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Downloaded to a Microcomputer for Graphical Display and Statistical Analysis ANATOMICAL, BIOMECHANICAL AND BEHAVIOURAL CHARACTERISTICS OF THE HUMAN MASSETER MUSCLE by MoNICA DE LORENZO TONNDORF D.D.S., Federal University of Rio de Janeiro, 1986 A THESIS SUBMHTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE STUDIES (Department of Oral Biology) We accept this thesis as conforming THE UNIVERSITY OF BRITISH COLUMBIA October 1993 ©Mônica L. Tonndorf, 1993 ______________________ In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the head of my department or by his or her representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission. (Signature) Department of Oral Biology The University of British Columbia Vancouver, Canada Date November 8, 1993 DE-6 (2/88) ABSThAC There is little information on the anatomical and functional organization of the human jaw muscles, despite their importance to the masticatory system and disorders which affect it. The current studies examined the anatomical, biomechanical and functional characteristics in the multipennate human masseter muscle as a model for understanding function in the human jaw. Masseter anatomy was investigated in fetuses, adult cadavers, and living subjects by histology, gross anatomical dissection and Magnetic-Resonance (MR) imaging. Nerve pathways and muscle-fibre arrangements suggested that both fetal and adult muscles could be divided into at least four neuromuscular compartments. Although some fetal specimens had developed peimation, internal aponeuroses were seldom present. Structural variations were also found in the cadaveric material and living subjects. As the number of aponeuroses increased with development, and their thickness varied between individuals, individualized contraction strategies are likely to occur during function. Movements of masseter insertion sites during jaw function were modelled in dry skulls. Muscle origins and insertions were measured three-dimensionally at different gapes and simulated masticatory positions. Their movements varied with craniofacial dimensions and their locations on the mandible. For some parts of the muscle, the balancing-side and the incisal-contact positions provided the most advantageous lines of muscle fibre action, while for others, the working-side task was most favourable. Separate portions of the muscle are thus uniquely placed to perform specific tasks. 11 Movements of four insertion sites were also recorded in four living subjects. Insertion areas were identified on MR-derived reconstructions, and movements recorded with a jaw-tracking device. Ranges of insertion displacement were similar to these estimated for dry skulls, and varied between individuals. Interference electromyography, and single-motor-unit (MU) techniques were used to study physiological responses in eight subjects. The behaviour of low-threshold MUs was investigated relative to changes in bite side and experimental paradigm while subjects were biting on a force transducer. For each unit, the recruitment threshold, sustained-bite forces, the rate and regularity of sustained firing, and the coefficient of variation, were measured. Assessments were also made of the accuracy with which the target rates were attained, and of the contribution of each MU’s firing rate to bite force. These measures of behaviour frequently differed between tasks, but not reproducibly. The highest reproducibility and firing-rate accuracy were achieved when visual and auditory MU feedback was provided. A tendency for increased firing rate, and decreased discharge variability was found when subjects had no feedback. As approximately 50% of the units did not show reproducible behavioural characteristics, it seems that differences in intramuscular activation, differential activation of other muscles, and the inherent variability seen in low-threshold MU studies generally make quantitative comparisons of focal activity in the masseter implausible. Finally, a method was developed for locating the positions of moving needle electrodes relative to internal aponeuroses. It combined scanning electromyography, optical tracking of electrodes, MR imaging, and three-dimensional reconstruction. The 111 territorial sizes of 162 MUs were then assessed in the muscles of four subjects. Their mean width was 3.7 ± 2.3 mm. Most MU territories were confined between tendons, although 10% of the units clearly extended across at least one tendon. This focal dispersion of most territories provides a firm anatomical basis for selective activation of the muscle. The findings collectively indicate an anatomical, biomechanical and physiological basis for differential motor control of at least four neuromuscular compartments in the human masseter muscle. The extent to which the central nervous system selectively activates these compartments, or coactivates them, remains to be demonstrated under functional conditions. iv TABLE OF CONTENTS PAGE ABSTRACT ii TABLE OF CONTENTS v LISTOFFIGURES xi LIST OF TABLES xvi ACKNOWLEDGEMENTS xvili 1. INTRODUCTION 1 1.0 Introduction to the Thesis 1 Review of the Literature 1.1 Skeletal Muscle Development 2 1.2 Muscle Architecture and Mechanics 10 1.3 Motor-Unit Organization 18 1.3.1 Motor-Unit Arrangement 18 1.3.2 Fibre Characteristics 19 1.4 Motor-Unit Activity 20 1.4.1 Recruitment 21 1.4.2 Firing Rate 21 1.4.3 Behaviour 22 1.4.4 Summary 25 1.5 Partitioning 25 V 1.6 Jaw Muscle Organization . 28 1.6.1 Structure 29 1.6.2 Fibre Composition 33 1.6.3 Jaw Biomechanics 35 1.6.4 Summary 36 1.7 Anatomical Design of the Masseter. 38 1.7.1 Muscle Organization 39 1.7.2 Innervation Pattern 43 1.7.3 Muscle Fibre Characteristics 45 1.7.4 Spindle Distribution 46 1.7.5 Summary 47 1.8 Functional Design of the Masseter 47 1.8.1 Motor-unit Territory 47 1.8.2 Functional Differentiation 49 1.8.3 Motor-unit Activity 52 1.8.3 Conclusion 54 2. STATEMENT OF THE PROBLEM 56 3. STUDIES 60 3.1 Masseter Morphology 61 3.1.1 Exploratory Experiments on Fetal Masseter Anatomy 61 3.1.1.1 Materials and Methods 62 3.1.1.1.1 Nerve Staining 65 vi 3.1.1.1.2 Connective-Tissue and Muscle-Fibre Staining. 68 3.1.1.1.3 Muscle-Fibre Staining and Orientation Assessment 68 3.1.1.1.4 Muscle Reconstruction 68 3.1.1.2 Results 74 3.1.1.2.1 Nerve Distribution 74 3.1.1.2.2 Connective-Tissue Development 76 3.1.1.2.3 Muscle-Fibre Orientation 76 3.1.1.3 Discussion 83 3.1.2 Adult Masseter Anatomy 87 3.1.2.1 Materials and Methods 88 3.1.2.1.1 Gross Anatomical Dissection 88 3.1.2.1.2 Chemical Dissection 89 3.1.2.2 Results 90 3.1.2.3 Discussion 98 3.1.3 Morphological Reconstruction in Living Subjects 101 3.1.3.1 Methods 101 3.1.3.1.1 Magnetic-Resonance Imaging 101 3.1.3.1.2 Imaging 103 3.1.3.1.3 Reconstruction 107 3.1.3.1.4 Error of Method 111 3.1.3.2 Results 111 vii 3.1.3.3 Discussion . 117 3.2 Movement of Masseter Insertions at different Jaw Positions 125 3.2.1 Simulated Function in Dry Skulls 126 3.2.1.1 Methods 126 3.2.1.2 Results 133 3.2.1.2.1 Cephalometric Analysis of the Skull Sample.. 133 3.2.1.2.2 Sample Variation in Insertion Site Location during Dental Intercuspation 136 3.2.1.2.3 Effect of Jaw Position on Insertion Site Location 136 3.2.1.2.4 Differences within Putative Muscle Layers ... 141 3.2.1.2.5 Differences between Putative Muscle Layers . 143 3.2.1.2.6 Orientation of Masseter Insertion relative to Origin 145 3.2.1.2.7 Discussion 147 3.2.2 Function in Living Subjects 157 3.2.2.1 Methods 158 3.2.2.2 Results 163 3.2.2.3 Discussion 169 3.3 Evaluation of the Masseter’s Functional Performance 175 3.3.1 Electromyographic Recording Techniques 175 3.3.2 Preliminary Experiments using Single-Wire EMO Recording viii Technique 176 3.3.2.1 Materials and Methods 177 3.3.2.2 Results 183 3.3.2.3 Discussion 187 3.3.3 Motor-Unit Behaviour 192 3.3.3.1 General Methods 192 3.3.3.1.1 Motor-Unit Recording 192 3.3.3.1.2 Bite-Force Measurement 196 3.3.3.1.3 Sampling and Data Analysis 201 3.3.3.2 Effect of Bite Side on MU Behaviour 202 3.3.3.2.1 Methods 204 3.3.3.2.2 Results 208 3.3.3.2.3 Discussion 217 3.3.3.3 Effect of Experimental Paradigm 222 3.3.3.3.1 Methods 222 3.3.3.3.2 Results 224 3.3.3.3.3 Discussion 227 3.4 Motor-Unit Territory Relative to the Masseter’s Internal Architecture . 230 3.4.1 Methods 232 3.4.1.1 Stereotactic Location of EMG Needle Electrode Scans 232 3.4.1.1.1 Morphologic Reconstruction 232 3.4.1.1.2 Motor-Unit Recording 233 ix 3.4.1.1.3 Needle Location • . 234 3.4.1.1.4 Scan Location • . 236 3.4.1.1.5 Methodological Errors • . 239 3.4.1.2 Motor-Unit Territory • . 243 3.4.2 Results • . 245 3.4.3 Discussion • . 250 4. GENERAL DISCUSSION AN]) CONCLUSIONS • . 260 5. FUTURE DIRECTIONS • . 265 6. BIBLIOGRAPHY • . 269 7. APPENDIX • . 299 x LIST OF FIGURES PAGE Figure 1 Fetal peripheral-nerve staining 66 Figure 2 Fetal connective-tissue staining 69 Figure 3 Cross-sectional optical scan (Z-scan) through a 10-jim fetal-muscle section 72 Figure 4 Superimposition of two horizontal optical sections situated at both extremes of a 1O-m-thick fetal muscle section 73 Figure 5 Masseteric nerve pathway in the human fetal masseter 75 Figure 6 Development of aponeurotic layers in the fetal masseter and medial pterygoid muscles 77 Figure 7 Masseter muscle fibres in the 18 weeks old human fetus 78 Figure 8 Characteristics of fetal muscle tissues 79 Figure 9 Parasagittal sections from two 18-week human fetuses showing fibre orientation complexity 80 Figure 10 Masseter-muscie dissection showing the superficial and intermediate muscle layers 92 Figure 11 Masseter-muscie dissection showing its layered arrangementposteriorly and the ascending attachment sites of muscle fibres as the layers become deeper 93 Figure 12 Masseter-muscie cross-section showing its internal aponeuroses .
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