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A New Electrode Technology for Neuro-Robotic Interfaces Alik Sunil Widge CMU-RI-TR-07-03

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A New Electrode Technology for Neuro-Robotic Interfaces Alik Sunil Widge CMU-RI-TR-07-03 Self-Assembled Monolayers of Polythiophene “Molecular Wires”: A New Electrode Technology for Neuro-Robotic Interfaces Alik Sunil Widge CMU-RI-TR-07-03 Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Robotics The Robotics Institute and Center for the Neural Basis of Cognition Carnegie Mellon University Pittsburgh, Pennsylvania 15213 January 3rd, 2007 Dr. Yoky Matsuoka, Thesis Committee Chair Dr. Kaigham Gabriel, Co-advisor Dr. Xinyan ”Tracy” Cui, University of Pittsburgh (external) Dr. Carl Lagenaur, University of Pittsburgh (external) Dr. Lee Weiss Copyright 2007 by Alik Widge. All rights reserved. Alik Sunil Widge Self-Assembled Monolayers of Polythiophene “Molecular Wires”: A New Electrode Technology for Neuro-Robotic Interfaces Abstract This thesis presents the proof of concept of a new type of electrode for inter- faces between living nervous systems and electronic devices (“neuro-robotic interfaces”). Such interfaces have long been pursued due to their high clin- ical and scientific value. However, progress has been hindered by inade- quate performance of the implanted electrodes that bridge biological, ion- based electricity and analog/digital electronics. These electrodes provoke inflammatory reactions in surrounding tissue and often cause detrimental effects when stimulating neurons to deliver information. The most promis- ing approach to improving electrode biocompatibility involves electrically polymerizing conductive polymers with biomolecules on metal electrodes. These coatings improve mechanical biocompatibility, attract neurons to the electrode, and lower electrode impedance. They are nevertheless limited by delamination of polymer from the electrode and inability to pattern or con- trol the composition of the polymer/biomolecule blend. The new electrode technology described herein addresses those limitations through two innovations: the use of self-assembled monolayer (SAM) tech- nology to bind polythiophene conductive polymers to metal electrodes, and the design of lipophilic polythiophenes (“molecular wires”) that can in- sert into a cell membrane and provide stable intracellular electrical access. Thiol-based SAMs should increase coating robustness and will permit better controllability and patterning, while still offering the same biocompatibility as electropolymerized coatings. Intracellular access that does not kill the target neuron will permit gentler and more specific stimulation and higher fidelity recording. Polythiophene SAMs are thinner than electrodeposited polymer films, and thus do not decrease impedance to the same degree, but should be able to compensate for this by allowing intracellular stimulation. Data from atomic force microscopy, cell culture, and impedance spec- troscopy are combined to show that functionalized polythiophenes can form SAMs and that these SAMs have the appropriate biological and elec- trical activity for a neuro-robotic interface electrode. The feasibility of polymer-based intracellular electrophysiology is demonstrated through ar- tificial lipid bilayer experiments and atomistic molecular dynamics simu- lations of the membrane-polymer interface. Taken together, these studies constitute proof of concept for the “molecular wire” SAM electrode and represent the first steps towards development and deployment of this new interface technology. 2 Acknowledgements All science is ultimately a collaborative effort, but this thesis in particular has depended on a small army of collaborators, assistants, friends, mentors, and fellow travelers. Naming them all would take a section that dwarfs the remainder of the document, so I will instead begin by apologizing to all those not named, either due to space limitations or the imperfections of human memory. The list of thanks is headed by my advisors, Drs. Yoky Matsuoka and Ken Gabriel, for being supportive of the direction I chose and for assisting me in making the connections necessary to access the appropriate materials and equipment. Credit is also due to the Robotics Institute as a whole, for encouraging interdisciplinary research that ranges into fields far removed from traditional robotics, and for taking better care of its students than any other graduate department I have ever encountered. Beyond that general gratitude, I must acknowledge that the majority of my work was conducted in other investigators’ laboratories, and without their generous donations of equipment, materials, and advice, none of this could have been done. Dr. Victor Weedn, formerly of Carnegie Mellon, provided the seed ideas that led to this project and arranged for laboratory space within the Molec- ular Biotechnology & Imaging Center. Dr. Malika Jeffries-El, also formerly of Carnegie Mellon and now at the University of Iowa, synthesized or supervised the synthesis of all the polymers used in these experiments, devoting a substantial percentage of her effort over four years with minimal rec- ompense. The atomic force microscopy of Chapter 4 and the thermal evaporations of Chapters 4-6 all used equipment in the laboratory of Dr. James Schneider of Carnegie Mellon. Dr. Schneider also provided critical advice on experimental approaches and interpretation of the results. Every- thing I know about neuronal cell culture, and certainly everything presented in Chapter 5, is due to instruction and guidance from Dr. Carl Lagenaur of the University of Pittsburgh, who also made his laboratory available for that work. Similarly, my knowledge of impedance spectroscopy and understanding of electrochemistry is largely due to Dr. Xinyan “Tracy” Cui, also of the University of Pittsburgh, who provided the equipment and software used in the experiments of Chapter 6. The artificial lipid bilayer work of Chapter 7 arose from discussions with Dr. Schneider and was per- formed at the National Institute of Standards and Technology, using the equipment and voluminous technical assistance of Drs. John Kasianowicz and Martin Misakian. In Dr. Kasianowicz’s case, this generosity extended to opening his own home to me as a place to stay while the experiments were underway. The results of the bilayer experiments would be of greatly reduced significance if not for the accompanying molecular dynamics simulations described in Chapters 8 and 9. These relied on expert guidance from Dr. Maria Kurnikova of Carnegie Mellon, as well as tens of thousands of hours of computer time using her personal resources and her grant allocations from the Pittsburgh Super- computing Center. Finally, credit is due to several undergraduate research assistants who mastered toxic chemicals, designed new equipment, researched new techniques, and traveled across the length and breadth of Pittsburgh to move this work forward. Chief among these are Kelly Collins, Ololade Olakanmi, Megan Tzeng, and Mengyao “Mona” Zhe. Work such as this involves many experimental and logistical barriers, and I faced many periods of deep frustration. In these times, I was lucky enough to have colleagues and organizations who helped me to vent that frustration, channel it into positive advocacy for my fellow students and future patients, and to grow as a person and a leader along the way. Again, with my deepest apologies to all those who are not listed here, I would like to single out a few from that multitude: 3 • The representatives and leaders of the Carnegie Mellon Graduate Student Assembly, especially Matt Cronin, Brian Fifarek, Kim Murday, Rob Reeder, and Miriam Rosenberg-Lee. Without their early support and mentorship, much of the rest of this list would not have happened. • The National Association of Graduate-Professional Students, and particularly Doris Dirks, Jim Masterson, and Serge Egelman. Although my work with NAGPS introduced me to only a small part of the Federal legislative process, I came away with a new understanding of the interaction between science, education, and politics. • The American Medical Association and its Medical Student Section, where, through the as- sistance of many patient and tolerant friends and mentors, I managed to polish away some of my rougher edges and learn to be a more effective leader. My year as AMA-MSS Chair unquestionably slowed my scientific progress, but has left me with skills and friendships that will affect my career for decades. Special thanks are due to Adam Gordon, Parag Parekh, Sadeq Quraishi, and David Winchester for their guidance, and to Anne Christensen, Chris DeRienzo, Ben Galper, Michael Katz, Brad Lancaster, Steve Sherick, Heather Smith, and Hannah Zimmerman for working and fighting by my side throughout these five years. • Mary Moore and Suzanne Lyons Muth, two Carnegie Mellon staff whose doors were always open and whose desks were always stocked with candy when I needed administrative assistance, advice, or simply someone to talk to. Without professionals like Suzanne and Mary, the Robotics Institute would grind to a halt in short order. • My colleagues in the Medical Scientist Training Program, especially Pedram Afshar, Lou Ghanem, Audrey Lau, Rod Tan, and Ron Trible. Their advice, fellowship, and trailblazing has helped me clear many administrative barriers and reminded me that even M.D./Ph.D. training does eventually end. The financial support for this work is as heterogeneous as the technical and moral support. My tuition and stipend were funded in the first year by the Center for the Neural Basis of Cognition (NIH institutional training grant T32 N507433-03), in years two through four by a National Defense Science & Engineering Fellowship
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