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Studies of Intracortical Microelectrode Array STUDIES OF INTRACORTICAL MICROELECTRODE ARRAY PERFORMANCE AND FOREIGN BODY RESPONSE IN YOUNG AND AGED RATS by Nicholas Fredrick Nolta A dissertation submitted to the faculty of The University of Utah in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Bioengineering The University of Utah December 2016 Copyright © Nicholas Fredrick Nolta 2016 All Rights Reserved The University of Utah Graduate School STATEMENT OF THESIS APPROVAL The thesis of Nicholas Fredrick Nolta has been approved by the following supervisory committee members: Patrick A. Tresco , Chair 12/1/2015 Date Approved Alan Dale Dorval II , Member 12/1/2015 Date Approved David W. Grainger , Member 11/17/2015 Date Approved Robert W. Hitchcock , Member 12/1/2015 Date Approved Florian Solzbacher , Member 12/4/2015 Date Approved and by Patrick A. Tresco , Chair/Dean of the Department/College/School of Bioengineering and by David B. Kieda, Dean of The Graduate School. ABSTRACT Intracortical microelectrode arrays create a direct interface between the brain and external devices. This “brain-machine interface” has found clinical application by allowing patients with tetraplegia to control computer cursors and robotic limbs. Unfortunately, use of intracortical microelectrode array technology is currently limited by its inconsistent ability to record neural signals over time. It is widely believed that the foreign body response (FBR) contributes to recording inconsistency. Most characterizations of the FBR to intracortical microelectrodes have been in the rat using devices with simple architecture, while the only device currently used in humans, the Utah Electrode Array (UEA), is much larger and more complex. In this work, we characterized the FBR to the UEA and found that, unlike with simpler devices, implantation of a UEA results in extensive vascular injury and loss of cortical tissue. We also sought to determine which features of the FBR correlated with recording inconsistency and found that biomarkers of astrogliosis, blood-brain barrier leakage, and tissue loss were associated with decreased recording performance. Next, since a significant portion of potential brain- machine interface recipients are aged, we applied similar methods in an aged cohort of rats in order to understand the effect of aging on the FBR and recording performance. We found that, surprisingly, recording performance was superior in the aged cohort. Astrogliosis was again associated with decreased recording performance in the aged cohort. Finally, we continued our development and validation of a finite element model of cytokine diffusion to assist in designing next-generation devices with a reduced FBR. Taken as a whole, this work provides meaningful insights into the mechanisms of inconsistent recording performance and discusses several promising avenues for overcoming them. iv TABLE OF CONTENTS ABSTRACT ....................................................................................................................... iii LIST OF FIGURES ......................................................................................................... viii LIST OF TABLES ...............................................................................................................x LIST OF ABBREVIATIONS ............................................................................................ xi ACKNOWLEDGEMENTS ............................................................................................. xiv Chapters 1. INTRODUCTION .........................................................................................................1 1.1 Clinical Populations ...........................................................................................1 1.2 Brain-Machine Interfaces ...................................................................................3 1.3 Intracortical Microelectrode Arrays ...................................................................5 1.4 Recording Inconsistency ....................................................................................7 1.5 Mechanisms of Recording Inconsistency ........................................................10 1.6 The Foreign Body Response ............................................................................11 1.7 The FBR to Intracortical Microelectrodes .......................................................13 1.8 Relationships between the FBR and Recording Performance .........................17 1.9 Aging and the FBR ..........................................................................................23 1.10 Strategies to Reduce the FBR to Intracortical Microelectrodes.....................27 1.10.1 The Effect of Materials ........................................................................27 1.10.2 The Effect of Coatings ........................................................................28 1.10.3 The Effect of Systemically-Administered Drugs ................................30 1.10.4 The Effect of Local Drug Delivery .....................................................32 1.10.5 The Effect of Device Architecture ......................................................34 1.10.6 The Effect of Mechanical Motion .......................................................35 1.10.7 The Effect of Device Type ..................................................................38 1.11 Finite Element Modeling to Predict the FBR ................................................39 2. BBB LEAKAGE, ASTROGLIOSIS, AND TISSUE LOSS CORRELATE WITH SILICON MICROELECTRODE ARRAY RECORDING PERFORMANCE ..........41 2.1 Abstract ............................................................................................................41 2.2 Introduction ......................................................................................................42 2.3 Materials and Methods .....................................................................................45 2.3.1 Microelectrodes .....................................................................................45 2.3.2 Animal Surgery .....................................................................................46 2.3.3 Electrophysiological Recordings ...........................................................47 2.3.4 Failure Analysis .....................................................................................47 2.3.5 Euthanasia and Tissue Preparation ........................................................48 2.3.6 Immunohistochemistry and Microscopy ...............................................48 2.3.7 Determination of Void Volume .............................................................49 2.3.8 Statistics .................................................................................................50 2.4 Results ..............................................................................................................50 2.4.1 Failure Analysis .....................................................................................50 2.4.2 Electrophysiology ..................................................................................52 2.4.3 Explanted Arrays ...................................................................................53 2.4.4 Histological Description of the FBR .....................................................53 2.4.5 Stab Wound Injuries ..............................................................................57 2.4.6 Relationships between Recording Performance and Histology ............60 2.5 Discussion ........................................................................................................61 2.6 Conclusions ......................................................................................................67 3. ADVANCED AGE IS NOT A BARRIER TO CHRONIC INTRACORTICAL SINGLE UNIT RECORDING IN RATS ....................................................................69 3.1 Abstract ............................................................................................................69 3.2 Introduction ......................................................................................................70 3.3 Materials and Methods .....................................................................................74 3.3.1 Microelectrodes .....................................................................................74 3.3.2 Animal Surgery .....................................................................................75 3.3.3 Electrophysiological Recordings ...........................................................76 3.3.4 Failure Analysis .....................................................................................77 3.3.5 Euthanasia and Tissue Preparation ........................................................77 3.3.6 Immunohistochemistry and Microscopy ...............................................78 3.3.7 Measurement of Lesion Cavity Volume ...............................................79 3.3.8 Image Quantification .............................................................................79 3.3.9 Statistics .................................................................................................80 3.4 Results ..............................................................................................................80 3.4.1 Aged Rat Model ....................................................................................80 3.4.2 Failure Analysis .....................................................................................80
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