were post-traumatic without MRI anomalies, and one associated with multiple sclerosis exhibiting pontine hyper signals on MRI.

Résumé

Nous présentons une revue des études du sommeil réalisées chez des patients porteurs de lésions cérébrales complétée par 16 cas personnels et par une discussion des résultats correspondants obtenus chez lˈanimal. Une grande prudence méthodologique est nécessaire avant dˈétablir une relation entre un comportement de sommeil anormal et une affection donnée en raison de lˈimportante variabilité inter- et intra-sujet des paramètres du sommeil.

Pathologie vasculaire : dans les suites immédiates dˈun accident vasculaire cérébral (AVC), la prévalence élevée des troubles respiratoires au cours du sommeil amènera dans un futur proche à proposer une respiration en pression positive continue. Les AVC bulbaires entraînent fréquemment des troubles du rythme respiratoire. Les lésions pontiques paramédianes bilatérales entraînent un syndrome associant une réduction extrême en sommeil à ondes lentes (SOL) et en SP, et une ophtalmoplégie latérale bilatérale. Les infarctus mésencéphalo-diencéphaliques bilatéraux entraînent une atteinte à un degré variable des deux systèmes de veille et de SOL responsable d’un éveil anormal, parfois d’une hypersomnie en stade 1 réversible après stimulation cathécholaminergique par modafinil ou bromocriptine.

La polysomnographie peut permettre de préciser lˈextension des différents processus dégénératifs. Le sommeil fragmenté de la maladie de Parkinson peut être précédé par des troubles du comportement au cours du sommeil paradoxal (TCSP) ; on insiste aussi sur l’association hallucinations visuelles, accès de sommeil et endormissement en SP qui évoque un phénotype narcoleptique. Les atrophies multi-systématisées sont associées à une très importante désorganisation du sommeil. La désorganisation du SP et un pattern spécifique des mouvements oculaires rapides caractérisent lˈophtalmoplégie supra-nucléaire progressive. Dans la maladie dˈAlzheimer, les perturbations sont parallèles à la gravité de la maladie et peuvent être reliées au déficit cholinergique. Il est possible que les démences fronto-temporales soient associées à une importante diminution du SP.

Un syndrome narcoleptique peut être associé avec une tumeur du 3^e ventricule ou une sclérose en plaques, ce qui pose la question de savoir sˈil sˈagit dˈune simple coïncidence, de la révélation dˈune maladie latente ou d’une responsabilité directe surtout chez les quelques sujets qui sont « R2DQW1 négatifs ».

La trypanosomiase et les maladies à prions altèrent de façon précoce les patterns de sommeil. En définitive, la polysomnographie est un moyen précieux pour évaluer le fonctionnement cérébral pourvu quˈelle soit réalisée dans des conditions optimales chez des patients stables, et interprétée avec précaution.

Parmi les cas présentés non publiés, on cite un cas de pseudo-hypersomnie due à un infarctus thalamique bilatéral corrigé par le modafinil, quatre probables ataxies cérébelleuses autosomiques récessives sans anomalie du sommeil, six cas de démences fronto-temporales avec une importante réduction du temps de sommeil total et du pourcentage SP au cours de la première nuit, un cas dˈhypersomnie périodique associé à un kyste hypophysaire et quatre cas de narcolepsie symptomatique avec un haplotype DR16DQ5, trois dˈentre elles étant post-traumatiques sans anomalie à lˈIRM et une associée à une sclérose en plaques qui montrait des hypersignaux pontiques à lˈIRM.

Section snippets

Acute phase

Sleepiness is one of the symptoms commonly seen in cerebral herniations, whether they be cingular, central or temporal: the most frequently proposed explanation is bilateral dysfunction of the arousal systems due the causative lesion and the resulting compression 〚158〛. However, sleepiness can also be due to interruption in the arousal systems at the level of the mesencephalic reticular formation by a haemorrhage or an ischemic process. Accordingly, it can be part of the terminal brain-stem

Degenerative diseases

These clinical entities are accompanied by a syndrome of poor sleep (table II). Nevertheless, some investigators have concluded that the sleep modifications are specifically caused by precise regional neuronal depopulation and the resulting neurotransmitter defects 118, 127, 129, 156. Sleep also influences abnormal movements and the extrapyramidal symptoms.

Tumours

A number of publications have reported narcolepsies associated with cerebral tumours. We will discuss granulomas along with tumours because they behave clinically like tumours and their consequences with respect to sleep are also similar.

Diagnostic and prognostic value of polysomnography

Before the introduction of the CT scan, the prognostic value of the polysomnographic recording had been tested in post-traumatic coma: the reappearance of sleep patterns 〚39〛, suggesting a good prognosis 〚26〛. A report mentioned a parallel between cognitive improvement and the reappearance of REMS 〚167〛; however, the causal link between these two simultaneous recoveries requires confirmation.

Over the long term, patients with a subjective brain-trauma syndrome manifest sleep difficulties mostly

Sleep and multiple sclerosis

Occasionally, special attention is required to distinguish simple fatigue from sleep attacks. However, an association between narcolepsy and multiple sclerosis (MS) has been reported in a limited number of cases. Three cases have been published involving familial MS, an infrequent form of the disease 〚54〛. Five cases which occurred in the usual sporadic form of the disease have been reported 25, 203, 179 to which we add a sixth (annex VI). Four of the reported cases plus ours were DR2-positive

Infection

Von Economo’s pioneer observations made during the encephalitis epidemic are worthy of consideration (see the review by Bogaert and Theodorides) 〚197〛. A number of patients presented hypovigilance similar to that seen in coma while others had excessive daytime sleepiness resembling physiologic sleep, i.e., reversible into a normal waking state without confusion after stimulation followed by the reappearance of sleepiness as soon as the stimulation ceased. Von Economo noted that the lesions in

Polysomnography as a tool for studying disturbances in brain function

To what extent does the preceding analysis allow polysomnography to be considered as a useful tool in the anatomo-functional evaluation of a lesioned brain?

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Not only may sleep disruption negatively affect stroke recovery, but brain lesions associated with a worse outcome may also involve critical structures responsible for sleep generation such as the thalamus or brainstem [15,16]. Based on few studies, REM sleep seems to be reduced in patients with brainstem lesions, as well as NREM sleep in those with hemispheric lesions [16–18]. In a single study, a reduction of REM sleep was reported in cerebellar strokes [19].
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REVIEWSleep and brain lesions: a critical review of the literature and additional new casesSommeil et lésions cérébrales : revue critique de la littérature et cas cliniques additionnels.

Abstract

Résumé

Section snippets

Acute phase

Degenerative diseases

Tumours

Diagnostic and prognostic value of polysomnography

Sleep and multiple sclerosis

Infection

Polysomnography as a tool for studying disturbances in brain function

Biol Psychiatry

Electroencephalogr Clin Neurophysiol

Electroencephalogr Clin Neurophysiol

Electroencephalogr Clin Neurophysiol

Lancet

Electroencephalogr Clin Neurophysiol

Electroencephalogr Clin Neurophysiol

Int J Pediatr Otorhinolaryngol

Brain Res

Neurological Sciences

Whipple's disease confined to the central nervous system

Ann Neurol

Obstructive sleep apnea in association with posterior fossa neurologic disease

Arch Neurol

Sleep-wake cycles in multi-infarct dementia and dementia of the Alzheimer type

Neurology

Narcolepsy associated with lesions of the diencephalon

Neurology

Symptomatic cataplexy

J Neurol Neurosurg Psychiatry

Léthargie intermittente traduisant l'existence d'une tumeur du IIIe ventricule

Rev Neurol

Disturbances of rapid eye movements sleep in patients with lesions of the nervous system

Electroencephalogr Clin Neurophysiol

Respiration and sleep in Parkinson's disease

J Neurol Neurosurg Psychiatry

Improvement of sleep architecture in PD with subthalamic nucleus stimulation

Neurology

Hallucinations, REM sleep, and Parkinson's disease. A medical hypothesis

Neurology

Sleep disorders and diaphragmatic function in patients with amyotrophic lateral sclerosis

Am J Respir Crit Care M

Hypersomnia after tegmental pontine hematoma : Case report

Neurologia

Reversal of sleep disturbance in Parkinson's disease by antiparkinsonian therapy : a preliminary study

Neurology

Sleep apnea as a feature of a bulbar stroke

Stroke

Parkinsonian tremor loses its alternating aspect during non-REM sleep and is inhibited by REM sleep

J Neurol Neurosurg Psychiatry

Étude physiopathologique et neuropathologique d'un syndrome de décortication cérébrale

Rev Neurol

A syndrome of REM and non-REM sleep reduction and lateral gaze paresis after medial tegmental pontine stroke : CT scans and anatomical correlations in four patients

Arch Neurol

Cataplexia, sleep disorganisation and apnea in probable striato-nigral degeneration

Séquelles encéphaliques graves vasculaires : étude de la veille et du sommeil

Sleep apnea and the Arnold-Chiari malformation

Am Rev Resp Dis

Hypersomnia following paramedian thalamic stroke: a report of 12 patients

Ann Neurology

Sleep-Disordered Breathing in Patients With Acute Supra- and Infratentorial Strokes. A prospective Study of 39 Patients

Stroke

Localized brainstem ischemic damage and Ondine's curse after near-drowning

Neurology

Narcolepsy in two cases of multiple sclerosis

Acta Neurol Scand

Clinical value of the sleep electroencephalographic patterns in posttraumatic coma

Acta Neurol Scand

L-Dopa plus dopa-decarboxylase inhibitor : sleep organization in Parkinson's syndrome before and after treatment

Acta Neurol Belg

Organisation du sommeil chez les sujets atteints d'inconscience post-traumatique chronique

Rev EEG Neurophysiol Clin

Symptomatic narcolepsis : a critical study

Disruption for endocrine rhythms in sleeping sickness with preserved relationship between hormonal pulsatility and the REM-NREM sleep cycles

J Biol Rhythms

Insomnia after bilateral stereotactic thalamotomy in man

J Neurol Neurosurg Psychiatry

Sleep-wake cycle in human African trypanosomiasis

J Clin Neurophysiol

REVIEW
Sleep and brain lesions: a critical review of the literature and additional new casesSommeil et lésions cérébrales : revue critique de la littérature et cas cliniques additionnels.

Léthargie intermittente traduisant l'existence d'une tumeur du III^e ventricule