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Thesis Prodanov MORPHOMETRIC ANALYSIS OF THE RAT LOWER LIMB NERVES ANATOMICAL DATA FOR NEURAL PROSTHESIS DESIGN Printing of this thesis was supported by The Biomedical Signals and Systems group, Twente University J.E. Jurriaanse Stichting c D. Prodanov, 2006 No part of this work may be reproduced by print, photocopy, or any other means without a prior written permission from the author. ISBN 90-365-2275-7 NOT FOR SALE This manuscript was typeset by the author with LATEX2ε using type 1 Computer Modern fonts. Refer- ences are formatted with the Natural BiB code using the J. Comp. Neurol. BibTex style shared kindly by P. W. Daly, SI units are formatted using the code of M. Heldoorn. MORPHOMETRIC ANALYSIS OF THE RAT LOWER LIMB NERVES ANATOMICAL DATA FOR NEURAL PROSTHESIS DESIGN PROEFSCHRIFT ter verkrijging van de graad van doctor aan de Universiteit Twente, op gezag van de rector magnificus, prof. dr. W.H.M. Zijm, volgens besluit van het College voor Promoties in het openbaar te verdedigen op donderdag 26 januari 2006 om 16.45 uur door Dimiter Petkov Prodanov geboren op 16 maart 1975 te Sofia, Bulgarije Dit proefschrift is goedgekeurd door de promotors en assistent promotor prof. dr. E. Marani (promotor) prof. dr. P. Veltink (promotor) dr. H.K.P. Feirabend (assistent promotor) For the less even as for the greater there is some deed that he may accomplish but once only; and in that deed his heart shall rest. J.R.R. Tolkien, The Silmarillion, ch. 9 To my parents andtomyfriendsLuc,Dani,andIvo iii TABLE OF CONTENTS 1 General Introduction 1 1.1Neuralprostheses.................................... 1 1.2Structureofthenerves................................. 2 1.3 Comparative anatomy of the sciatic nerve in man and in rat . 4 1.4Aims........................................... 5 1.5Outlineofthethesis.................................. 6 2 FES for Sensory and Motor Functions: Progress and Problems 11 2.1Historyofelectricalstimulation............................ 12 2.2PrincipalnotionsinFES................................ 17 2.3ResearchProblems................................... 26 2.4 Contemporary Clinical applications of FES . 31 2.5 Evidence based evaluation of the FES applications . 36 2.6 Experimental and theoretical research........................ 38 2.7Modelingstudiesonselectivity............................ 40 2.8Conclusions....................................... 43 3 3D Topography of the Motor Endplates of the Rat Gastrocnemius Muscle 55 3.1Introduction....................................... 56 3.2MaterialsandMethods................................. 57 3.3Results.......................................... 60 3.4Discussion........................................ 65 3.5Conclusions....................................... 67 4 Fiber Populations of the Rat Sciatic Nerve, Its Spinal Roots and Branches 71 4.1Introduction....................................... 72 4.2MaterialsandMethods................................. 72 4.3Results.......................................... 75 4.4Discussion........................................ 93 4.5Conclusions....................................... 99 A Morphometricliteraturedata.............................100 B Mixturemodelingofthehistograms.........................100 C Parametersoftheoptimalmodels...........................104 5 Automatic Morphometry of Synaptic Boutons by Granulometric Analysis 109 5.1Introduction.......................................110 iv 5.2Methods.........................................110 5.3Results..........................................113 5.4Discussion........................................119 5.5Conclusions.......................................121 A Mathematicalmorphology...............................121 B Integralthresholding..................................122 6 Nerve Fiber Populations Innervating the Rat Gastrocnemius Muscles 125 6.1Introduction ......................................126 6.2Methods.........................................126 6.3Results..........................................131 6.4Discussion........................................136 6.5Conclusions.......................................138 7 Motor Axonal Clustering in the Rat Ventral Spinal Roots 141 7.1Introduction.......................................142 7.2Methods.........................................142 7.3Results..........................................147 7.4Discussion........................................152 A Statisticaldescriptions.................................156 8 General Discussion 163 8.1Thegastrocnemiusmuscle...............................163 8.2 Morphometric and spatial analysis of neuronal structures . 163 8.3Electricstimulationandstructuralorganization...................164 8.4Thecompositionofthenervesandtheroots.....................165 8.5Isthenerveaplexusoracable?...........................165 8.6Thegradienthypothesis................................166 8.7 Electric stimulation and spatial organization . 167 8.8Futureoutlooks.....................................168 9 Summaries and Appendices 173 v LIST OF FIGURES 1.1 MedicalconditionatdischargefromhospitalafterSCI.............. 2 1.2 Thespinalreflexarch................................ 3 1.3 Anatomyofthesciaticnerveinman........................ 4 1.4 Anatomyofthesciaticnerveinrat......................... 5 2.1 TheexperimentsofL.Galvani........................... 13 2.2 TheCuthbertsonfrictionmachine.......................... 14 2.3 TheMcNealmodel.................................. 20 2.4 Cuffelectrode..................................... 22 2.5 TheTwentearray................................... 24 2.6 The Twente implantable drop-foot stimulator . 32 2.7 SelectivityModeling................................. 41 3.1 Superficial AChE staining of the gastrocnemius muscle . 58 3.2 AChE staining of cross and longitudinal sections of the gastrocnemius muscle . 59 3.3 3DmapofMGL................................... 62 3.4 3DmapofMGM................................... 63 3.5 Totalparticleareapersection............................ 64 3.6 3DmapandtheTPAdistribution......................... 66 4.1 Histologyofselectedsamples............................ 74 4.2 Fibercountsinthespinalroots........................... 76 4.3 Densityoffibersinrootsandnerves........................ 77 4.4 Fiber diameter variation with functional modality . 78 4.5 Prevalentmodels................................... 82 4.6 Representative cases with optimal models . 84 4.7 Comparisonsofthespinalroots........................... 88 4.8 Transitionstothesciaticnerve........................... 89 4.9 Comparisonsofthesciaticnerve.......................... 91 4.10 Conduction velocities . 92 4.11 Borders and identities of the fiber populations in the roots and nerves . 95 5.1 Granulometryofabinaryimage...........................111 5.2 Granulometric filtering procedure of a synthetic image . 114 5.3 Averaged granulometric size density distribution of the entire image set . 115 5.4 The granulometric filtering applied on a real image . 116 5.5 Effect on DIV on the size distribution of the synaptic boutons . 117 vi 5.6 SensitivitytoAF...................................118 5.7 Sensitivitytobandwidth...............................119 5.B.1 Dependence of the AF on the pixel intensity . 123 6.1 Tracingandfiberidentification...........................128 6.2 Reconstructionofthematchedfiberpopulations.................134 6.3 Reconstructed diameter distributions of total populations of detected fibers . 135 7.1 Simulations of different types of point processes . 143 7.2 Definition of LCp(h) .................................144 7.3 Influence of the scale on T0.95(h)forsimulatedpatterns.............148 7.4 Behavior of Ψh(x, y)atdifferentscalesofstudy..................149 7.5 Inter-point and nearest neighbor distribution functions, case N1230 . 150 7.6 Inter-point and nearest neighbor distribution functions, case N1268 .......151 7.7 Influence of the scale parameter on the observed clustering . 153 7.8 Detected clusters related to the cross-sections...................155 7.A.1Examplesofthesimulationmasks..........................158 7.A.2 Inter-point distance analysis of the simulated patterns . 159 9.A.13DmapofMGL...................................179 9.A.23DmapofMGM...................................180 9.A.3 Granulometric filtering procedure of a synthetic image . 181 9.A.4 The granulometric filtering technique applied on a real image . 182 9.A.5 Behavior of the contour map Ψh(x, y)atdifferentscalesofstudy........183 9.A.6 Influence of the scale parameter on the observed clustering . 184 9.A.7 Detected clusters related to the cross-sections...................185 vii LIST OF TABLES 2.1 Morphology and electrophysiology of the fibers in the Peripheral Nervous System 21 4.1 Measured and derived morphological parameters of the myelinated fibers . 73 4.2 Quantitative parameters of the roots and nerves . 75 4.3 Comparisons between subsamples constituting the studied materials . 79 4.4 Side differences with respect to the fiber diameter . 80 4.5 Optimalmodelselection............................... 82 4.6 Fiber conduction velocities estimation according to the ABK equations . 90 4.7 Identities of the A, B,andC populations in the peripheral nerves . 96 4.A.1 Literature morphometric data on the normal rat lumbar nerves and roots . 100 4.C.1Parametersoftheoptimalmodels..........................104 5.1 Parameters and comparisons used in the validation studies . 112 5.2 Descriptive statistics of the measured boutons . 115 5.3 Matched synapses and disagreements - free trial . 115 5.4 Matched synapses and disagreements - calibrated trial
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