Loss of consciousness (LOC) is a dramatic clinical manifestation of temporal lobe seizures. Its underlying mechanism could involve altered coordinated neuronal activity between the brain regions that support conscious information processing. The consciousness access hypothesis assumes the existence of a global workspace in which information becomes available via synchronized activity within neuronal modules, often widely distributed throughout the brain. Re-entry loops and, in particular, thalamo-cortical communication would be crucial to functionally bind different modules together. In the present investigation, we used intracranial recordings of cortical and subcortical structures in 12 patients, with intractable temporal lobe epilepsy (TLE), as part of their presurgical evaluation to investigate the relationship between states of consciousness and neuronal activity within the brain. The synchronization of electroencephalography signals between distant regions was estimated as a function of time by using non-linear regression analysis. We report that LOC occurring during temporal lobe seizures is characterized by increased long-distance synchronization between structures that are critical in processing awareness, including thalamus (Th) and parietal cortices. The degree of LOC was found to correlate with the amount of synchronization in thalamo-cortical systems. We suggest that excessive synchronization overloads the structures involved in consciousness processing, preventing them from treating incoming information, thus resulting in LOC.
Summary
Purpose: Loss of consciousness (LOC) in epileptic seizures has a strongly negative impact on quality of life. Recently, we showed that LOC occurring during temporal lobe seizures was correlated with a nonlinear increase of neural synchrony in associative—and particularly parietal—cortices. Whether these mechanisms might be observed in other types of seizures is unknown. This study aimed at investigating the relationship between changes in synchrony and degree of LOC during parietal lobe epilepsy (PLE), a form of epilepsy in which seizures directly involve the parietal associative cortices.
Methods: Ten patients undergoing stereoelectroencephalography (SEEG) during presurgical evaluation of PLE were studied. The LOC intensity was scored using the Conscious Seizure Scale (CSS). For each studied seizure (n = 29), interdependencies between signals recorded from six brain regions were estimated as a function of time by using nonlinear regression analysis (h2 coefficient).
Key Findings: Seizures were divided into three groups according to the CSS scale: group A (no LOC) with a score ≤1, group B (intermediate or partial LOC) with a score ranging from 2 to 5, and group C (maximal LOC) with a score ≥6. The majority of seizures in patients with PLE disclosed significant LOC (17/29, group C). Mean h2 values were significantly different between the three groups (p = 0.008), the maximal values of synchrony being observed in group C. In addition, a statistically significant nonlinear relationship (p = 0.0021) was found between the h2 values and the CSS scores, suggesting a threshold effect.
Significance: This study indicates that excess of EEG signal synchrony within associative cortices is likely to be a crucial phenomenon associated with LOC.
Forced normalization is a clinical entity defined by the appearance of psychiatric disturbance following control of epileptic seizures that were previously uncontrolled. It was first described by Landolt in 1953. The first cases described were mostly psychosis, however, subsequent work suggested that any behavioural disturbance of acute/or subacute onset concomitant with seizure control could be considered as forced normalization. We report the case of a 65‐year‐old, right‐handed Caucasian patient who was followed in the Epilepsy Centre of Marseille, for left temporal drug‐resistant epilepsy. The frequency of seizures was one seizure per month at the time before surgery. Left anterior temporal lobectomy was proposed based on presurgical evaluation. The patient remained seizure‐free after surgery, but he presented with an episode of acute psychosis three months after. At this point, EEG was performed, showing rare left temporal epileptiform activity mainly provoked by hyperventilation, with breach rhythm over the left temporal surgical. The appearance of acute psychosis after cessation of epileptic seizures and reduced epileptiform activity on the EEG led us to question the forced normalization process in this case. Another hypothesis would be the effect of surgery itself, since there is an increased risk of any psychiatric disturbance unrelated to seizure cessation during the postoperative period. In conclusion, psychosis in this case could have resulted from the combination of several factors, including the effect of surgery itself and seizure cessation. This case illustrates the need for specific psychiatric care in the perioperative period in patients with epilepsy.
Psychogenic nonepileptic seizures (PNES) are paroxysmal clinical events that are often misdiagnosed as epileptic seizures, but which are not associated with electrographic discharge. Brain connectivity changes occurring during PNES are not known. We studied functional connectivity (Fc) in two patients with drug-resistant epilepsy, explored by stereotactic electroencephalography (EEG), in whom we recorded both epileptic seizures (ES) and PNES. Functional connectivity using pair-wise nonlinear correlation was computed between signals from seven brain areas: amygdala, hippocampus, lateral temporal cortex, anterior insula, orbitofrontal cortex, prefrontal cortex, and lateral parietal cortex. We assessed changes in global Fc during PNES in comparison with a background period. During PNES, a global decrease of Fc occurred between the different brain regions studied, compared with the interictal period. In both patients, decreased Fc was prominent in connections involving the anterior insula and parietal cortex. In conclusion, some PNES are associated with ictal functional disconnection between brain areas, particularly involving the parietal cortices and the anterior insula.
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