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Implantable Microelectrodes on Soft Substrate with Nanostructured Active Surface for Stimulation and Recording of Brain Activities Valentina Castagnola

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Implantable Microelectrodes on Soft Substrate with Nanostructured Active Surface for Stimulation and Recording of Brain Activities Valentina Castagnola Implantable microelectrodes on soft substrate with nanostructured active surface for stimulation and recording of brain activities Valentina Castagnola To cite this version: Valentina Castagnola. Implantable microelectrodes on soft substrate with nanostructured active sur- face for stimulation and recording of brain activities. Micro and nanotechnologies/Microelectronics. Universite Toulouse III Paul Sabatier, 2014. English. tel-01137352 HAL Id: tel-01137352 https://hal.archives-ouvertes.fr/tel-01137352 Submitted on 31 Mar 2015 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. THÈSETHÈSE En vue de l’obtention du DOCTORAT DE L’UNIVERSITÉ DE TOULOUSE Délivré par : l’Université Toulouse 3 Paul Sabatier (UT3 Paul Sabatier) Présentée et soutenue le 18/12/2014 par : Valentina CASTAGNOLA Implantable Microelectrodes on Soft Substrate with Nanostructured Active Surface for Stimulation and Recording of Brain Activities JURY M. Frédéric MORANCHO Professeur d’Université Président de jury M. Blaise YVERT Directeur de recherche Rapporteur Mme Yael HANEIN Professeur d’Université Rapporteur M. Pascal MAILLEY Directeur de recherche Examinateur M. Christian BERGAUD Directeur de recherche Directeur de thèse Mme Emeline DESCAMPS Chargée de Recherche Directeur de thèse École doctorale et spécialité : GEET : Micro et Nanosystèmes Unité de Recherche : Laboratoire d’Analyse et d’Architecture des Systèmes (UPR 8001) Directeur(s) de Thèse : M. Christian BERGAUD et Mme Emeline DESCAMPS Rapporteurs : M. Blaise YVERT et Mme Yael HANEIN a Luca... "Nihil est in intellectu quod non fuerit in sensu, excipe: nisi intetlectus ipse" Gottfried Wilhelm von Leibniz, Monadology "To light a candle is to cast a shadow" Ursula K. Le Guin, A Wizard of Earthsea "Siamo ancora dove il buon pan si cuoce..." Anonimo montanaro Abstract Implantable microelectrodes on soft substrate with nanostructured active surface for stimulation and recording of brain activities Implantable neural prosthetics devices offer, nowadays, a promising opportunity for the restoration of lost functions in patients affected by brain or spinal cord injury, by providing the brain with a non-muscular channel able to link machines to the nervous system. The long-term reliability of these devices constituted by im- plantable electrodes has emerged as a crucial factor in view of the application in the "brain-machine interface" domain. However, current electrodes for recording or stimulation still fail within months or even weeks. This lack of long-term reliability, mainly related to the chronic foreign body reaction, is induced, at the beginning, by insertion trauma, and then exacerbated as a result of mechanical mismatch between the electrode and the tissue during brain motion. All these inflammatory factors lead, over the time, to the encapsulation of the electrode by an insulating layer of reactive cells thus impacting the quality of the interface between the implanted device and the brain tissue. To overcome this phenomenon, both the biocompatibility of materials and processes, and the mechanical properties of the electrodes have to be considered. During this PhD, we have addressed both issues by developing a simple process to fabricate soft implantable devices fully made of parylene. The resulting flexible electrodes are fully biocompatible and more compliant with the brain tissue thus limiting the inflammatory reaction during brain motions. Once the fabrication process has been completed, our study has been focused on the device performances and stability. The use of high density micrometer electrodes with a diameter ranging from 10 to 50 µm, on one hand, provides more localized recordings and allows converting a series of electrophysiological signals into, for instance, a movement command. On the other hand, as the electrode dimensions decrease, the impedance increases affecting the quality of signal recordings. Here, an organic conductive polymer, the poly(3,4-ethylenedioxythiophene), PEDOT, has been used to improve the recording characteristics of small electrodes. PEDOT was deposited on electrode surfaces by elec- trochemical deposition with a high reproducibility. Homogeneous coatings with a high electrical conductivity were obtained using various electrochemical routes. Thanks to the increase of the surface to volume ratio provided by the PEDOT coating, a significant lowering of the electrode impedance (up to 3 orders of magnitude) has been obtained over a wide range of frequencies. Thermal accelerated ageing tests were also performed without any significant impact on the electrical properties demonstrating the stability of the PEDOT coatings over several months. The resulting devices, made of parylene with a PEDOT coating on the active surface of electrodes, have been tested in vitro and in vivo in mice brain. An improved signal to noise ratio during neural recording has been measured in comparison to results obtained with commercially available electrodes. In conclusion, the technology described here, combining long-term stability and low impedance, make these implantable electrodes suitable candidates for the development of chronic neural interfaces. Résumé Microélectrodes implantables souples à surface nanostructurée pour la stimulation et l’enregistrement de l’activité cérébrale Les prothèses neuronales implantables offrent de nos jours une réelle opportunité pour restaurer des fonctions perdues par des patients atteints de lésions cérébrales ou de la moelle épinière, en associant un canal non-musculaire au cerveau ce qui permet la connexion de machines au système nerveux. La fiabilité sur le long terme de ces dis- positifs, se présentant sous la forme d’électrodes implantables, est un facteur crucial pour envisager des applications dans le domaine des interfaces cerveau- machine. Cependant, les électrodes actuelles pour l’enregistrement et la stimulation se détériorent en quelques mois voire quelques semaines. Ce défaut de fiabilité sur le long terme, principalement lié à une réaction chronique con- tre un corps étranger, est induit au départ par le traumatisme consécutif à l’insertion du dispositif et s’aggrave ensuite, durant les mouvements du cerveau, à cause des propriétés mécaniques inadaptées de l’électrode par rapport à celles du tissu. Au cours du temps, l’ensemble de ces facteurs inflammatoires conduit à l’encapsulation de l’électrode par une couche isolante de cellules réactives détériorant ainsi la qualité de l’interface entre le dispositif implanté et le tissu cérébral. Pour s’affranchir de ce phénomène, la biocompatibilité des matériaux et des procédés, ainsi que les propriètés mécaniques de l’électrode doivent être pris en consid- ération. Durant cette thèse, nous avons abordé la question en développant un procédé de fabrication simple pour réaliser des dispositifs implantables souples en parylène. Les électrodes flexibles ainsi obtenues sont totalement biocompatibles et leur compliance est adaptée à celle du tissu cérébral ce qui limite fortement la réaction inflammatoire occasion- née par les mouvements du cerveau. Après avoir optimisé le procédé de fabrication, nous avons focalisé notre étude sur les performances du dispositif et sa stabilité. L’utilisation d’une grande densité d’électrodes mi- crométriques, avec un diamètre de 10 à 50 µm, permet de localiser les zones d’enregistrement en rendant possible, par exemple, la conversion d’un ensemble de signaux électrophysi- ologiques en une commande de mouvement. En contrepartie, la réduction de la taille des élec- trodes conduit à une augmentation de l’impédance ce qui dégrade la qualité d’enregistrement des signaux. Ici, un polymère conducteur organique, le poly(3,4-ethylenedioxythiophene), PEDOT, a été utilisé pour améliorer les caractéristiques électriques d’enregistrement d’électrodes de petites dimensions. Le PEDOT a été déposé sur la surface des élec- trodes par électrochimie avec une grande reproductibilité. Des dépôts homogènes avec des conductivités électriques très élevées ont été obtenus en utilisant différents procédés élec- trochimiques. Grâce à l’augmentation du rapport surface/volume induit par la présence de la couche de PEDOT, une diminution significative de l’impédance de l’électrode (jusqu’à 3 ordres de grandeur) a été obtenue sur une large plage de fréquences. De tests de vieillissement thermique accéléré ont également été effectués sans influence notable sur les propriétés électriques démontrant ainsi la stabilité de la couche de PEDOT durant plusieurs mois. Les dispositifs ainsi obtenus, fabriqués en parylène avec un dépôt de PEDOT sur la surface active des èlectrodes, ont été testés in vitro et in vivo sur des cerveaux de souris. Un meilleur rapport signal sur bruit a été mesuré durant des enregistrements neu- ronaux en comparaison avec des résultats obtenus avec des électrodes commerciales. En conclusion, la technologie décrite ici, associant stabilité sur le long terme et faible impédance, a permis d’obtenir des électrodes implantables parfaitement adaptées pour le développement d’interfaces neuronales chroniques. Thank
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