Transient alteration of awareness triggered by direct electrical stimulation of the brain

• Published in: Brain stimulation 2024-09, Vol.17 (5), p.1024-1033
• Main Authors: Lévi-Strauss, Julie, Makhalova, Julia, Medina Villalon, Samuel, Carron, Romain, Bénar, Christian G., Bartolomei, Fabrice
• Format: Article
• Language: English
• Subjects: Adult; Awareness; Awareness - physiology; Brain - diagnostic imaging; Brain - physiology; Brain - physiopathology; Brain stimulation; Disorders of consciousness; Drug Resistant Epilepsy - diagnostic imaging; Drug Resistant Epilepsy - physiopathology; Drug Resistant Epilepsy - therapy; Electric Stimulation - methods; Electroencephalography - methods; Female; Focal epilepsy; Humans; Male; Neurophysiology; Young Adult
• ISSN: 1935-861X; 1876-4754; 1876-4754
• DOI: 10.1016/j.brs.2024.08.013

Awareness is a state of consciousness that enables a subject to interact with the environment. Transient alteration of awareness (AA) is a disabling sign of many types of epileptic seizures. The brain mechanisms of awareness and its alteration are not well known. Transient and isolated AA induced by electrical brain stimulation during a stereoelectroencephalography (SEEG) recording represents an ideal model for studying the associated modifications of functional connectivity and locating the hubs of awareness networks. We investigated the SEEG signals-based brain functional connectivity (FC) changes vs background occurring during AA triggered by three thalamic and two insular stimulations in three patients explored by SEEG in the frame of presurgical evaluation for focal drug-resistant epilepsy. The results were compared to the stimulations of the same sites that did not induce clinical changes (negative stimulations). We observed decreased node strength in the pulvinar, insula, and parietal associative cortices during the thalamic and insular stimulations that induced AA. The link strengths characterizing functional coupling between the thalamus and the insular, prefrontal, temporal, or parietal associative cortices were also decreased. In contrast, there was an increased synchronization between the precuneus and the temporal lateral cortex. These FC changes were absent during the negative stimulations. Our study highlights the role of the pulvinar, insular, and parietal hubs in maintaining the awareness networks and paves the way for invasive or non-invasive neuromodulation protocols to reduce AA manifestations during epileptic seizures. •Altered awareness is a disabling sign of many types of epileptic seizures.•Stimulations of the insula and thalamus can induce transient alteration of awareness.•Pulvinar, insular, and parietal hubs are involved in maintaining awareness.•Altered awareness was associated with a decrease in thalamocortical synchrony.