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Neck Muscle Control During Three-Dimensional Gaze

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Neck Muscle Control During Three-Dimensional Gaze NECK MUSCLE CONTROL DURING THREE-DIMENSIONAL GAZE BEHAVIOUR IN THE PRIMATE by FARSHAD FARSHADMANESH A dissertation submitted to the Faculty of Graduate Studies in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Graduate Programme in Biology York University Toronto, Ontario December 2011 Library and Archives Bibliotheque et Canada Archives Canada Published Heritage Direction du Branch Patrimoine de I'edition 395 Wellington Street 395, rue Wellington Ottawa ON K1A0N4 Ottawa ON K1A 0N4 Canada Canada Your file Votre reference ISBN: 978-0-494-88685-4 Our file Notre reference ISBN: 978-0-494-88685-4 NOTICE: AVIS: The author has granted a non­ L'auteur a accorde une licence non exclusive exclusive license allowing Library and permettant a la Bibliotheque et Archives Archives Canada to reproduce, Canada de reproduire, publier, archiver, publish, archive, preserve, conserve, sauvegarder, conserver, transmettre au public communicate to the public by par telecommunication ou par I'lnternet, preter, telecommunication or on the Internet, distribuer et vendre des theses partout dans le loan, distrbute and sell theses monde, a des fins commerciales ou autres, sur worldwide, for commercial or non­ support microforme, papier, electronique et/ou commercial purposes, in microform, autres formats. paper, electronic and/or any other formats. The author retains copyright L'auteur conserve la propriete du droit d'auteur ownership and moral rights in this et des droits moraux qui protege cette these. Ni thesis. Neither the thesis nor la these ni des extraits substantiels de celle-ci substantial extracts from it may be ne doivent etre imprimes ou autrement printed or otherwise reproduced reproduits sans son autorisation. without the author's permission. In compliance with the Canadian Conformement a la loi canadienne sur la Privacy Act some supporting forms protection de la vie privee, quelques may have been removed from this formulaires secondaires ont ete enleves de thesis. cette these. While these forms may be included Bien que ces formulaires aient inclus dans in the document page count, their la pagination, il n'y aura aucun contenu removal does not represent any loss manquant. of content from the thesis. Canada iv ABSTRACT During natural gaze behaviour, both the eye and head contribute to making a gaze shift. Compared to the oculomotor system, the head-neck system has been studied less extensively in part due to the redundancy of neck musculature. This dissertation contributes to an understanding of the neuromuscular mechanisms underlying head movement control by examining the relationships between neck muscle activation and three-dimensional (3-D) head kinematics. These are the first set of studies to employ a statistical technique known as cross-validation to examine these relationships in non- human primates. The electromyographic (EMG) activation was recorded in six bilateral neck muscle pairs: sternocleidomastoid, splenius capitis, complexus, biventer cervicis, rectus capitis posterior major and occipital capitis inferior while the animals made head- unrestrained gaze shifts. First, I compared neck EMG during torsional head postures evoked by stimulating the interstitial nucleus of Cajal (INC) to similar postures evoked by inactivation of the opposite INC. I found that, similar head postures could correspond to different patterns of muscle activation, depending on the neural origin of the activation. Second, I used cross-validation to examine neck EMG-head kinematics relationships during natural gaze behaviour. During head holding periods, neck EMG primarily contributed to position-dependent horizontal head orientation, with more complex multi-dimensional contributions emerging during the head movements. Third, during normal gaze behaviour, the relationship between neck muscle EMG and torsional head kinematics was not clear, I again used microstimulation and chemical inactivation V of the INC to induce acute head tilts and obtain a larger range of torsional head kinematics. Bilateral muscle pairs showed opposite kinematic coupling patterns during INC stimulation, INC inactivation and corrective post-stimulation movements, but left versus right INC perturbation had no clear influence on muscle-kinematic coupling. These suggest that neck muscles control specific torsional head orientations and movements via two general simplifying principles for the head-neck control system: symmetric bilateral control, and input-invariant muscle-kinematic coupling. Overall, the findings of the current dissertation suggest that neck muscle activation is not easily predicted from either behaviour or anatomy. However, cross-validation allowed me to examine neck EMG-kinematic relationships in a conservative and generalizable way. While during natural gaze behaviour horizontal head orientation is the main contributor to neck EMG, other components of 3-D head kinematics emerge during head movements. Some of my results may help to understand a clinical postural deficit known as torticollis. vi This dissertation is dedicated to my love, Maryam Rasti, whose sympathetic support, helped me to finish this chapter of my life. vii ACKNOWLEDGMENTS I would like to express my sincere gratitude to my supervisor, Dr. Douglas Crawford whose wisdom, continuous support and 'big-picture-attitude' was always with me during my PhD at York University. Without his guidance and thoughtftilness, I could have not been here. Dear Doug: THANK YOU! I would also like to thank my supervisory committee members, Dr. Barry Loughton and Dr. Maz Fallah who were very helpful in putting together my PhD results in perspective and refining my understanding of Physiology. My sincere thanks also go to Dr. Brian Corneil who was my mentor on neck electromyography and was tremendously helpful in making sense of my PhD findings. I would also like to take the opportunity to thank the people in Dr. Crawford's lab including the staff (Dr. Hongying Wang, Dr. Xiaogang Yan, and Saihong Sun), post-docs (Dr. Joost Dessing and Dr. Surya Dash) and my lab mates who were 'always there' whenever I needed their help and support. I would specially thank Dr. Pengfei Chang who helped me with data collection and Dr. Patrick Byrne whose help was very crucial in developing the statistical approach for my PhD dissertation. And last but not least, I would like to express my heartfelt appreciation for my fiance Mary am Rasti, her family and two of my best friends Mary am Rowghani and Hamidreza Seifollahi. Without these people's support, my life would have been different. TABLE OF CONTENTS GENERAL INTRODUCTION 1 Head and neck anatomy 1 Eye-head coordination in gaze 6 Donders' law of the head and Fick strategy 10 General neural mechanisms of gaze and head control 11 The interstitial nucleus of Cajal 20 Head movement control models 22 EMG technique 26 Neck muscle EMG 28 The goals of the current dissertation 30 CHAPTER 1: NECK MUSCLE SYNERGIES DURING STIMULATION AND DEACTIVATION OF THE INTERSTITIAL NUCLEUS OF CAJAL (INC) 32 ABSTRACT. 33 INTRODUCTION 34 METHODS 37 Surgical procedures 37 Experimental procedures 38 Data collection and analysis 40 RESULTS 44 Typical patterns of EMG activity of neck muscles 48 Normalized effects of INC stimulation/inactivation 51 DISCUSSION. 55 Comparison between stimulation of the INC and other brain areas 56 Relationship between muscle EMG and kinematics 57 Relationship between stimulation and inactivation 59 Clinical implications 61 SUPPLEMENTARY MATERIAL FOR CHAPTER 1 63 CHAPTER 2: CROSS-VALIDATED MODELS OF THE RELATIONSHIPS BETWEEN NECK MUSCLE ELECTROMYOGRAPHY AND THREE- DIMENSIONAL HEAD KINEMATICS DURING GAZE BEHAVIOUR 68 ABSTRACT. 69 INTRODUCTION 70 METHODS 74 Surgical procedures 74 Experimental task 77 Data collection 78 Data selection 78 Stepwise regression procedure 81 ix Reference frames and coordinate systems 88 RESULTS 93 Part I: static interval analysis 93 Neck EMG activity as a function of head orientation 94 Selection of 'static' model terms 97 Static model fits and coefficients 98 Part II: dynamic interval analysis and motion terms 104 Adding motion terms to the model 107 Acceleration versus deceleration Ill Visualizing the EMG versus 3-D head motion relationship 112 DISCUSSION 115 Neck EMG versus head orientation during static intervals 117 Neck EMG versus head kinematics during active head rotation (dynamic intervals) 119 Muscle anatomy versus functional activation 121 Implications for neural control 123 SUPPLEMENTARY MATERIAL FOR CHAPTER 2 127 CHAPTER 3: RELATIONSHIPS BETWEEN NECK MUSCLE ELECTROMYOGRAPHY AND THREE-DIMENSIONAL HEAD KINEMATICS DURING CENTRALLY-INDUCED TORSIONAL HEAD PERTURBATIONS. 131 ABSTRACT. 132 INTRODUCTION 133 METHODS 138 Surgical procedures 138 Experimental task 139 INC stimulation and inactivation 140 Data collection 141 Data selection 142 Data analysis: cross-validation and stepwise regression 148 RESULTS 149 Temporal head kinematics and neck EMG 149 Distributions of head orientation in the three datasets 154 Distributions of head velocity in the three datasets 157 Basic model for pooled corrective data 161 Left and right INC fits for stimulation, corrective and inactivation datasets 166 Comparative analysis 169 Anatomic and neural symmetry 170 Influence of perturbation source on EMG-kinematic coupling 175 DISCUSSION. 178 Neck muscle contributions during natural versus torsionally-perturbed head rotations 180 Relationship to anatomy and 3-D behaviour 183 Effect of the kinematic range on deriving model terms 184 X Bilateral
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