Cortico-striatal synchronization in human focal seizures

• Published in: Brain (London, England : 1878) England : 1878), 2019-05, Vol.142 (5), p.1282-1295
• Main Authors: Aupy, Jerome, Wendling, Fabrice, Taylor, Kenneth, Bulacio, Juan, Gonzalez-Martinez, Jorge, Chauvel, Patrick
• Format: Article
• Language: English
• Subjects: Adolescent; Adult; Bioengineering; Cerebral Cortex - diagnostic imaging; Cerebral Cortex - physiology; Child; Corpus Striatum - diagnostic imaging; Corpus Striatum - physiology; Cortical Synchronization - physiology; Electroencephalography - methods; Female; Humans; Life Sciences; Male; Middle Aged; Nerve Net - diagnostic imaging; Nerve Net - physiology; Prospective Studies; Seizures - diagnostic imaging; Seizures - physiopathology; Young Adult
• ISSN: 0006-8950; 1460-2156
• DOI: 10.1093/brain/awz062

Increasing evidence suggests an interaction between cortical and striatal signals during focal seizures. By studying stereoelectroencephalographic recordings in patients with drug-resistant epilepsy, Aupy et al. demonstrate that cortico-striatal synchronization may arise from the start of focal seizures and reach its maximum during their termination. Abstract Although a number of experimental and clinical studies have pointed out participation or an even more prominent role of basal ganglia in focal seizures, the mode of interaction between cortical and striatal signals remains unclear. In the present study, we took stereoelectroencephalographic (SEEG) recordings in drug-resistant epilepsy patients, to qualitatively and quantitatively analyse the ictal striatum activity as well as its synchronization with cerebral cortex. Eleven patients who underwent SEEG evaluation were prospectively included if they fulfilled two inclusion criteria: (i) at least one orthogonal intracerebral electrode contact explored the basal ganglia, in either their putaminal or caudate part; and (ii) at least two SEEG seizures were recorded. Cortical and subcortical regions of interest were defined and different periods of interest were analysed. SEEG was visually inspected and h2 non-linear correlation analysis performed to study functional connectivity between cortical region of interest and striatum. Six correlation indices were calculated. Two main patterns of striatal activation were recorded: the most frequent was characterized by an early alpha/beta activity that started within the first 5 s after seizure onset, sometimes concomitant with it. The second one was characterized by late, slower, theta/delta activity. A significant difference in h2 correlation indices was observed during the preictal and seizure onset period compared to background for global striatal index, mesio-temporal/striatal index, latero-temporal/striatal index, insular/striatal index, prefrontal/striatal index. In addition, a significant difference in h2 correlation indices was observed during the seizure termination period compared to all the other periods of interest for the six indices calculated. These results indicate that cortico-striatal synchronization can arise from the start of focal seizures. Depending on the ictal frequency pattern, desynchronization can occur later, but a late and terminal hypersynchronization progressively takes over. These changes in synchronization level between cortical and