Sleep deprivation increases thalamocortical excitability in the somatomotor pathway, especially during seizure-prone sleep or awakening states in feline seizure models

doi:10.1016/0014-4886(88)90183-5

Experimental Neurology

Volume 99, Issue 3, March 1988, Pages 664-677

https://doi.org/10.1016/0014-4886(88)90183-5 Get rights and content

Abstract

Pathological somatomotor system excitability and generalized seizures occur throughout the sleep-wake cycle but peak at different times in the amygdala kindling and systemic penicillin epilepsy models. Sleep loss increases seizure activity in both models during all waking and sleep states but does not alter the timing of seizure susceptibility in the sleep-wake cycle. Although the mechanism for sleep-deprivation seizures is unknown, we propose that sleep loss magnifies somatomotor system hyperexcitability patterns in all states, thereby increasing seizure vulnerability at all times but preferentially during seizure-prone intervals. To evaluate this hypothesis, the timing of ventral lateral thalamic and motor cortex excitability, indexed by amplitudes of primary evoked responses, was studied throughout the sleep-wake cycle in eight cats before and after nearly total sleep deprivation. Sleep loss was induced by 24-h exposure to a modified “flower pot” procedure; the control procedure consisted of 24-h exposure to a larger pedestal which did not affect sleep time. Findings confirmed the hypothesis, as follows: (i) Sleep deprivation increased ventral lateral thalamic and motor cortical excitability nonspecifically. (ii) Motor cortex hyperexcitability correlated best with penicillin seizure activity; both were elevated in slow-wave sleep and drowsiness after awakening from slow-wave sleep before sleep loss and were further increased by sleep loss. (iii) Ventral lateral thalamic hyperexcitability patterns correlated best with the timing of kindled seizure susceptibility; both peaked during transitions from slow-wave to REM sleep before and after sleep loss but were maximal after sleep loss. (iv) Sleep loss increased thalamocortical excitability and seizure susceptibility during stable REM sleep in both models, but values were lower than in other states. These results suggest a chronic neuropathology at different levels of the neuraxis for dissimilar epilepsy models and upon which the sleep-waking state modulation of seizures is superimposed. Sleep deprivation may aggravate seizures in both models by nonspecific enhancement of thalamic and cortical excitability.

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Sleep deprivation decreases neuronal excitability and responsiveness in rats both in vivo and ex vivo
2018, Brain Research Bulletin
Citation Excerpt :
A series of studies in humans in the 1960s and 1970s suggested repeatedly that sleep deprivation is a clear promoter of the epileptogenic activities (Janz, 1962; Gunderson et al., 1973). This hypothesis was supported later in various animal models including amygdala kindling and systemic penicillin epilepsy models in cats (Shouse, 1988a,b). In a study in humans, effectiveness of sleep deprivation to promote seizures independently of the inherent seizure activating effects of sleep was emphasized (Fountain et al., 1998).
Sleep deprivation has severe consequences for higher nervous functions. Its effects on neuronal excitability may be one of the most important factors underlying functional deterioration caused by sleep loss. In the present work, excitability changes were studied using two complementary in vivo and ex vivo models. Auditory evoked potentials were recorded from freely-moving animals in vivo. Amplitude of evoked responses showed a near-continuous decrease during deprivation. Prevention of sleep also reduced synaptic efficacy ex vivo, measured from brain slices derived from rats that underwent sleep deprivation. While seizure susceptibility was not affected significantly by sleep deprivation in these preparations, the pattern of spontaneous seizure activity was altered. If seizures developed, they lasted longer and tended to contain more spikes in slices obtained from sleep-deprived than from control rats. Current-source density analysis revealed that location and sequence of activation of local cortical networks recruited by seizures did not change by sleep deprivation. Moderate differences seen in the amplitude of individual sinks and sources might be explained by smaller net transmembrane currents as a consequence of decreased excitability. These findings contradict the widely accepted conception of synaptic homeostasis suggesting gradual increase of excitability during wakefulness. Our results also indicate that decreased neuronal excitability caused by sleep deprivation is preserved in slices prepared from rats immediately after deprivation. This observation might mean new opportunities to explore the effects of sleep deprivation in ex vivo preparations that allow a wider range of experimental manipulations and more sophisticated methods of analysis than in vivo preparations.
Increased photosensitivity following short sleep in sleep deprived patients
2017, Neurophysiologie Clinique
Citation Excerpt :
Short sleep following sleep deprivation increases discharges in all vigilance levels including the awake state [9]. Additionally, evoked potential studies in feline models revealed that sleep deprivation increased thalamocortical excitability and this effect is more prominent in drowsiness state after awakening from slow wave sleep, especially following sleep deprivation [17]. The thalamocortical network plays an important role in the generation of epileptic activity in the idiopathic generalized epilepsies such as JME and absence epilepsy.
We aimed to determine the effect of short day-time sleep on photoparoxysmal epileptic activity in sleep-deprived patients.
We retrospectively reviewed video-EEG recordings performed between 2003 and 2015. All recordings following at least four hours of sleep deprivation, including intermittent photic stimulation (IPS) both before and after sleep with any form of epileptiform activity were included. The study group was divided into four subgroups: (1) no photoparoxysmal response (PPR) group, with epileptiform activities other than PPRs; (2) increment group, with PPR duration increased by ≥ 200% after vs. before sleep; (3) no significant change group, with PPR duration increased between 50% and 200% after vs. before sleep; (4) decrement group, with PPR duration increased ≤ 50% after vs. before sleep.
A total number of 5805 EEG recordings from 459 patients was analyzed. Photosensitivity was present in 98 patients (21.4%). The PPRs after sleep were increased in 70% of the photosensitive patients, did not change in 23%, and were decreased in 7%. The increase in duration of PPRs was statistically significant (P < 0.001). In our cohort, photosensitivity would have been detected in 67 patients if IPS was applied only before sleep and in 91 patients if IPS was applied only after awakening (P < 0.05).
This study demonstrates that photosensitivity is enhanced after awakening from a short sleep following sleep deprivation. Thus, we recommend performing IPS after awakening to increase sensitivity to detect photoparoxysmal epileptiform discharges.
Nous avons cherché à déterminer l’effet d’un sommeil de jour de courte durée sur l’activité épileptique photoparoxystique chez des patients privés de sommeil.
Nous avons examiné rétrospectivement des enregistrements vidéo-EEG effectués entre 2003 et 2015. Tous les enregistrements effectués après au moins quatre heures de privation de sommeil, comprenant une stimulation lumineuse intermittente (SLI) réalisée avant et après le sommeil, et caractérisés par une activité épileptiforme quelle qu’en soit le type, ont été inclus. La population étudiée a été divisée en quatre sous-groupes : (1) groupe sans réponse photoparoxystique (RPP), incluant des activités épileptiformes autres que des RPP ; (2) groupe incrémental, avec une durée des RPP augmentée de 200 % ou plus entre après et avant le sommeil ; (3) groupe sans changement significatif, avec une durée des RPP augmentée de 50 % à 200 % entre après et avant le sommeil ; (4) groupe décrémental, avec une durée des RPP augmentée de 50 % ou moins entre après et avant le sommeil.
Un total de 5805 enregistrements EEG correspondant à 459 patients a été analysé. La photosensibilité était présente chez 98 patients (21,4 %). Les RPP étaient augmentées après le sommeil chez 70 % des patients photosensibles, inchangées chez 23 % et diminuées chez 7 %. L’augmentation de la durée des RPP était statistiquement significative (p < 0,001). Dans notre cohorte, la photosensibilité aurait été détectée chez 67 patients si la SLI avait été appliquée seulement avant le sommeil et chez 91 patients s’il avait été appliquée seulement après le réveil (p < 0,05).
Cette étude démontre que la photosensibilité est augmentée au réveil d’un sommeil de courte durée suivant une privation de sommeil. Ainsi, nous recommandons d’effectuer des SLI après le réveil pour augmenter la sensibilité à détecter des décharges épileptiformes photoparoxystiques.
Sleep affects cortical source modularity in temporal lobe epilepsy: A high-density EEG study
2015, Clinical Neurophysiology
Citation Excerpt :
We were able to show how the topographical appearance of interictal epileptic spikes differs in wake and in sleep. The facilitatory effect of sleep and sleep deprivation on IEDs has been demonstrated in vivo and in vitro (Cohen and Dement, 1965; Naitoh and Dement, 1974; Shouse, 1988; Manganotti et al., 2006; Del Felice et al., 2011, 2013). To our knowledge, systematic study of differences in temporal spike scalp distribution between wake and sleep dates back to >30 years ago (Lieb et al., 1980; Rowan et al., 1982).
Interictal epileptiform discharges (IEDs) constitute a perturbation of ongoing cerebral rhythms, usually more frequent during sleep. The aim of the study was to determine whether sleep influences the spread of IEDs over the scalp and whether their distribution depends on vigilance-related modifications in cortical interactions.
Wake and sleep 256-channel electroencephalography (EEG) data were recorded in 12 subjects with right temporal lobe epilepsy (TLE) differentiated by whether they had mesial or neocortical TLE. Spikes were selected during wake and sleep. The averaged waking signal was subtracted from the sleep signal and projected on a bidimensional scalp map; sleep and wake spike distributions were compared by using a t-test. The superimposed signal of sleep and wake traces was obtained; the rising phase of the spike, the peak, and the deflections following the spike were identified, and their cortical generator was calculated using low-resolution brain electromagnetic tomography (LORETA) for each group.
A mean of 21 IEDs in wake and 39 in sleep per subject were selected. As compared to wake, a larger IED scalp projection was detected during sleep in both mesial and neocortical TLE (p < 0.05). A series of EEG deflections followed the spike, the cortical sources of which displayed alternating activations of different cortical areas in wake, substituted by isolated, stationary activations in sleep in mesial TLE and a silencing in neocortical TLE.
During sleep, the IED scalp region increases, while cortical interaction decreases.
The interaction of cortical modules in sleep and wake in TLE may influence the appearance of IEDs on scalp EEG; in addition, IEDs could be proxies for cerebral oscillation perturbation.
What is the role for EEG after sleep deprivation in the diagnosis of epilepsy? Issues, controversies, and future directions
2014, Neuroscience and Biobehavioral Reviews
Citation Excerpt :
These authors demonstrated that SD increased the amplitude of motor-evoked potentials in both models. However, it did not alter the pre-existing level of somatomotor cortical excitability, which was tightly dependent on the specific wakefulness or sleep stage (Shouse, 1988b, 1987). Further studies conducted on rodent models do not show uniform results.
In patients with a first seizure, the identification of early sensitive and specific biomarkers for formulating a diagnosis of epilepsy is fundamental. Sleep deprivation (SD) has long been used as a means of enhancing EEG sensitivity in the diagnostic process. However, huge methodological differences among the studies addressing this topic have led to highly variable results and often confusing assumptions. Here, we provide a detailed description of the correlations between SD and epilepsy, along with their putative mechanistic explanations derived from experimental studies in animals and humans. We also outline the clinical studies evaluating the role of SD EEG and discuss them critically in terms of: (a) study design and SD EEG methodology; (b) EEG sensitivity and specificity; (c) the role of drug-induced sleep EEG and EEG during spontaneously occurring sleep; and (d) the relevance of patient features, syndromes, and subsyndromes, as well as their correlations with neuroimaging details. Finally, we propose specific studies that might increase the role of SD EEG in the diagnosis and prognosis of epilepsy.
Neurochemical and electrophysiological changes induced by paradoxical sleep deprivation in rats
2011, Behavioural Brain Research
Citation Excerpt :
It has been reported that sleep deprivation increases neuronal excitability and decreases the threshold for seizures in epileptic model [48]. In animals, sleep deprivation resulted in a lowering of the thresholds to electric shock convulsions [49] and for kindling to occur [50]. Accordingly, this increase in glutamine could be an adaptive mechanism to alleviate the state of excitation mediated by glutamate.
The present study aims to investigate the effects of paradoxical sleep deprivation (PSD) on the waking EEG and amino acid neurotransmitters in the hippocampus and cortex of rats. Animals were deprived of paradoxical sleep for 72 h by using the multiple platform method. The EEG power spectral analysis was carried out to assess the brain's electrophysiological changes due to sleep deprivation. The concentrations of amino acid neurotransmitters were assessed in the hippocampus and cortex using HPLC. Control data showed slight differences from normal animals in the delta, theta and alpha waves while an increase in the beta wave was obtained. After 24 h of PSD, delta relative power increased and the rest of EEG wave's power decreased with respect to control. After 48 h and 72 h the spectral power analysis showed non-significant changes to control. The amino acid neurotransmitter analysis revealed a significant increase in cortical glutamate, glycine and taurine levels while in the hippocampus, glutamate, aspartate, glutamine and glycine levels increased significantly. Both the waking EEG and neurotransmitter analyses suggest that PSD induced neurochemical and electrophysiological changes that may affect brain proper functionality.
The sleep-deprived brain in normals and patients with juvenile myoclonic epilepsy: A perturbational approach to measuring cortical reactivity
2011, Epilepsy Research
Citation Excerpt :
The activation of epileptic patterns has been attributed to drowsiness and sleep (Pratt et al., 1968), while sleep deprivation has been shown to have a specific activating effect on patients who remain awake during recording (Naitoh and Dement, 1974). In animals, sleep deprivation results in a lowering of the threshold for electroshock convulsions (Cohen and Dement, 1965) and kindling (Shouse, 1988) due to a shift in the balance between excitatory and inhibitory neurotransmitters (Naitoh and Dement, 1974). In humans, a noninvasive method for investigating motor excitability is transcranial magnetic stimulation (TMS), which measures amplitude variations of the motor evoked potential (MEP).
Simultaneous electroencephalography⿿transcranial magnetic stimulation (EEG⿿TMS) investigates cortical reactivity to external perturbations. TMS evoked potentials (TEPs) have been described in normals during sleep and wake but not after sleep deprivation or in pathologically enhanced excitability, i.e., epilepsy. The aim of our study was to identify TEPs and their modifications via EEG⿿TMS co-registration in healthy controls and patients with juvenile myoclonic epilepsy (JME) during wake, sleep deprivation and sleep conditions. Focal TMS was administered to the primary motor cortex in 12 healthy controls and 10 patients with JME. At least 150 TMS were delivered randomly every 8⿿15 s during wake, sleep deprivation and sleep conditions. EEG was simultaneously acquired from 32 scalp electrodes. A significant increase in late peak amplitudes (P100 and N190) was observed in all subjects during the sleep-deprived condition, with a marked anterior increase and overall higher amplitude potentials in the JME patients. We demonstrated an overall higher cortical excitability in the JME patients, particularly over the anterior cortex after sleep deprivation and rebound sleep. This phenomenon could be related to the cortico-thalamic circuit dysfunctions believed to cause myoclonic epilepsy and a higher susceptibility of the frontal and prefrontal areas to the effects of sleep deprivation.

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^☆: This work was supported by the Veterans Administration.

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Sleep deprivation increases thalamocortical excitability in the somatomotor pathway, especially during seizure-prone sleep or awakening states in feline seizure models☆

Abstract

Exp. Neurol.

Exp. Neurol.

Neurosci. Lett.

Electroencephalogr. Clin. Neurophysiol.

Electroencephalogr. Clin. Neurophysiol.

Electroencephalogr. Clin. Neurophysiol.

Electroencephalogr. Clin. Neurophysiol.

Electroencephalogr. Clin. Neurophysiol.

Exp. Neurol.

Brain Res.

Electroencephalogr. Clin. Neurophysiol.

Int. Rev. Neurobiol.

Electroencephalogr. Clin. Neurophysiol.

Complex partial seizures and REM sleep

Inhibitory influence of paradoxical sleep on the amygdaloid kindling development of the cats

Sleep Res.

The effect of electroconvulsive shock in cats deprived of REM sleep

Science

Sleep stages, REM deprivation and electroconvulsive threshold in the cat

Brain Res.

Diagnosis of epilepsy with the aid of sleep methodology: evaluation of 1163 cases

Generalized epilepsy with spike-and-wave discharge: a reinterpretation of its electrographic and clinical manifestations

Epilepsia