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Effects of Deep Brain Stimulation on Speech in Patients with Parkinson’S Disease and Dystonia

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Effects of Deep Brain Stimulation on Speech in Patients with Parkinson’S Disease and Dystonia Effects of deep brain stimulation on speech in patients with Parkinson’s disease and dystonia. Elina Tripoliti Thesis submitted for the degree of PhD in Neurological studies Institute of Neurology University College London October 2010 1 I, Elina Tripoliti, confirm that the work presented in this thesis is my own. Where information has been derived form other sources, I confirm that this has been indicated in the thesis. 2 Abstract Disorders affecting the basal ganglia can have a severe effect on speech motor control. The effect can vary depending on the pathophysiology of the basal ganglia disease but in general terms it can be classified as hypokinetic or hyperkinetic dysarthria. Despite the role of basal ganglia on speech, there is a marked discrepancy between the effect of medical and surgical treatments on limb and speech motor control. This is compounded by the complex nature of speech and communication in general, and the lack of animal models of speech motor control. The emergence of deep brain stimulation of basal ganglia structures gives us the opportunity to record systematically the effects on speech and attempt some assumptions on the role of basal ganglia on speech motor control. The aim of the present work was to examine the impact of bilateral subthalamic nucleus deep brain stimulation (STN-DBS) for Parkinson’s disease (PD) and globus pallidus internus (GPi-DBS) for dystonia on speech motor control. A consecutive series of PD and dystonia patients who underwent DBS was evaluated. Patients were studied in a prospective longitudinal manner with both clinical assessment of their speech intelligibility and acoustical analysis of their speech. The role of pre-operative clinical factors and electrical parameters of stimulation, mainly electrode positioning and voltage amplitude was systematically examined. In addition, for selected patients, tongue movements were studied using electropalatography. Aerodynamic aspects of speech were also studied. The impact of speech therapy was assessed in a subgroup of patients. The clinical evaluation of speech intelligibility one and three years post STN-DBS in PD patients showed a deterioration of speech, partly related to medially placed electrodes and high amplitude of stimulation. Pre-operative predictive factors included low speech intelligibility before surgery and longer disease duration. Articulation rather 3 than voice was most frequently affected with a distinct dysarthria type emerging, mainly hyperkinetic-dystonic, rather than hypokinetic. Traditionally effective therapy for PD dysarthria had little to no benefit following STN-DBS. Speech following GPi-DBS for dystonia did not significantly change after one year of stimulation. A subgroup of patients showed hypokinetic features, mainly reduced voice volume and fast rate of speech more typical of Parkinsonian speech. Speech changes in both STN-DBS and GPi-DBS were apparent after six months of stimulation. This progressive deterioration of speech and the critical role of the electrical parameters of stimulation suggest a long-term effect of electrical stimulation of basal ganglia on speech motor control. 4 Acknowledgements My heartfelt and warmest thanks go to my supervisor Dr Patricia Limousin. Without her steadfast support and trust this work would not have been completed. I have benefited enormously by her experience, knowledge, clarity of thought, and above all her true care for the patients. I am equally thankful to Professor Marwan Hariz, whose constant encouragement, inspiration and integral, meticulous approach have set the highest clinical and research standards. This study is the result of teamwork. I’m gratefully indebted to Mr Ludvic Zrinzo for his practical help, enthusiasm and confident dynamism, to Dr Tom Foltynie for his organised and persistent approach to data analysis, Mr Joseph Candelario and Ms Ellie Borrell, Dr Irene Martinez-Torres and Dr Iciar Aviles, to Dr Diane Ruge for our discussions, to Dr Stephen Tisch and to Professor Marjan Jahanshahi. I would also like to thank Professor John Rothwell and Dr Serge Pinto who supported the study at the very beginning; Sue McGowan and the Speech & Language Therapy Team at the National Hospital for our friendship and encouragement; Ms Laura Strong, Ms Eleanor Frost and Ms Freya Hickey for all the hours of listening to recorded speech they provided. I was also very fortunate to work with Mr Michael Roughton, Senior Statistician at UCL, who supported me with positive and clear advice on the data analysis. I owe a lot to my husband Mark who made it all possible with his strong belief, his persistence, his sense of humour and the joy of our conversations. I also owe a lot to my late grandmother Stamatia who first impressed on me the value of “logos” – the Greek word for both speech and nous. 5 Most of all I would like to thank the patients who took part in this study over the last six years. I hope this is the beginning and that one day someone will be able to resolve the mystery of speech and electrical stimulation of deep brain structures. 6 Table of contents ACKNOWLEDGEMENTS ....................................................................................................................... 5 LIST OF TABLES ................................................................................................................................... 13 ABBREVIATIONS .................................................................................................................................. 14 PUBLICATIONS ..................................................................................................................................... 16 CHAPTER 1: INTRODUCTION ........................................................................................................... 19 1.1 BASAL GANGLIA STRUCTURE AND FUNCTION ................................................................................... 19 1.1.1 Anatomy ................................................................................................................................... 19 1.1.2 Neuronal morphology .............................................................................................................. 21 1.1.3 Dopaminergic control .............................................................................................................. 25 1.1.4 Connectivity and functional organisation ................................................................................ 26 1.2 SPEECH MOTOR CONTROL IN HEALTHY ADULTS AND THE ROLE OF BASAL GANGLIA ........................ 31 1.2.1 Imaging data ............................................................................................................................ 32 1.2.2 Neural control of human vocalisation ..................................................................................... 37 1.2.3 Neural control of facial muscles .............................................................................................. 42 1.3 MUSCLE CONTROL FOR SPEECH ........................................................................................................ 43 1.3.1 Laryngeal muscles involved in the production of speech, swallowing, respiration and cough 44 1.3.2 Lingual and palatal muscles .................................................................................................... 47 1.4 PERCEPTUAL AND ACOUSTICAL CHARACTERISTICS OF SPEECH IN PARKINSON’S DISEASE ................ 48 1.4.1 Respiration ............................................................................................................................... 50 1.4.2 Phonation................................................................................................................................. 56 1.4.3 Articulation and resonance ...................................................................................................... 63 1.4.4 Speech intelligibility and people with PD ................................................................................ 67 1.4.5 Prosody .................................................................................................................................... 73 1.4.6 Correlation of speech with motor symptoms............................................................................ 77 1.4.7 Patient perceptions and complaints ......................................................................................... 79 1.4.8 Neural control of speech in Parkinson’s disease ..................................................................... 81 1.4.9 Effects of medication on speech in PD .................................................................................... 84 1.4.10 Effects of deep brain stimulation on speech in PD ................................................................ 87 1.5 DYSTONIA ........................................................................................................................................ 96 1.5.1 Definition and classification .................................................................................................... 97 1.5.2 Pathophysiology of dystonia and implications for speech ....................................................... 98 1.5 3 Speech disorders associated with primary and secondary dystonia ...................................... 100 1.5.4 Examination findings ............................................................................................................. 103 1.5.5 Treatment of communication disorders in
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