Long-term deep intracerebral microelectrode recordings in patients with drug-resistant epilepsy: Proposed guidelines based on 10-year experience
Katia Lehongre,
Virginie Lambrecq,
Stephen Whitmarsh,
Valerio Frazzini,
Louis Cousyn,
Daniel Soleil,
Sara Fernandez-Vidal,
Bertrand Mathon,
Marion Houot,
Jean-Didier Lemaréchal,
Stéphane Clemenceau,
Dominique Hasboun,
Claude Adam,
Vincent Navarro
Affiliations
Katia Lehongre
Sorbonne Université, Paris Brain Institute – Institut du Cerveau, ICM, INSERM, CNRS, APHP, Pitié-Salpêtrière Hospital, Paris France
Virginie Lambrecq
Sorbonne Université, Paris Brain Institute – Institut du Cerveau, ICM, INSERM, CNRS, APHP, Pitié-Salpêtrière Hospital, Paris France; AP-HP, EEG Unit, Neurophysiology Department, Pitié-Salpêtrière Hospital, DMU Neurosciences, Paris, France; AP-HP, Epilepsy Unit, Pitié-Salpêtrière Hospital, DMU Neurosciences, Paris, France
Stephen Whitmarsh
Sorbonne Université, Paris Brain Institute – Institut du Cerveau, ICM, INSERM, CNRS, APHP, Pitié-Salpêtrière Hospital, Paris France
Valerio Frazzini
Sorbonne Université, Paris Brain Institute – Institut du Cerveau, ICM, INSERM, CNRS, APHP, Pitié-Salpêtrière Hospital, Paris France; AP-HP, EEG Unit, Neurophysiology Department, Pitié-Salpêtrière Hospital, DMU Neurosciences, Paris, France; AP-HP, Epilepsy Unit, Pitié-Salpêtrière Hospital, DMU Neurosciences, Paris, France
Louis Cousyn
Sorbonne Université, Paris Brain Institute – Institut du Cerveau, ICM, INSERM, CNRS, APHP, Pitié-Salpêtrière Hospital, Paris France; AP-HP, Epilepsy Unit, Pitié-Salpêtrière Hospital, DMU Neurosciences, Paris, France
Daniel Soleil
Bureau d'Etudes CEMS, 801 Route d'Eyguieres, 13 560 Senas, France
Sara Fernandez-Vidal
Sorbonne Université, Paris Brain Institute – Institut du Cerveau, ICM, INSERM, CNRS, APHP, Pitié-Salpêtrière Hospital, Paris France
Bertrand Mathon
Sorbonne Université, Paris Brain Institute – Institut du Cerveau, ICM, INSERM, CNRS, APHP, Pitié-Salpêtrière Hospital, Paris France; AP-HP, Neurosurgery Department, Pitié-Salpêtrière Hospital, Paris, France
Marion Houot
Centre of Excellence of Neurodegenerative Disease (CoEN), AP-HP, Pitié-Salpêtrière Hospital, Paris, France; Institute of Memory and Alzheimer's Disease (IM2A), Department of Neurology, AP-HP, Pitié-Salpêtrière Hospital, Paris, France.; Clinical Investigation Centre, Institut du Cerveau et de la Moelle épinière (ICM), Pitié-Salpêtrière Hospital Paris, France
Jean-Didier Lemaréchal
Sorbonne Université, Paris Brain Institute – Institut du Cerveau, ICM, INSERM, CNRS, APHP, Pitié-Salpêtrière Hospital, Paris France; Institut de Neurosciences des Systèmes, Aix-Marseille Université, Marseille, France
Stéphane Clemenceau
AP-HP, Neurosurgery Department, Pitié-Salpêtrière Hospital, Paris, France
Dominique Hasboun
Sorbonne Université, Paris Brain Institute – Institut du Cerveau, ICM, INSERM, CNRS, APHP, Pitié-Salpêtrière Hospital, Paris France; AP-HP, Neuroradiologiy Department, Pitié-Salpêtrière Hospital, Paris, France
Claude Adam
AP-HP, Epilepsy Unit, Pitié-Salpêtrière Hospital, DMU Neurosciences, Paris, France
Vincent Navarro
Sorbonne Université, Paris Brain Institute – Institut du Cerveau, ICM, INSERM, CNRS, APHP, Pitié-Salpêtrière Hospital, Paris France; AP-HP, EEG Unit, Neurophysiology Department, Pitié-Salpêtrière Hospital, DMU Neurosciences, Paris, France; AP-HP, Epilepsy Unit, Pitié-Salpêtrière Hospital, DMU Neurosciences, Paris, France; AP-HP, Center of Reference for Rare Epilepsies, Pitié-Salpêtrière Hospital, Paris, France; Corresponding author at: AP-HP, Epilepsy Unit, Pitié-Salpêtrière Hospital, 47-83 Boulevard de l'Hôpital, Paris 75013, France.
Purpose: Human neuronal activity, recorded in vivo from microelectrodes, may offer valuable insights into physiological mechanisms underlying human cognition and pathophysiological mechanisms of brain diseases, in particular epilepsy. Continuous and long-term recordings are necessary to monitor non predictable pathological and physiological activities like seizures or sleep. Because of their high impedance, microelectrodes are more sensitive to noise than macroelectrodes. Low noise levels are crucial to detect action potentials from background noise, and to further isolate single neuron activities. Therefore, long-term recordings of multi-unit activity remains a challenge. We shared here our experience with microelectrode recordings and our efforts to reduce noise levels in order to improve signal quality. We also provided detailed technical guidelines for the connection, recording, imaging and signal analysis of microelectrode recordings. Results: During the last 10 years, we implanted 122 bundles of Behnke-Fried hybrid macro-microelectrodes, in 56 patients with pharmacoresistant focal epilepsy. Microbundles were implanted in the temporal lobe (74%), as well as frontal (15%), parietal (6%) and occipital (5%) lobes. Low noise levels depended on our technical setup. The noise reduction was mainly obtained after electrical insulation of the patient's recording room and the use of a reinforced microelectrode model, reaching median root mean square values of 5.8 µV. Seventy percent of the bundles could record multi-units activities (MUA), on around 3 out of 8 wires per bundle and for an average of 12 days. Seizures were recorded by microelectrodes in 91% of patients, when recorded continuously, and MUA were recorded during seizures for 75 % of the patients after the insulation of the room. Technical guidelines are proposed for (i) electrode tails manipulation and protection during surgical bandage and connection to both clinical and research amplifiers, (ii) electrical insulation of the patient's recording room and shielding, (iii) data acquisition and storage, and (iv) single-units activities analysis. Conclusions: We progressively improved our recording setup and are now able to record (i) microelectrode signals with low noise level up to 3 weeks duration, and (ii) MUA from an increased number of wires . We built a step by step procedure from electrode trajectory planning to recordings. All these delicate steps are essential for continuous long-term recording of units in order to advance in our understanding of both the pathophysiology of ictogenesis and the neuronal coding of cognitive and physiological functions.