In the last decade, single pulse electrical stimulation (SPES) has been used as an investigational tool in the field of epilepsy surgery. Direct cortical stimulation applied at a frequency of ∼1Hz can probe cortico-cortical connections by averaging electrocorticogram time-lock to the stimuli (2×20-30 trials). These evoked potentials that emanate from adjacent and remote cortices have been termed cortico-cortical evoked potentials (CCEPs). Although limited to patients undergoing invasive presurgical evaluations with intracranial electrodes, CCEP provides a novel way to explore inter-areal connectivity in vivo in the living human brain to probe functional brain networks such as language and cognitive motor networks. In addition to its impact on systems neuroscience, this method, in combination with 50Hz electrical cortical stimulation, could contribute clinically to map the functional brain systems by tracking the cortico-cortical connections among the functional cortical regions in each individual patient. This approach may help identify the normal cortico-cortical network within pathology as well as reveal connections that might arise from neural plasticity. Because of its high practicality, it has been recently applied for intraoperative monitoring of the functional brain networks for patients with brain tumor. With regard to epilepsy, SPES has been used for the two major purposes, one to probe cortical excitability of the focus, namely, epileptogenicity, and the other to probe seizure networks. Both early (i.e., CCEP) and delayed responses, and probably their high frequency oscillation counterparts, are regarded as a surrogate marker of epileptogenicity. With regards to its impact on the human brain connectivity map, worldwide collaboration is warranted to establish the standardized CCEP connectivity map as a solid reference for non-invasive connectome researches.

Single pulse electrical stimulation to probe functional and pathological connectivity in epilepsy.

Advances in human intracranial electroencephalography research, guidelines and good practices

Over the last decade, advances in genetics, neuroimaging and EEG have enabled the aetiology of epilepsy to be identified earlier in the disease course than ever before. At the same time, progress in the study of experimental models of epilepsy has provided a better understanding of the mechanisms underlying the condition and has enabled the identification of therapies that target specific aetiologies. We are now witnessing the impact of these advances in our daily clinical practice. Thus, now is the time for a paradigm shift in epilepsy treatment from a reactive attitude, treating patients after the onset of epilepsy and the initiation of seizures, to a proactive attitude that is more broadly integrated into a 'P4 medicine' approach. This P4 approach, which is personalized, predictive, preventive and participatory, puts patients at the centre of their own care and, ultimately, aims to prevent the onset of epilepsy. This aim will be achieved by adapting epilepsy treatments not only to a given syndrome but also to a given patient and moving from the usual anti-seizure treatments to personalized treatments designed to target specific aetiologies. In this Review, we present the current state of this ongoing revolution, emphasizing the impact on clinical practice.

Impact of predictive, preventive and precision medicine strategies in epilepsy.

With a prevalence of 0.8 to 1.2%, epilepsy represents one of the most frequent chronic neurological disorders; 30 to 40% of patients suffer from drug-resistant epilepsy (that is, seizures cannot be controlled adequately with antiepileptic drugs). Epilepsy surgery represents a valuable treatment option for 10 to 50% of these patients. Epilepsy surgery aims to control seizures by resection of the epileptogenic tissue while avoiding neuropsychological and other neurological deficits by sparing essential brain areas. The most common histopathological findings in epilepsy surgery specimens are hippocampal sclerosis in adults and focal cortical dysplasia in children. Whereas presurgical evaluations and surgeries in patients with mesial temporal sclerosis and benign tumors recently decreased in most centers, non-lesional patients, patients requiring intracranial recordings, and neocortical resections increased. Recent developments in neurophysiological techniques (high-density electroencephalography [EEG], magnetoencephalography, electrical and magnetic source imaging, EEG-functional magnetic resonance imaging [EEG-fMRI], and recording of pathological high-frequency oscillations), structural magnetic resonance imaging (MRI) (ultra-high-field imaging at 7 Tesla, novel imaging acquisition protocols, and advanced image analysis [post-processing] techniques), functional imaging (positron emission tomography and single-photon emission computed tomography co-registered to MRI), and fMRI significantly improved non-invasive presurgical evaluation and have opened the option of epilepsy surgery to patients previously not considered surgical candidates. Technical improvements of resective surgery techniques facilitate successful and safe operations in highly delicate brain areas like the perisylvian area in operculoinsular epilepsy. Novel less-invasive surgical techniques include stereotactic radiosurgery, MR-guided laser interstitial thermal therapy, and stereotactic intracerebral EEG-guided radiofrequency thermocoagulation.

/pdf/presurgical-epilepsy-evaluation-and-epilepsy-surgery-qdcrpdml69.pdf

Presurgical epilepsy evaluation and epilepsy surgery.

Why are people with focal epilepsy not continuously having seizures? Previous neuronal signaling work has implicated gamma-aminobutyric acid balance as integral to seizure generation and termination, but is a high-level distributed brain network involved in suppressing seizures? Recent intracranial electrographic evidence has suggested that seizure onset zones have increased inward connectivity which could be associated with interictal suppression of seizure activity. Accordingly, we hypothesize that seizure onset zones are actively suppressed by the rest of the brain network during interictal states. Full testing of this hypothesis would require collaboration across multiple domains of neuroscience. We focused on partially testing this hypothesis at the electrographic network level within 81 individuals with drug resistant focal epilepsy undergoing presurgical evaluation. We utilized intracranial electrographic resting-state and neurostimulation recordings to evaluate the network connectivity of seizure onset, early propagation, and non-involved zones. We then utilized diffusion imaging to acquire estimates of white matter connectivity to evaluate structure-function coupling effects on connectivity findings. Finally, we generated a resting-state classification model to assist clinicians in detecting seizure onset and propagation zones without the need for multiple ictal recordings. Our findings indicate that seizure onset and early propagation zones demonstrate markedly increased inward connectivity and decreased outward connectivity using both resting-state (one-way ANOVA, p-value=3.13e-13) and neurostimulation analyses to evaluate evoked responses (one-way ANOVA, p-value=2.5e-3). When controlling for the distance between regions, the difference between inward and outward connectivity remained stable up to 80 mm between brain connections (two-way repeated measures ANOVA, group effect p-value of 2.6e-12). Structure-function coupling analyses revealed that seizure onset zones exhibit abnormally enhanced coupling (hypercoupling) of surrounding regions compared to presumably healthy tissue (two-way repeated measures ANOVA, interaction effect p-value of 9.76e-21). Using these observations, our support vector classification models achieved a maximum held-out testing set accuracy of 92.0±2.2% to classify early propagation and seizure onset zones. These results suggest that seizure onset zones are actively segregated and suppressed by a widespread brain network. Furthermore, this electrographically observed functional suppression is disproportionate to any observed structural connectivity alterations of the seizure onset zones. These findings have implications for the identification of seizure onset zones using only brief electrographic recordings to reduce patient morbidity and augment the presurgical evaluation of drug resistant epilepsy. Further testing of the interictal suppression hypothesis can provide insight into potential new resective, ablative, and neuromodulation approaches to improve surgical success rates in those suffering from drug resistant focal epilepsy.

The interictal suppression hypothesis in focal epilepsy: network-level supporting evidence.

Single Pulse Electrical Stimulation to identify epileptogenic cortex: Clinical information obtained from early evoked responses.

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Single Pulse Electrical Stimulation to identify epileptogenic cortex: Clinical information obtained from early evoked responses.