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Control of Epileptic Seizures by the Basal Ganglia: Clinical and Experimental Approaches Feddersen Berend

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Control of Epileptic Seizures by the Basal Ganglia: Clinical and Experimental Approaches Feddersen Berend Control of epileptic seizures by the basal ganglia: clinical and experimental approaches Feddersen Berend To cite this version: Feddersen Berend. Control of epileptic seizures by the basal ganglia: clinical and experimental ap- proaches. Neurons and Cognition [q-bio.NC]. Université Joseph-Fourier - Grenoble I, 2009. English. tel-00413972 HAL Id: tel-00413972 https://tel.archives-ouvertes.fr/tel-00413972 Submitted on 7 Sep 2009 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Ecole Doctorale Chimie et Sciences du Vivant UNIVERSITE JOSEPH FOURIER GRENOBLE Thèse Neuroscience - Neurobiologie Berend Feddersen Control of epileptic seizures by the basal ganglia: clinical and experimental approaches Soutenue publiquement le: 10.07.2009 Membres du jury : Franck Semah (Rapporteur 1) Stephane Charpier (Rapporteur 2) Philippe Kahane Soheyl Noachtar Antoine Depaulis (Directeur de thèse) Colin Deransart 1 ACKNOWLEDGEMENTS Many fantastic people were inolved in this thesis, whom I want to thank deeply for all their help and support. I want to thank my supervisors Soheyl Noachtar, Antoine Depaulis and Colin Deransart for all their help and fruitfull discussions in every kind of situation. Sohyel Nochtar teached me in a perfect structured manner clinical epileptology and gave me always all the support I needed, especially for my stay in Grenoble. Antoine Depaulis and Colin Deransart were at the origin of the enthusiasm for animal studies in epilepsy. They showed me how exciting stereotactic surgery in small animals can be, and were always present for discussions and helpfull comments on any sort of problems, not only related to my thesis. Sorry for the numerous “last minute corrections”. It is wonderful to have you as friends, thanks a lot also to your families for all the hospitality you gave me. I thank the reporters of this jury for having agreed to judge this work and for all the comments to improve this thesis. I wanted to thank also all members of the lab for such a wonderful year in Grenoble, especially Karine Bressand. Merci beaucoup aussi aux cliniciens et techniciens du laboratoire EEG à Grenoble und in München, für die gute Atmosphäre und Hilfe. Ralph Meier is thanked for his help and co-work in the field of coherence analysis and EEG-signaling-post-processing. I want to thank the European Neurological Society (ENS) for the 12 months fellowship and financial support for my stay in Grenoble. Ein ganz besonderer Dank geht an Pia, meine Frau, die mit viel Verständnis und Unterstützung nicht nur diese Arbeit begleitet hat. Vielen Dank für alles! 2 Bei Edgar, Emil und Anton möchte ich mich für die Zeit entschuldigen, die ich nicht mit Ihnen, sondern am Computer verbracht habe. Ein besonderer Dank geht an Gisela und Felix für das "einhüten" und die ständige Unterstützung zu Hause. Felix, Danke für die aufmunternden Worte und den Glauben daran, dass ich es schaffen kann. Natürlich haben auch meine Eltern eine riesengrossen Dank verdient. Friddi und Jens, danke, dass ihr mich bei der Umsetzung all meiner Plänen unterstützt habt. Ausserdem habt ihr den Grundstein für die enge Verbundenheit nach Frankreich gelegt. Merci beaucoup à tous. 3 INDEX ABBREVIATIONS 9 LIST OF FIGURES AND TABLES 10 RESUME EN FRANÇAIS 11 ENGLISH ABSTRACT 13 PROLOGUE 15 I. INTRODUCTION 17 A. The epilepsies 17 1. Epileptic seizures 1.1. Classification of epileptic seizures 18 1.2. Semiological seizure classification 19 1.3. The epileptogenic zone 23 1.4. Localizing significance of different seizure types 24 1.5. Localizing significance of different seizure evolutions 26 1.6. Ictal lateralizing phenomena 26 2. Epileptic syndromes 29 2.1. Mesial temporal lobe epilepsy (mTLE) 32 2.2. Neocortical temporal lobe epilepsy (nTLE) 32 2.3. Frontal lobe epilepsy (FLE) 32 2.4. Parietal lobe epilepsy (PLE) 33 2.5. Occipital lobe epilepsy (OLE) 33 3. Status epilepticus 33 4. Intractable epilepsy 34 5. Treatment of epilepsy 36 5.1. Pharmacological therapy 36 5.2. Resective surgical therapy 38 5.3. Multiple subpiale transsection 41 5.4. Callosotomie 41 5.5. Neurostimulation 41 5.5.1. Vagus Nerve Stimulation 41 5.5.2. Stimulation of the epileptic focus 42 5.5.3. Deep brain stimulation 44 Thalamus 45 Subthalamicus nucleus 47 4 B. The basal ganglia 6. Organisation of the basal ganglia 48 6.1. Organisation of basal ganglia circuits 51 6.2. Organisation of functional loop systems within the basal ganglia 53 7. Involvement of the basal ganglia in the control of epileptic seizures 55 7.1. Animal studies 55 7.1.1. Pharmacology 55 Striatum 55 Subthalamic nucleus 56 Substantia nigra 57 7.1.2. Electrophysiology 58 Striatum 58 Subthalamic nucleus 59 Substantia nigra 60 7.1.3. Metabolism 60 7.1.4. Deep brain stimulation 61 Stimulation of the caudate nucleus 62 Stimulation of the subthalamic nucleus 62 Stimulation of the substantia nigra pars reticulata 63 7.2. Clinical studies 64 7.2.1. Pharmacology 64 7.2.2. Electrophysiology 65 7.2.3. Imaging 66 7.2.4. Deep brain stimulation 68 Stimulation of the caudate nucleus 68 Stimulation of the subthalamic nucleus 69 II. QUESTIONS AND OBJECTIVES 70 1. Does seizure spread to the basal ganglia inhibits secondary generalization in focal epilepsies? 70 2. What are the optimal single stimulation parameters for acute 5 seizure interruption? 71 3. What are the optimal repeated stimulation parameters for sustained seizure suppression? 71 4. Is it possible to characterize markers that heralds epileptic seizures into the basal ganglia? 72 The GAERS model 73 III. RESULTS 75 Main findings 1. B. Feddersen, J. Remi, M. Kilian, L. Vercueil, C. Deransart, A. Depaulis, S. Noachtar, Does ictal dystonia have an inhibitory effect on seizure propagation in focal epilepsies? Submitted to Epilepsia as a full-length original research article. 76 2. B. Feddersen, L. Vercueil, S. Noachtar, O. David, A. Depaulis, C. Deransart. Controlling seizures is not controlling epilepsies: a parametric study of deep brain stimulation for epilepsy. Neurobiology of Disease 2007; 27: 292-300. 77 3. B. Feddersen, R. Meier, A. Depaulis, C. Deransart. EEG Changes Between Left and Right Substantia Nigra Heralds the Occurrence of Generalized Seizures in a model of GAERS. In preparation, to be submitted to Epilepsia as a short communication.78 4. M. Langlois, S. Saillet, B. Feddersen, L Minotti, L Vercueil, S Chabardès, O. David, A. Depaulis, P. Kahane, C. Deransart. Deep brain stimulation in epilepsy: experimental and clinical data. In: Deep Brain Stimulation. Mark H. Rogers and Paul B. Anderson Eds. Nova Science Publishers, Inc. 2009, in press. 79 IV. DISCUSSION 80 1. Question 1: Which epileptic syndromes and seizures are optimal for deep brain stimulation in epilepsy? 80 Can epileptic candidates for deep brain stimulation be selected - According to their seizure semiology? 80 6 - According to the seizure focus? 82 - According to their deficit in dopaminergic functions? 83 2. Question 2: What is the optimal target for deep brain stimulation in epilepsy? 87 2.1. Anatomical considerations 87 2.1.1. Stimulation of the focus 87 2.1.2. Thalamus stimulation 88 2.1.2.1. Anterior nucleus 88 2.1.2.2. Centromedian nucleus 89 2.1.3. Stimulation of the basal ganglia 89 2.1.3.1. Caudate nucleus 89 2.1.3.2. Subthalamic nucleus 90 2.1.3.3. Substantia nigra pars reticulata 90 2.2. Considerations according to the seizure onset zone 91 2.3. Considerations according to the mechanism of action of deep brain stimulation 92 3. Question 3: Which are the optimal parameters in deep brain stimulation 3.1. for acute seizure interruption? 93 3.2. for repeated seizure interruption? 95 4. Seizure aggravation by substantia nigra pars reticulata stimulation 97 5. How can seizures be predicted to release a seizure triggered closed-loop stimulation? 98 V. CONCLUSION 100 VI. PERSPECTIVES 101 1. Animal studies 101 2. Human studies 102 7 REFERENCES 104 SCIENTIFIC PRODUCTION 121 Article 1 121 Article 2 138 Article 3 148 Article 4 158 Original publications 183 Book chapters 186 Abstracts 187 Letters 191 Oral presentation 191 Grants and Awards 194 ANNEXE 195 8 ABBREVIATIONS AN - Anterior nucleus (of the thalamus) CM - Centromedian Thalamus CN - Caudate nucleus DBS - Deep brain stimulation GABA - Gamma-Amino-Butyric-Acid GAERS - Genetic Absence Epilepsy Rats from Strasbourg GP - Globus pallidus GPe - Globus pallidus externus GPi - Globus pallidus internus HFS - High-frequency stimulation ID - ictal dystonia ILAE - International League Against Epilepsy SN - Substantia nigra SNr - Substantai nigra pars reticulata SNc - Substantia nigra pars compacta STN - Subthalamic nucleus MRI - Magnet Resonance Imaging PET - Positron emission tomography SPECT - Single photon emission computed tomography TLE - Temporal lobe epilepsy mTLE - mesial temporal lobe epilepsy nTLE - neocortical temporal lobe epilepsy PLE - Parietal lobe epilepsy OLE - Occipital lobe epilepsy RNS - Responsive neuro-stimulation system SUDEP - Sudden Unexpected Death in Epilepsy VM - ventro medial (thalamus) VNS - Vagal nerve stimulation 9 LIST OF FIGURES AND TABLES Figures : Figure 1: Overview
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