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An Autoradiographic Study of the Ontogeny of Receptor AN AUTORADIOGRAPHIC STUDY OF THE ONTOGENY OF RECEPTOR BINDING SITES IN THE CENTRAL VISUAL PATHWAY OF THE RAT. Dominic Hansel Lobo Submitted for the Degree of Doctor of Philosophy Department of Anatomy and Developmental Neurobiology University College, London MAY 1991 1 ProQuest Number: 10629656 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a com plete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. uest ProQuest 10629656 Published by ProQuest LLC(2017). Copyright of the Dissertation is held by the Author. All rights reserved. This work is protected against unauthorized copying under Title 17, United States C ode Microform Edition © ProQuest LLC. ProQuest LLC. 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106- 1346 TO ALL MY NDUGU’S 2 I ACKNOWLEDGMENTS First and foremost, this is dedicated to the three wise men who have shown me the True Way, Professor Guz for being my usurer, to Ndugu for his concern in my affairs, the Family for all the inspiration and, to Dooz for seeing me over the final hurdles and sorting out the final edit. My thanks and appreciation extends to Dr. John Pamavelas for his faith in me through all the trials and tribulations, Professor Lieberman for the use of laboratory space, Dr. Pradeep Bhide for his exorbitant consultation fees, Dr. Mike Stewart for the use of the Image Analysis system at the Open University, Dr. Steve Hunt for starting me off and Dr. Kevin Murphy for the printer control. Last and by no means least, to all those innumerable to mention, thank you for your inspirations, concerns, advice and support shown to me during my time at UCL. 3 ABSTRACT The developmental profile of somatostatin ( SS ), neuropeptide Y ( NPY ), cholecystokinin ( CCK ) and vasoactive intestinal polypeptide ( VIP ) receptor binding sites has been examined in the central visual pathway of the rat, from late embryonic life through to adulthood, using in vitro receptor autoradiographic techniques. High levels of SS receptor binding sites which were detected in late embryonic life were considerably diminished at birth. SS receptor binding site levels increased from postnatal day 4 ( P4 ) to the end of the third postnatal week; concentrations decreased slightly but still remained high and persisted throughout the rest of development. A caudo-rostral gradient seemed to exist in the developing cortex. Receptor binding sites for CCK were not present in the embryo or at birth but appeared in the first week of postnatal life. During the second postnatal week, the concentration of CCK receptor binding sites increased dramatically, continuing to rise until the end of the fourth postnatal week and was maintained in the adult. VIP receptor binding sites were present in the embryo and these low levels persisted in the first postnatal week. The density of binding sites gradually increased in the second week, reaching a peak at the end of third postnatal week. These concentrations of VIP receptor binding sites remained at this level in adult life. NPY receptor binding site densities were low in the perinatal period. These levels increased slightly in the first postnatal week and showed a peak at the the beginning of the second week. Thereafter, the density of NPY receptor binding sites remained constant and this trend continued into adulthood. The results are discussed in relation to other processes occurring during the development of the visual system. 4 TABLE OF CONTENTS Page No. ACKNOWLEDGMENTS 3 ABSTRACT 4 1.0 INTRODUCTION 8 1.1 Historical overview of receptors 9 1.1.1 Receptor characterization by autoradiography 14 1.2 Overview of the rat visual pathway 17 1.2.1 Morphology of the dorsal lateral geniculate nucleus 17 1.2.2 Connections of the dorsal lateral geniculate nucleus 18 1.2.3 Neurochemistry of the dorsal lateral geniculate nucleus 19 1.2.4 Morphology of the superior colliculus 22 1.2.5 Connections of the superior colliculus 23 1.2.6 Neurochemistry of the superior colliculus 24 1.2.7 Morphology of the visual cortex 27 1.2.8 Connections of the visual cortex 29 1.2.9 Neurochemistry of the visual cortex 31 1.3 Neuropeptides in the visual cortex 38 (i) Somatostatin 38 (ii) Cholecystokinin 40 (iii) Vasoactive intestinal polypeptide 42 (iv) Neuropeptide Y 43 1.3.1 Development of the superior colliculus, dorsal lateral geniculate nucleus and visual cortex 45 (i) Neurogenesis and migration 47 5 (ii) Morphogenisis and differentation 49 Afferent and efferent connections 51 Neuropeptides in development 52 (i) Somatostatin 52 (ii) Cholecystokinin 53 (iii) Vasoactive intestinal polypeptide 54 (iv) Neuropeptide Y 55 MATERIALS and METHODS 57 Receptor binding methodology - General considerations 57 Preparation of animals 58 Slide and section preparation 59 Receptor autoradiography method 60 Computer image analysis of autoradiograms 62 (i) Assay conditions 64 (ii) Buffers and Materials 65 RESULTS 67 The normal development of somatostatin receptor binding sites 67 Development of somatostatin receptor binding sites in monocularly enucleated animals 70 The normal development of cholecystokinin receptor binding sites 83 6 3.2.1 Development of cholecystokinin receptor binding sites in monocularly enucleated animals 87 3.3 The normal development of vasoactive intestinal polypeptide receptor binding sites 88 3.3.1 Development of vasoactive intestinal polypeptide receptor binding sites in monocularly enucleated animals 105 3.4 The normal development of neuropeptide Y receptor binding sites 107 3.4.1 Development of neuropeptide Y receptor binding sites in monocularly enucleated animals 120 4.0 DISCUSSION 132 4.1 Methodology - Technical considerations 132 4.1.1 Tissue preservation 134 4.1.2 Assay conditions 135 4.1.3 Visualization of the image 137 4.1.4 Analysis of computer-assisted autoradiographs 138 4.2 Development of somatostatin receptor binding sites 140 4.3 Development of cholecystokinin receptor binding sites 144 4.4 Development of vasoactive intestinal polypeptide receptor binding sites 151 4.5 Development of neuropeptide-Y receptor binding sites 157 4.6 SUMMARY 161 5.0 LIST OF ABBREVIATIONS 164 6.0 REFERENCES 166 7 1.0 INTRODUCTION It is thought that virtually all information processing in the brain involves synaptic communication mediated via neurotransmitters acting at specific receptor sites. For optimal response of a cell or organism, the demands are that they be sensitive and responsive to a variety of signals of intracellular and extracellular origin. Specific cellular mechanisms must therefore exist to ensure such environmental sensitivity. This signal responding ability is a function of receptors designed to respond specifically to the coding sequences of a wide variety of chemical and physical stimuli. In order to demonstrate that a substance found in nerve cells is the transmitter those cells secrete at their synapses, certain criteria have to be met ( Werman, 1966 ). As a rule, at least five different stages are considered in chemical neurotransmission, these being that, the substance is present within the nerve cell and specifically in its presynaptic terminals, that the nerve cell can synthesize or accumulate the substance, that it can release the substance when activated, and when the substance is released, it must be shown to mimic in every aspect the functional activity following stimulation of the nerves that released it, including the magnitude and quality of changes in postsynaptic membrane conductances. There should also be binding to postsynaptic receptors and finally inactivation through enzymatic or re-uptake processes. This sequence of events is firmly established for numerous neurotransmitters in both the peripheral ( PNS ) and central nervous systems ( CNS ). Confusion surrounds the study of neuroactive peptides. Various classes or families of peptides based on their common molecular structure are known to exist, but this chemical index does not provide an insight into the way these substances are utilized in signal transduction between neurons. Some peptides which perform modulatory or regulatory roles, do not satisfy the strict criteria requirements for neurotransmitters and are classified as " neuromodulators ". The physiological and pharmacological effects of the regulatory peptides are mediated by their interaction with specific recognition sites 8 termed H receptors". In parallel with the growing number of peptides being discovered, multiple receptors for these peptides have been characterized ( Snyder and Innis, 1979; Hokfelt et al., 1980; Krieger et al., 1983; Bjorklund et al., 1985 ). Pharmacological and biochemical techniques have provided evidence for the existence of multiple receptors for the different peptide families ( Boast et al., 1986; Kuhar et al., 1986; Leslie, 1987; McLean et al., 1987 ). It is of interest to know to what extent the shape and connections of a neuron are determined by other neurons, glia, chemical gradients and other factors in the ontogenesis of the neuron. Investigation into these questions are answered in two ways: observation of interrelationships in normal development or observation of patterns of variation arising in abnormal circumstances due to particular mutations, chemical or surgical manipulations. As to the role function plays in defining patterns of connections, this has been addressed by research into the role of visual input in
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