Nocturnal frontal lobe epilepsy (NFLE) is a syndrome characterized by the occurrence of sleep related seizures of variable complexity and duration. Hypermotor seizures (HMS) represent a classic manifestation of this syndrome, associated with a perturbation of the ventromesial frontal cortex and anterior cingulate gyrus regions. Nevertheless, in recent years, reports have showed that the seizure onset zone (SOZ) need not be of frontal origin to generate HMS. Here we report an unusual case of a patient presenting with a seven-year history of drug-resistant sleep related HMS arising from the mesial parietal region. The presence of an infrequent feeling of levitation before the HMS was key to suspecting a subtle focal cortical dysplasia in the right precuneus region. A stereo-EEG investigation confirmed the extra-frontal seizure onset of the HMS and highlighted the interrelationship between unstable sleep and seizure precipitation.
Gibbs SA, Figorilli M, Casaceli G, Proserpio P, Nobili L. Sleep related hypermotor seizures with a right parietal onset. J Clin Sleep Med 2015;11(8):953–955.
Nocturnal frontal lobe epilepsy (NFLE) is a syndrome characterized by the occurrence of sleep related seizures of variable complexity and duration. The hallmark seizure consists of asymmetric tonic/dystonic postures or complex hypermotor movements, lasting about 30 seconds and occurring many times per night.1 Stereo-electroencephalographic (stereo-EEG) studies conducted in drug-resistant patients have identified the ventromesial frontal cortex and anterior cingulate gyrus regions of the frontal lobe as the structures mainly involved during a hypermotor seizure (HMS).2 Here we report an unusual case of a patient presenting classic NFLE features arising from the mesial parietal region.
REPORT OF CASE
An 18-year-old man presented with a 7-year history of sleep related episodes that were characterized by rhythmic pelvic thrashing, pedalling, and stereotyped rapid distal arm movements, sometimes associated with repetitive moaning, lasting 20–30 seconds. Patient recollection was uncommon, but parents had witnessed many episodes, which occurred 6 to 10 times per night, almost every night, without a specific timing. Immediately before the episodes, the patient occasionally felt a vivid sensation of levitation. Sleep history was unremarkable apart from a complaint of frequent nocturnal awakenings and occasional nonrestorative sleep.
A diagnosis of probable NFLE was given at age 12, and pharmacological treatment with carbamazepine was initiated with some initial success, but episodes reappeared. During the next 6 years, no further seizure remission was achieved with various antiepileptic drug trials in either mono- or polytherapy.
At our center, an overnight video-polysomnography recording with a full 10–20 EEG montage captured 6 stereotyped episodes with a predominance of right-sided manual automatisms accompanied by semi-rhythmic pelvic thrashing occurring mainly during unstable NREM sleep (Video 1). Immediately following the event, the patient was fully responsive. Interictal and ictal scalp EEG were uninformative. A brain MRI was performed and, in accordance with a levitation aura, a complex proprioceptive sensation known to arise from the parietal lobe, the presence of a small focal cortical dysplasia (FCD) with imprecise borders was suspected in the depths of the right precuneus, near the marginal ramus of the cingulate gyrus (Figure 1A).
Brain MRI and position of depth electrodes.
(A) Sagittal and coronal Fluid-attenuated inversion recovery (FLAIR) MR images of the brain showing a subtle hyperintensity over the anterior border of the right precuneus, in the depths of the marginal ramus of the cingulate gyrus (arrowhead). (B) Cortical reconstruction showing a superior and a mesial view of the right hemisphere. On the lower left image, the dark circles represent the entry point of each depth electrode. The shaded cortical area identifies the pre-central gyrus. On the lower right image, the symbols represent the deepest electrode contacts recording the EEG activity of the mesial portion of the brain and the suspected lesional area (one oblique electrode is not represented).
Brain MRI and position of depth electrodes. (A) Sagittal and coronal Fluid-attenuated inversion recovery (FLAIR) MR images of the brain showing a subtle hyperintensity over the anterior border of the right precuneus, in the depths of the marginal ramus of the cingulate gyrus (arrowhead). (B) Cortical reconstruction showing a superior and...
In view of the available anatomo-electro-clinical data, a stereo-EEG investigation comprising multiple multilead intracerebral electrodes was proposed, covering mainly the right centro-parietal region in order to precisely delimit the seizure onset zone (SOZ) (Figure 1B). In the right precuneus region, stereo-EEG exhibited the typical pathological activity associated with a type II FCD3 (Figure 2A, 2B). Behaviorally, seizures were generally preceded by a paroxysmal arousal (PA), characterized by various short lasting and inconsistent automatisms (e.g., sudden eye opening, head elevation, manual automatisms, leg stretching) (Video 1) and ending with a rapid return to sleep during which the HMS occurred shortly afterwards. On both scalp and stereo-EEG, an increase in sleep instability was seen before the PAs, along with quasi-periodic bursts of epileptiform discharges inside the SOZ (Figure 2B). PAs on scalp EEG were associated with bursts of slow waves with superimposed beta activity. On stereo-EEG, PAs were associated with a “dissociated” pattern of coexistent sleep-like slow waves and rapid wake-like activity (Figure 2C). Following the PA, this stereo-EEG pattern continued while on scalp the patient remained in NREM sleep (Figure 2D). A clear increase in quasi-periodic interictal discharges was subsequently observed on stereo-EEG, progressively evolving into a full-blown electro-clinical seizure (Figure 2D). The ictal discharge quickly spread from the anterior border of the precuneus to the anterior part of the frontal cingulate gyrus. In addition, intracortical low frequency stimulation of the suspected SOZ consistently induced an ictal EEG discharge that reproduced levitation auras of the patient. The patient is now awaiting surgical resection of the identified SOZ.
Overnight recording of simultaneous stereo-EEG and scalp EEG (reduced montage).
Each EEG segment represents a 30-second epoch. (A) Wakefulness: the seizure onset zone (SOZ) exhibits the typical wake interictal activity of type II focal cortical dysplasia (FCD) consisting of sub-continuous rhythmic or sub-rhythmic spike- and polyspike-and-waves.3,7 Of note, this activity is not transferred to the scalp EEG recording over the SOZ. (B) NREM sleep: the SOZ produces the typical pseudo-rhythmic low voltage fast discharges (“brushes”) that are intermingled with spindle-like activity.7 Stereo-EEG contacts outside the lesional area and scalp EEG show periodic K-complexes, bursts of slow waves and sleep spindles.8(C) Paroxysmal arousal (PA): example of the observed “dissociated” pattern of co-existent sleep-like slow waves and fast wake-like activity on stereo-EEG. Following arousal, the lateral portion of the frontal lobe (sfg, mfg1, mfg2) produces high voltage sleep-like slow waves, which are also detectable in the centro-parietal regions on scalp EEG. Meanwhile, the motor cortex (Mc), the somatosensory cortex (SSc) and the SOZ shift from delta rhythms to wake-like beta activity. (D) Seizure: a hypermotor seizure occurs in NREM sleep approximately 1 minute after the end of the PA. The SOZ initiates a low voltage fast rhythmic epileptiform discharge (asterisk) that progressively evolves, reaching other contacts outside the SOZ at the end of the epoch. (mfg1-2, mesial frontal gyrus contacts; sfg, superior frontal gyrus; pcl, paracentral lobule; Mc, motor cortex; SSc, somatosensory cortex; pcg, posterior cingulate gyrus; PC1-4, precuneus contacts; EKG, electrocardiogram; EOG, electro-oculogram; EMG, electromyogram).
Overnight recording of simultaneous stereo-EEG and scalp EEG (reduced montage). Each EEG segment represents a 30-second epoch. (A) Wakefulness: the seizure onset zone (SOZ) exhibits the typical wake interictal activity of type II focal cortical dysplasia (FCD) consisting of sub-continuous rhythmic or sub-rhythmic spike- and polyspike-and-waves.3,7 Of note, this activity is...
We report a case of sleep related HMS shown to originate from the right mesial parietal lobe. Although the scalp EEG was negative for epileptiform discharges, clinical features were highly suggestive of sleep related epilepsy.1 Episodes occurred almost nightly, many times per night, and presented a short and stereotyped hypermotor pattern that ended abruptly. Immediately after, the patient was fully responsive.
We believe this case highlights interesting electro-clinical features of sleep related seizures. First, although HMS typically have a frontal lobe onset, a non-negligible proportion of cases have a SOZ outside the frontal lobe, most commonly from temporal or operculo-insular regions.1,3 Recent case-series of parietal-onset HMS have also been published, although none were sleep related.4,5 Nevertheless, it seems the spread of ictal activity in these cases follows the same epileptogenic network to engage or at least perturb the frontal lobe structures responsible for the hyperkinetic behavior.1,3,4 Clinically, the presence of an aura serves as a very useful diagnostic clue to localize HMS of extra-frontal onset.1,3,4 Moreover, in drug-resistant cases, the presence of a small type II FCD on brain MRI should strongly be suspected since this histopathological substrate has often been associated with sleep related seizures, independent of its cortical location.1,3 When the limits of such a lesion is unclear, as in our case, or overlaps eloquent cortex, invasive intracranial EEG monitoring is warranted, not to confirm the diagnosis of epilepsy but to identify the SOZ and possibly offer a curative surgical treatment.
Finally, EEG findings in this case allows to reiterate that: (1) a very active epileptogenic lesion can be undetectable on scalp,1 even when performing polysomnography with a full 10–20 EEG montage, known to increase the diagnostic and localization sensitivity of sleep related epilepsy6; and (2) the electrophysiological activity of type II FCD is greatly influenced by the sleep-wake cycle. During wakefulness and REM sleep, the FCD produces characteristic rhythmic and subcontinous spike- and polyspike- and wave discharges (Figure 2A). In NREM sleep, fewer spike-and-wave discharges are seen, replaced by frequent short-lasting bursts of low-voltage fast discharges (Figure 2B)3,7 in relation with arousal fluctuations, which may promote the appearance, synchronization, and spread of epileptiform discharges.8
This was not an industry supported study. The authors have indicated no financial conflicts of interest.
The authors thank our colleagues at the Claudio Munari Centre for Epilepsy Surgery. Dr. Gibbs gratefully acknowledges the support of the Fonds de recherche du Québec en Santé.
Nobili L, Proserpio P, Combi R, et al., authors. Nocturnal frontal lobe epilepsy. Curr Neurol Neurosci Rep. 2014;14:424. [PubMed]
Bonini F, McGonigal A, Trébuchon A, et al., authors. Frontal lobe seizures: from clinical semiology to localization. Epilepsia. 2014;55:264–77. [PubMed]
Proserpio P, Cossu M, Francione S, et al., authors. Epileptic motor behaviors during sleep: anatomo-electro-clinical features. Sleep Med. 2011;12 Suppl 2:S33–8. [PubMed]
Montavont A, Kahane P, Catenoix H, et al., authors. Hypermotor seizures in lateral and mesial parietal epilepsy. Epilepsy Behav. 2013;28:408–12. [PubMed]
Enatsu R, Bulacio J, Nair DR, Bingaman W, Najm I, Gonzalez-Martinez J, authors. Posterior cingulate epilepsy: clinical and neurophysiological analysis. J Neurol Neurosurg Psychiatry. 2014;85:44–50. [PubMed]
Foldvary-Schaefer N, De Ocampo J, Mascha E, Burgess R, Dinner D, Morris H, authors. Accuracy of seizure detection using abbreviated EEG during polysomnography. J Clin Neurophysiol. 2006;23:68–71. [PubMed]
Tassi L, Garbelli R, Colombo N, et al., authors. Electroclinical, MRI and surgical outcomes in 100 epileptic patients with type II FCD. Epileptic Disord. 2012;14:257–66. [PubMed]
Parrino L, Halasz P, Tassinari CA, Terzano MG, authors. CAP, epilepsy and motor events during sleep: the unifying role of arousal. Sleep Med Rev. 2006;10:267–85. [PubMed]
Description of Video 1
Video 1 shows different sleep related events during an overnight stereo-EEG recording of a patient with sleep-related hypermotor seizures (HMS). A paroxysmal arousal (PA) generally preceded the onset of the HMS, by approximately 1 minute (see text and Figure 2). Part 1 (PA): the patient experiences a sudden arousal with a startled facial expression followed by head elevation and rotation followed by a right-hand motion towards the forehead. Part 2 (HMS): the patient experiences a sudden arousal with head and trunk rocking movements. He adopts a dorsal decubitus position while correctly responding to the technician's questions. He then initiates bilateral leg adducting movements with mild pelvic thrashing and upper arm automatisms, repetitively touching his face with his right hand.