Intracranial electroencephalographic seizure-onset patterns: effect of underlying pathology

Abstract

Because seizures originate from different pathological substrates, the question arises of whether distinct or similar mechanisms underlie seizure generation across different pathologies. Better defining intracranial electroencephalographic morphological patterns at seizure-onset could improve the understanding of such mechanisms. To this end, we investigated intracranial electroencephalographic seizure-onset patterns associated with different epileptogenic lesions, and defined high-frequency oscillation correlates of each pattern. We analysed representative seizure types from 33 consecutive patients with drug-resistant focal epilepsy and a structural magnetic resonance imaging lesion (11 mesial temporal sclerosis, nine focal cortical dysplasia, six cortical atrophy, three periventricular nodular heterotopia, three polymicrogyria, and one tuberous sclerosis complex) who underwent depth-electrode electroencephalographic recordings (500 Hz filter, 2000 Hz sampling rate). Patients were included only if seizures arose from contacts located in lesional/peri-lesional tissue, and if clinical manifestations followed the electrographic onset. Seizure-onset patterns were defined independently by two reviewers blinded to clinical information, and consensus was reached after discussion. For each seizure, pre-ictal and ictal sections were selected for high-frequency oscillation analysis. Seven seizure-onset patterns were identified across the 53 seizures sampled: low-voltage fast activity (43%); low-frequency high-amplitude periodic spikes (21%); sharp activity at ≤13 Hz (15%); spike-and-wave activity (9%); burst of high-amplitude polyspikes (6%); burst suppression (4%); and delta brush (4%). Each pattern occurred across several pathologies, except for periodic spikes, only observed with mesial temporal sclerosis, and delta brush, exclusive to focal cortical dysplasia. However, mesial temporal sclerosis was not always associated with periodic spikes nor focal cortical dysplasia with delta brush. Compared to other patterns, low-voltage fast activity was associated with a larger seizure-onset zone (P = 0.04). Four patterns, sharp activity at ≤13 Hz, low-voltage fast activity, spike-and-wave activity and periodic spikes, were also found in regions of seizure spread, with periodic spikes only emerging from mesial temporal sclerosis. Each of the seven patterns was accompanied by a significant increase in high-frequency oscillations upon seizure-onset. Overall, our data indicate that: (i) biologically-distinct epileptogenic lesions share intracranial electroencephalographic seizure-onset patterns, suggesting that different pathological substrates can affect similarly networks or mechanisms underlying seizure generation; (ii) certain pathologies are associated with intracranial electroencephalographic signatures at seizure-onset, e.g. periodic spikes which may reflect mechanisms specific to mesial temporal sclerosis; (iii) some seizure-onset patterns, including periodic spikes, can also be found in regions of spread, which cautions a...

Advances of Intracranial Electroencephalography in Localizing the Epileptogenic Zone

“…But these features are commonly used to identify the seizure onset zone (SOZ), so long as the changes are relatively focal in one or a small number of electrodes and are recorded before the first clinical sign. Low-voltage fast activity [2][3][4][5] is the most commonly reported IOP in neocortical epilepsy, and low-frequency high-amplitude repetitive spiking is the most commonly reported IOP in mesial temporal lobe epilepsy (mTLE). Delta activity is usually held to be a spread pattern rather than a true IOP from the SOZ.…”

Initiation, Propagation, and Termination of Partial (Focal) Seizures

“…With some exceptions, seizure patterns recorded in different lobes and cortical areas do not differ substantially. In a recent report, among seven types of intracranial EEG seizure patterns identified in a population of patients with partial epilepsies caused by different etiologies (Perucca et al 2014), two were the most commonly observed (see below). Ictal patterns specific for the underlying epileptogenic lesion have been described in type IIb focal cortical dysplasias (Tassi et al 2002), periventricular heterotopias , and mesial TLE with massive cell loss and gliosis (Spencer and Pappas 1992;Ogren et al 2009).…”

“…The hypersynchronous pattern is most often seen in TLEs with hippocampal sclerosis Ogren et al 2009) and was never reported in neocortical focal epilepsies. Other less frequent patterns of seizure initiation have been described (Perucca et al 2014) and are interpreted as either propagated activity or "far fields," which are volume-conducted from the cortical generators. These patterns, therefore, do not localize the epileptogenic network.…”

“…These two patterns may be the expression of the activation of the same networks, because the large-amplitude spikes typically detected in the hypersynchronous pattern are often followed by short runs of low-voltage fast activity (Perucca et al 2014). In line with the concept of the epileptic network, experimental work has shown that both patterns are generated by the limbic system in vivo in the pilocarpine model of mesial TLE (Levesque et al 2012), and in the in vitro whole guinea pig brain treated with different proconvulsive drugs, such as bicuculline or 4-aminopyridine (4AP) (Uva et al 2005;Carriero et al 2010;Boido et al 2014a).…”

“…The electrographic epileptiform patterns expressed during a partial seizure are distinctive for the structures and networks entrained by the seizure discharge and, with some exceptions (see below), they are thought to be independent of the original primary insult (Pelliccia et al 2013;Perucca et al 2014). The existence of system-specific susceptibility to seizures and epi-lepsy is supported by the demonstration that arterial perfusion of proconvulsive drugs induce acute interictal and ictal epileptiform patterns, which are segregated to specific cortical systems (Librizzi and de Curtis 2003;Boido et al 2014a).…”