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A Theoretical and Experimental Investigation Into the Distribution, Morphology and Function of Pacinian Corpuscles

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A Theoretical and Experimental Investigation Into the Distribution, Morphology and Function of Pacinian Corpuscles A theoretical and experimental investigation into the distribution, morphology and function of pacinian corpuscles. Submitted by Joanne Danielle Dale to the University of Exeter as a dissertation for Master of Philosophy in Physics, October 2014. This dissertation is available for Library use on the understanding that it is copyright material and that no quotation from the dissertation may be published without proper acknowledgement. I certify that all material in this dissertation which is not my own work has been identified and that no material has previously been submitted and approved for the award of a degree by this or any other University. (Signature) ……………………………………………………………………………… 1 Abstract The distribution, morphology and function of the pacinian corpuscle was examined. The distribution in rat feet was recorded using both Magnetic Resonance Imaging (MRI) and dissection. The mechanical properties of the corpuscle were investigated using a theoretical model based upon previous work by (Loewenstein & Skalak, 1966). The model was used to examine how the corpuscle’s structure affects its function in healthy and diseased states. Distribution data gathered by dissection revealed the majority of corpuscles were restricted to the adipose tissue of each foot pad. Densest concentrations were in the rear foot pads. The remainder were located in the digits and in close proximity of bone via the interosseous membrane and wrist ligaments. Localisation near capillaries was common. MRI was not invasive and detected a greater number of corpuscles but held limitations in its ability to separate corpuscles in close proximity. Dissection was invasive and showed a lower number of corpuscles but greater confidence could be contributed to the correct identification of each corpuscle. The theoretical model was developed over three levels: (i) the original model (LSM) as described by Loewenstein and Skalak. (ii) the L2 model where a second order elastic force is added and finally (iii) the L3 model where the parameters are modernised based upon current literature. These models describe how mechanical force is transmitted through the structural components of the corpuscle. The L2 model shows the additional elastic forces overall 2 impact is relatively small. Adjusting the original model's parameters for the L3 model shows decreased sensitivity of the corpuscle. Finally, the L3 model was applied to examine how the high number of lamellae layers associated with Dupuytren’s contracture and other pacinian pathologies reduces the amount of pressure felt at the core, thus providing a potential insight into the cause of loss of touch perception in patients. 3 Acknowledgements I would like to thank my supervisors Dr I.R.Summers and Prof C.P.Winlove for the opportunity they provided for me to pursue my love of science and for their contribution of knowledge towards this study. I wish them all the best for the future. Further thanks must go to my husband Dr Steven Hepplestone, my parents Mr Ian Dale and Mrs Diane Dale, my mother in law Mrs Eileen Hepplestone and my three children Cherry, Coral and Indiana for providing endless encouragement, support and inspiration throughout. I would also like to take this time to thank the many people who provided the resources and facilities to complete the work contained. These include but are not limited to Dr Ellen Green for her assistance in the wet laboratory of Exeter University, Dr Dr. Abdelmalek Benattayallah of the MR research centre for his professional guidance using the MR scanner, Dr Kenton Arkill of Bristol university for access to the tissue samples, Prof Phillipe Young for the use of his FE software Simpleware and all the other members of the Biomedical Physics research group at the University of Exeter for tea, chat, cake and good company. 4 Title page with declaration ………………………………………….1 Abstract ………………………………………………………………..2 Acknowledgements……………………………………………………4 List of Contents …………………………………………………… ….6 List of Figures…………………………………………………………10 List of Tables………………………………………………………….13 5 List of Contents 1. Introduction to touch 1.1 The importance of skin……………………………………………………....14 1.2 Structure of mammalian skin………………….………………………........15 1.3 Mammalian cutaneous receptors…………….……………………………15 1.4 Mechanoreceptors……………………………………………………………17 1.5 The pacinian corpuscle………………………………………………………19 1.6 The somatosensory pathway of the pacinian corpuscle……………….22 1.7 The importance of touch research………………………………………….23 1.8 Study overview…………………………………………………………………23 2. Investigation of the distribution of the pacinian corpuscle in the rat foot. 2.1 Introduction…………………………………………………………………….25 2.2 Background…………………………………………………………………….25 2.3 Methods…………………………………………………………………………27 2.3.1 High resolution Magnetic Resonance Imaging…………………………27 2.3.2 Gross dissection…………………………………………………………….28 6 2.4 Results…………………………………………………………………………..29 2.5 Discussion………………………………………………………………………42 3. Models of the pacinian corpuscle. 3.1 Background….………………………………………………………………...48 3.1.2 Pathologies of the pacinian corpuscle…………………………………55 3.2 Previous modelling…………………………………………………………..57 3.2.1 Loewenstein & Skalak……………………………………………………..57 3.2.2 Holmes & Bell………………………………………………………………59 3.3 Method…………………………………………………………………………59 3.3.1 The Loewenstein & Skalak model………………………………………60 3.3.2. The LSM with additional elastic components (the L2 model)…….64 3.3.3 Modernising parameterisation………………………………………….66 3.3.4 Computational method…………………………………………………..71 3.4 Results………………………………………………………………………..72 3.4.1 Replication of Loewenstein & Skalak…………………………………72 3.4.1.1 Displacement in response to static compression………………..73 3.4.1.2 Pressure in response to static compression………………………74 7 3.4.1.3 Pressure in response to sinusoidal stimulation…………………..76 3.4.1.4 Pressure in response to decompression…………………………..77 3.4.2 Additional modelling…………………………………………………….79 3.4.3 The effect of an additional elastic force (or comparison between L1 and L2 models)………………………………………………………………….81 3.4.4 The effect of parameter modernisation (or comparison between L1 and L3 models)………………………………………………………………….87 3.4.4.1 Varying the number of lamellae……………………………………..87 3.4.4.2 Total corpuscle length………………………………………………..91 3.4.4.3 Thickness of lamellae…………………………………………………92 3.5 Discussion of the L3 model………………………………………………95 4. Using the L3 to help explain the effect of Dupuytren’s disease on the pacinian corpuscle’s function. 4.1 Background……………………………………………………………….…97 4.2 Method…………………………………………………………………….….97 4.3 Results……………………………………………………………………..…98 4.4 Discussion…………………………………………………………………..100 8 5. Conclusions and suggestions for future work. 5.1 Experimental conclusions……………………………………………..……101 5.2 Theoretical conclusions……………………………………………………..102 5.3 Suggestions for future work……………………………………………......103 References…………………………………………………………………………106 Appendix A…………………………………………………………………………114 9 List of Figures Figure 1: Cutaneous touch receptors. Figure 2: Mammalian hairy skin. Figure 3: The pacinian corpuscle and its internal structure. Figure 4: Stretch activated ion channels. Figure 5: Somatosensory pathway. Figure 6 (a): MR image of rat rear foot. Figure 6 (b): MR image of rat rear foot with fat suppression. Figure 7 (a): MR image of the rat fore foot. Figure 7 (b): MR image of the rat fore foot with fat suppression. Figure 8: Sketch of pacinian corpuscles found in rear rat foot by gross dissection. Figure 9: Sketch of pacinian corpuscles found in fore rat foot by gross dissection. Figure 10: Sketch of pacinian corpuscles found in rear rat foot by MRI. Figure 11: Sketch of pacinian corpuscles found in fore foot by MRI. Figure 12: Sketch of pacinian corpuscles found in rear foot by MRI and gross dissection. 10 Figure 13: Sketch of pacinian corpuscles found in fore foot by MRI and gross dissection. Figure 14: Cluster sizes in rat rear foot. Figure 15: Cluster sizes in rat fore foot. Figure 16: Schematic of rapid adaptation function. Figure 17: Growth curves of corpuscle length and width. Figure 18: Cord and finger bend associated with Dupuytren’s disease. Figure 19: Loewenstein & Skalak schematic of the pacinian corpuscle Figure 20: Additional forces included in enhanced models (L2 and L3). Figure 21: Static lamella displacement in response to varying compressions (L1). Figure 22: Core pressure against radius for a static compression of 20µ applied to the outermost lamellae (L1). Figure 23: Core pressure resulting from sinusoidal displacement of the outermost lamellae. Figure 24: Core pressure for a sudden release from a total compression of 20 µm (L1). Figure 25: Computed and experimental membrane action potentials. Figure 26: Pressure amplitude at different positions in the corpuscle for sinusoidal stimulation at various frequencies. 11 Figure 27: Displacement amplitude at different positions in the corpuscle for sinusoidal stimulation at various frequencies. Figure 28: Comparison between L1 and L2 showing how lamellae displace with depth in response to external static compressions. Figure 29: Comparison between L1 and L2 showing pressure throughout the corpuscle with a static compression of 20 µm. Figure 30: Comparison between L1 and L2 showing core pressure in response to various static input pressures. Figure 31: Comparison between L1 and L2 showing core pressure for a fixed compression followed by release. Figure 32: Strength of the second order elastic constant on core pressure in response to static load (L3). Figure 33: Effect of varying α on core pressure in response to a fixed pressure
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