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Theoretical and Experimental Predictions of Neural Elements

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Theoretical and Experimental Predictions of Neural Elements THEORETICAL AND EXPERIMENTAL PREDICTIONS OF NEURAL ELEMENTS ACTIVATED BY DEEP BRAIN STIMULATION by SVJETLANA MIOCINOVIC Submitted in partial fulfillment of the requirements For the degree of Doctor of Philosophy Dissertation Adviser: Dr. Cameron McIntyre Department of Biomedical Engineering CASE WESTERN RESERVE UNIVERSITY August, 2007 CASE WESTERN RESERVE UNIVERSITY SCHOOL OF GRADUATE STUDIES We hereby approve the dissertation of SVJETLANA MIOCINOVIC candidate for the PhD degree*. (signed) Dominique Durand (chair of the committee) Ruth Siegel Ken Gustafson Jerrold Vitek Cameron McIntyre (date) 5/23/2007 * We also certify that written approval has been obtained for any proprietary material contained therein. Dedicated to my parents Posvećeno mojim roditeljima TABLE OF CONTENTS List of Tables ………………………………………………………………………….….2 List of Figures ……………………………………………………………………………..3 List of Abbreviations ……………………………………………………………………..5 Acknowledgements ……………………………………………………………………….7 Abstract …………………………………………………………………………………...9 Chapter 1: Introduction, background and project significance ………………………….11 Chapter 2: Software system for stereotactic neurosurgical navigation in non-human primates (Cicerone)………….………………..….….….……………..…………40 Chapter 3: Spatial and temporal characteristics of voltage field generated by deep brain stimulation electrode …………………….………….……………..………65 Chapter 4: Computational analysis of subthalamic nucleus and lenticular fasciculus activation during therapeutic deep brain stimulation ……….……..…………….90 Chapter 5: Summary and future directions ….………………...….…………...….……124 Bibliography ……………………………………………………………………...……136 Appendix A: Cicerone user manual….…………………...….…………………………147 1 LIST OF TABLES 3-1. Parameters optimized for modeling DBS-induced voltage fields in saline and subcortical gray matter – static model 3-2. Parameters optimized for modeling DBS-induced voltage fields in saline and subcortical gray matter – Fourier model 2 LIST OF FIGURES 1-1. Deep brain stimulation 1-2. Simplified circuit diagram of the basal ganglia 1-3. DBS in a parkinsonian monkey 1-4. Neural environment in the subthalamic region 1-5. Spread of direct stimulation effects in a PD patient 2-1. Cicerone display and graphical user interface 2-2. Microelectrode recording data and Cicerone atlas 2-3. Cicerone atlas accuracy 3-1. In vitro voltage field recordings 3-2. Surgical planning and electrode implantation 3-3. Repeated in vivo DBS voltage measurements 3-4. In vivo voltage field recordings 3-5. Effect of DBS electrode impedance on recorded voltage 3-6. Stimulation waveforms from in vivo and in vitro recordings and corresponding model solutions 4-1. Three-dimensional reconstruction of the basal ganglia 4-2. Multicompartment cable model of an STN projection neuron 4-3. Neural populations and DBS electrode in the context of 3D neuroanatomy 4-4. Field-neuron model of STN DBS 4-5. STN neuron firing in response to extracellular stimulation 4-6. Neural activation during clinically effective and ineffective DBS 3 4-7. Experimentally recorded GPi firing during STN DBS 4-8. Sensitivity of neural activation to electrode position 4-9. STN firing frequency under the influence of stimulation-induced trans-synaptic GABAa inhibitory inputs 4 LIST OF ABBREVIATIONS 2D two-dimensional 3D three-dimensional AC anterior commissure AL ansa lenticularis AP anterior-posterior CST corticospinal tract CT computed tomography DBS deep brain stimulation EP entopeduncular nucleus FEM finite element model fMRI functional magnetic resonance imaging GABA gamma aminobutyric acid GP globus pallidus GPe globus pallidus externus GPi globus pallidus internus HFS high frequency stimulation IPG implantable pulse generator L-dopa levodopa LF lenticular fasciculus MER microelectrode recording ML medio-lateral 5 MPTP 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine MRI magnetic resonance imaging PC posterior commissure PD Parkinson's disease PET positron emission tomography SNc substantia nigra pars compacta SNr substantia nigra pars reticulata STN subthalamic nucleus STN DBS subthalamic deep brain stimulation STN HFS subthalamic high frequency stimulation VD ventral-dorsal VTA volume of tissue activated VTK Visualization Toolkit ZI zona incerta 6 ACKNOWLEDGEMENTS I would first like to thank my advisor Dr. Cameron McIntyre. Cameron has been an incredible source of support and guidance during my four years in his lab. He was always able to put things into perspective and make me see what is truly important. He was also always very encouraging of my professional development and sensitive to my educational goals in the Medical Scientist Training Program. Next, I would like to express gratitude to Dr. Jerry Vitek and his lab, who have accepted me as one of their own. My biggest thanks goes to Dr. Gary Russo who has taught me most of what I know about monkey electrophysiology. Drs. Weidong Xu and Jianyu Zhang were always there to help and share their vast knowledge of experimental techniques. Jennie Minnich was an incredibly dedicated and capable lab manager. Her predecessor Karen Zingale was always helpful as well, as were the wonderful people in Biological Resources Unit who took care of the animals. A big thanks goes to the members of my own lab. Scott Lempka was incredibly patient and helped me do most of the experiments described in Chapter 3. Chris Butson provided a lot of guidance in the modeling phase of the project. Angela Noecker offered advice and technical assistance during Cicerone software development. Phil Hahn, Matt Johnson, Chris Maks, and Luis Lujan contributed to the success of the project as well. Everybody’s generosity and enthusiasm made our lab a wonderful and inspiring environment to work in. My graduate school research experience started in the lab of Dr. Warren Grill who introduced me to the exciting field of neural engineering. I thank Dr. Grill for the early support and encouragement that set me on this path. 7 I would also like to thank Drs. Dominique Durand, Jerry Vitek, Ruth Siegel and Ken Gustafson for having served on my thesis committee. This research was financially supported by the National Institutes of Health (RO1 NS-47388, RO1 NS-37019, and T32 GM07250) 8 Theoretical and Experimental Predictions of Neural Elements Activated by Deep Brain Stimulation Abstract by SVJETLANA MIOCINOVIC Chronic electrical stimulation of the brain, known as the deep brain stimulation (DBS), has become the preferred surgical treatment for advanced Parkinson’s disease. Despite its clinical success the mechanisms of DBS are still unknown and there is limited understanding of the neural response to DBS. As a result the therapeutic neural target has not been clearly identified, which limits opportunities to improve the technology and increase treatment efficacy. We hypothesized that subthalamic (STN) projection neurons are primarily activated during clinically effective STN DBS. Non-human primate models of DBS provide unique opportunities to study the therapeutic mechanisms of DBS in vivo. The therapeutic benefits of DBS are dependent on accurate placement of the electrode in the appropriate neuroanatomical target. Stereotactic neurosurgical navigation systems that exist for clinical applications are lacking in the area of non-human primate research. Therefore, we developed a software system (Cicerone) for stereotactic neurosurgical planning, neurophysiological data collection, and DBS visualization in primates. Computational volume conductor models are commonly used to estimate neuronal response to electrical stimulation. To date there has been no direct validation of 9 models aimed at investigating stimulation of subcortical structures. We have therefore measured voltages generated by DBS electrode in the thalamus of a monkey. Furthermore, we have calculated model parameters that can be used to accurately capture both spatial and temporal properties of voltage fields induced by DBS. Utilizing the stereotactic navigation system and voltage field model we built a comprehensive computational model of STN DBS in the parkinsonian monkey. We compared our model predictions with results from experimental animals to quantify the relative activation of STN neurons and pallidothalamic (GPi) fibers during therapeutic DBS. The results indicate that activation of nearly half of the STN neurons is sufficient for the behavioral manifestation of the therapeutic effects, which confirms our hypothesis. The additional recruitment of GPi fibers of passage may also play an important role in therapeutic outcome, but large-scale activation of GPi fibers is not necessary. The position of the electrode in the STN region and the choice of active contact can strongly effect recruitment of either neural population. 10 Chapter 1: Introduction, background and project significance 1.1 Deep brain stimulation in treatment of Parkinson’s disease Deep brain stimulation (DBS) has become a preferred surgical therapy in the treatment of movement disorders (Benabid et al., 1996; Obeso et al., 2001) and it is being investigated as a treatment for epilepsy (Hodaie et al., 2002), obsessive-compulsive disorder (Gabriels et al., 2003) and depression (Mayberg et al., 2005). It has been particularly successful for patients in the late stages of Parkinson’s disease (PD) when medications are no longer sufficient to alleviate the disease symptoms. Tremor, rigidity and bradykinesia (slowness of movement) are the main manifestations of PD and initially the drug levodopa can ameliorate most symptoms. However after 5-10 years of levodopa
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