Desynchronization of temporal lobe theta-band activity during effective anterior thalamus deep brain stimulation in epilepsy
Maximillian Scherer,
Luka Milosevic,
Robert Guggenberger,
Volker Maus,
Georgios Naros,
Florian Grimm,
Iancu Bucurenciu,
Bernhard J. Steinhoff,
Yvonne G. Weber,
Holger Lerche,
Daniel Weiss,
Sabine Rona,
Alireza Gharabaghi
Affiliations
Maximillian Scherer
Division of Functional and Restorative Neurosurgery, Department of Neurosurgery, And Tübingen NeuroCampus, University of Tübingen, 72076, Tübingen, Germany
Luka Milosevic
Division of Functional and Restorative Neurosurgery, Department of Neurosurgery, And Tübingen NeuroCampus, University of Tübingen, 72076, Tübingen, Germany
Robert Guggenberger
Division of Functional and Restorative Neurosurgery, Department of Neurosurgery, And Tübingen NeuroCampus, University of Tübingen, 72076, Tübingen, Germany
Volker Maus
Division of Functional and Restorative Neurosurgery, Department of Neurosurgery, And Tübingen NeuroCampus, University of Tübingen, 72076, Tübingen, Germany
Georgios Naros
Division of Functional and Restorative Neurosurgery, Department of Neurosurgery, And Tübingen NeuroCampus, University of Tübingen, 72076, Tübingen, Germany
Florian Grimm
Division of Functional and Restorative Neurosurgery, Department of Neurosurgery, And Tübingen NeuroCampus, University of Tübingen, 72076, Tübingen, Germany
Iancu Bucurenciu
Kork Epilepsy Center, Kehl-Kork, Germany
Bernhard J. Steinhoff
Kork Epilepsy Center, Kehl-Kork, Germany
Yvonne G. Weber
Department of Neurology and Epileptology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany; Epilepsy Unit, Department of Neurosurgery, University of Tübingen, Tübingen, Germany
Holger Lerche
Department of Neurology and Epileptology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
Daniel Weiss
Department for Neurodegenerative Diseases, Hertie Institute for Clinical Brain Research, And German Centre of Neurodegenerative Diseases (DZNE), University Tübingen, Tübingen, Germany
Sabine Rona
Epilepsy Unit, Department of Neurosurgery, University of Tübingen, Tübingen, Germany
Alireza Gharabaghi
Division of Functional and Restorative Neurosurgery, Department of Neurosurgery, And Tübingen NeuroCampus, University of Tübingen, 72076, Tübingen, Germany; Corresponding author. Division of Functional and Restorative Neurosurgery, University of Tübingen, Otfried-Mueller-Str.45, 72076, Tübingen, Germany.
Background: Bilateral cyclic high frequency deep brain stimulation (DBS) of the anterior nucleus of the thalamus (ANT) reduces the seizure count in a subset of patients with epilepsy. Detecting stimulation-induced alterations of pathological brain networks may help to unravel the underlying physiological mechanisms related to effective stimulation delivery and optimize target engagement. Methods: We acquired 64-channel electroencephalography during ten ANT-DBS cycles (145 Hz, 90 μs, 3–5 V) of 1-min ON followed by 5-min OFF stimulation to detect changes in cortical activity related to seizure reduction. The study included 14 subjects (three responders, four non-responders, and seven healthy controls). Mixed-model ANOVA tests were used to compare differences in cortical activity between subgroups both ON and OFF stimulation, while investigating frequency-specific effects for the seizure onset zones. Results: ANT-DBS had a widespread desynchronization effect on cortical theta and alpha band activity in responders, but not in non-responders. Time domain analysis showed that the stimulation induced reduction in theta-band activity was temporally linked to the stimulation period. Moreover, stimulation induced theta-band desynchronization in the temporal lobe channels correlated significantly with the therapeutic response. Responders to ANT-DBS and healthy-controls had an overall lower level of theta-band activity compared to non-responders. Conclusion: This study demonstrated that temporal lobe channel theta-band desynchronization may be a predictive physiological hallmark of therapeutic response to ANT-DBS and may be used to improve the functional precision of this intervention by verifying implantation sites, calibrating stimulation contacts, and possibly identifying treatment responders prior to implantation.
