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Development of a Neuromodulation-Based Therapy for the Rehabilitation of Patients with SCI

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Development of a Neuromodulation-Based Therapy for the Rehabilitation of Patients with SCI UNIVERSIDAD DE CASTILLA LA MANCHA Escuela Internacional de Doctorado Development of a neuromodulation-based therapy for the rehabilitation of patients with SCI by Stefano Piazza A thesis submitted in the fulfillment for the degree of Doctor of Philosophy. Directors Dr. José Luis Pons Dr. Julio Gómez Soriano November 2016 i Acknowledgements A Iris, per essere sempre al mio lato, per supportarmi e incoraggiarmi, consigliarmi ed aiutarmi. Per l’energia e l’allegria, il coraggio e la passione. Perché hai aggiunto groove alla mia vita, e da allora non abbiamo piú smesso di ballare. A Mattia, che durante questa tesi sei passato da nano a gigante, per la tua simpatia e irriverenza, per le burle e per le sfide. Mi hai insegnato a non prendermi troppo sul serio ed a vedere tutte le cose con la giusta prospettiva. Ai miei genitori, sempre presenti in questi anni, avete creduto in me fin dal primo momento e non avete mai smesso di appoggiarmi. Grazie per il vostro conforto, la vostra pazienza, e per l’entusiasmo con cui avete colto ogni piccolo passo che mi avvicinava un po’ di piú a questo traguardo. Ed a Tommy, che appoggiato su una spalla non mi perde mai di vista. Alla famiglia spagnola, per accogliermi con calore, sfamarmi in svariate occasioni ed incoraggiare fin da subito tutti i nostri progetti. Ai molti buoni amici, fonte costante di gioia ed evasione, per tutti i bei momenti passati insieme, per essere sempre pronti a rallegrarmi e stimolarmi in tutti questi anni. Credo che una buona parte della mia salute mentale la debba anche a voi. Alle persone che maggiormente hanno contribuito alla direzione di questa tesi: Julio e Julian, per aver creduto in questa ricerca fin dal primo momento ed aver lavorato alacramente per realizzarla, e José Luis, per il supporto economico e istituzionale, e per garantirmi la libertá e i mezzi per portare avanti questo progetto. A tutti i volontari ed i pazienti, che hanno deciso di dedicare parte del loro tempo a questi studi. A voi, e a tutti quelli che meriterebbero di essere citati in queste poche righe, grazie di cuore. Stefano iii Abstract Spinal cord injury (SCI) refers to a damage to the spinal cord that affects sensory, motor, or autonomic functions, with a huge impact on the patient and on the society. Locomotion is one of the more frequently affected functions after SCI, and therefore his recovery is a high priority for these subjects. Upstanding locomotor training exercises are commonly performed to rehabilitate locomotion: this effect is attributed to the repetitive stimulation of specific motor pathways in combination with the reception of an appropriate sensory feedback, which helps to restore proper sensorimotor integration - the coupling between the sensory and motor systems. Unfortunately, these therapies are tiring for the patient and demanding for the therapists. Furthermore, they cannot be performed in the first period after the injury, a period of fundamental importance for maximising rehabilitation outcomes. On the contrary, leg-cycling is a commonly recommended exercise that activates similar control networks as locomotion and suitable to be performed early after the lesion or by the most impaired subjects. However, during leg-cycling, the afferent feedback produced by load receptors and plantar cutaneous mechanoreceptors is limited. In this thesis, we consider the opportunity to combine leg-cycling with the delivery of plantar electrical stimulation that would increase sensory system recruitment. To this account, we compared the effects of single-bout sessions of cycling and cycling with electrical stimulation, applied to non- injured subjects and subjects with iSCI. To estimate the early effects of the therapy, we developed a test of spinal sensorimotor integration, based on the assessment of soleus H-reflex excitability following a conditioning electrical stimulation delivered to the ipsilateral plantar surface of the subject. Lastly, we propose a procedure, based on this assessment technique and on the leg cycling exercise, to perform a deeper examination of spinal sensorimotor integration in subjects with SCI. v Table of Contents Page List of Tables ix List of Figures xi Acronyms xiii Structure of the document xv 1 Introduction 1 1.1 Anatomy and Function of the Spinal Cord . 1 1.2 Spinal Cord Injury . 5 1.3 Spinal Cord Plasticity . 11 1.4 Traditional approaches to rehabilitation after SCI . 14 1.5 Neurophysiological basis for motor control neuromodulation . 15 1.6 Targeted Modulation for motor recovery . 20 1.7 Targeted Modulation for restoring autonomic functions . 29 1.8 Conclusion . 33 2 Motivation 35 3 Hypotheses and Objectives 39 3.1 Hypotheses . 39 3.2 Objectives . 40 4 Methodology 41 4.1 Architecture of the experimental platform . 42 4.2 Financial and Experimental Support . 46 5 Results 51 vii Stefano Piazza 5.1 StudyI............................................... 51 5.2 Study II . 66 5.3 Study III . 78 6 Discussion 91 6.1 Limitations . 93 6.2 Futurework............................................ 94 7 Conclusions 97 Bibliography 99 Appendix 125 Contributions of the dissertation . 125 viii List of Tables TABLE Page 1.1 Three phases of SCI . 6 1.2 AIS scale . 7 4.1 Serial communication protocol of the experimental platform . 45 5.1 Study I: demographic and clinical characteristics of participants . 58 5.2 Study I: correlation between clinical characteristics and conditioned H-reflex activity . 62 5.3 Study II: demographic and clinical characteristics of participants . 74 5.4 Study III: demographic and clinical characteristics of participants . 82 ix List of Figures FIGURE Page 1.1 Anatomy and neural organization of the Spinal Cord . 2 4.1 Screenshots of the clinical interface . 44 4.2 Model of motor recovery after a neurological lesion . 47 5.1 Study I: experimental protocol . 55 5.2 Study I: representative conditioned soleus H-reflex activity . 56 5.3 Study I: analysis of conditioned soleus H-reflex activity after cycling . 60 5.4 Study I: stability of control variables before and after leg-cycling . 61 5.5 Study I: conditioned soleus H-reflex modulation at 75 ms ISI . 63 5.6 Study II: experimental protocol . 70 5.7 Study II: analysis of conditioned soleus H-reflex activity after cycling and ES-cycling . 73 5.8 Study III: description of the experimental platform for neural activity assessment . 81 5.9 Study III: experimental protocol . 85 5.10 Study III: ES-cycling effects on conditioned soleus H-reflex activity considering different impairment levels . 87 xi Acronyms AIS American spinal injury association impairment scale CNS Central nervous system CPG Central pattern generators cSCI Motor complete spinal cord injury EMG Electromyography ES Electrical stimulation ES-cycling Leg-cycling with phase-dependent plantar electrical stimulation FES Functional electrical stimulation iSCI Motor incomplete spinal cord injury ISI Inter-stimulus interval SC Spinal cord SCI Spinal cord injury WISCI Walking index for spinal cord injury xiii Structure of the document This dissertation is organised in 7 chapters and an appendix. In order to facilitate the consultation, a brief description of the content of each chapter is here presented. Chapter 1 - Introduction to Spinal Cord Injury: this chapter introduces to the reader the definition of Spinal Cord Injury (SCI) and its consequences, especially considering the socioeconomic impact and associated clinical complications. The concept of spinal cord plasticity is intro- duced, and discussed in relation to its potentials for the development of new therapies after SCI. Traditional rehabilitation techniques are presented and their effects interpreted in light of Central Nervous System (CNS) neuronal plasticity. Finally, the concept of neuromodulation is introduced, together with an overview of the principal rehabilitation methods based on it. In particular, one section is entirely dedicated to the rehabilitation of motor function, because of its special relevance in this thesis, and a second section focuses on the rehabilitation of autonomic functions, because of its high impact on the quality of life of people with SCI. Chapter 2 - Motivation: this chapter introduces the general framework that inspired this thesis and the problem addressed. Chapter 3 - Hypotheses and Objectives: this chapter formulates the hypothesis and lists the objec- tives that are behind the realisation of this thesis. Chapter 4 - Methodology: this chapter describes the methodology of the research, including the technical, scientific and logistic aspects behind the realisation of this doctoral work. First, the chapter presents the technical details of the platform that have been developed for supporting the studies discussed in this dissertation. Then, it describes the projects and organisations that provided financial and logistic support to the realisation of this thesis. Chapter 5 - Results: this chapter presents the three studies at the core of this doctoral work. The first study is dedicated to the characterization of spinal sensorimotor integration and its xv Stefano Piazza relation with motor function. Non-injured subjects and subjects with SCI took part in the experiment. In each group, spinal sensorimotor excitability was compared before and after a short leg-cycling session and clinically relevant results were obtained. The second study introduces a novel intervention, based on cycling with plantar electrical stimulation, to train spinal sensorimotor excitability in subjects with SCI. The effects of a single session of this exercise on spinal sensorimotor excitability
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