Rockefeller University Digital Commons @ RU Student Theses and Dissertations 1967 Inhibitory Fields in the Limulus Lateral Eye Robert B. Barlow Follow this and additional works at: http://digitalcommons.rockefeller.edu/ student_theses_and_dissertations Part of the Life Sciences Commons Recommended Citation Barlow, Robert B., "Inhibitory Fields in the Limulus Lateral Eye" (1967). Student Theses and Dissertations. Paper 42. This Thesis is brought to you for free and open access by Digital Commons @ RU. It has been accepted for inclusion in Student Theses and Dissertations by an authorized administrator of Digital Commons @ RU. For more information, please contact [email protected]. INHIBITORY FIELDS IN THE LIMULUS LATERAL EYE A thesis submitted to the Faculty of the Rockefeller University in partial fulfillment of the requirements for the degree of Doctor of Philosophy by Robert B. Barlow Jr., A. B. April 1967 The Rockefeller University New York, New York Preface I would like to express my gratitute to the administration of Rockefeller University and especially to Dr. Detlev Bronk for the opportunity to participate in the graduate program and for their generous support of my family and myself. Also, I would like to thank the students and faculty of the University who together provided a stimulating atmosphere for the pursuit of a graduate education. My deepest personal thanks go to my advisors, Drs. H. Keffer Hartline and Floyd Ratliff. The rich experience of working with them in the laboratory and of discussing with them the many aspects of this work have been invaluable to me. I am indebted to Dr. Don Quarles, research mathematician at the IBM Watson Research Center, Yorktown Heights, New York for the theoretical analysis contained in this thesis. Some of his many contributions are cited within the text. I thank him for his generous assistance and uncountable hours of helpful discussions. There are many others to whom thanks are due: Drs. David Lange, Fred Dodge, and Bruce Knight for their very helpful suggestions which are too numerous to list; to Dr. Victor Wilson and the thesis committee for their instructive comments; to the skilled instrument makers, Werner Krug and Hans Braun; to the American Optical Company for supplying the fiber optic instruments; to my wife for typing the early drafts of the thesis and Mrs. Richard Costello for typing the final draft; and to Miss Ruth Mandlebaum and the illustration service for their artistry in preparing the figures. For the patience and understanding of my wife and family I am forever grateful. Ill Summary The spatial distribution of the inhibitory influences exerted by ommatidia in the Limulus lateral eye was measured. The source of inhibition was a small cluster of ommatidia illuminated through a flexible bundle of glass fibers ("fiber optics"). The inhibitory field of the cluster was determined by measuring the decrease it produced in the response frequency of surrounding ommatidia which were illuminated individually through single glass fibers. Applied directly to the corneal facets of the ommatidia, the single fibers provided unusually effective stimulation with a minimum of light scatter into adjacent receptors. The inhibitory field is elliptically shaped with its major axis in the antero-posterior direction on the eye. In the adult 2 animal the field covers an area of 15 mm (about 30% of the eye) and contains approximately 300 ommatidia; however, less than one- third of that number receives the bulk (75%) of the inhibitory effects exerted by the small cluster in the center. The position of maximum inhibition is located at some distance from the center of the field: 0.8 mm or 3 ommatidial diameters in the dorso-ventral direction and 1.3 mm or 5 ommatidial diameters in the antero­ posterior. The inhibitory effect tapers off toward the periphery becoming negligible at approximately 2 mm from the center of the field in the dorso-ventral direction and at 3.3 mm in the ventro- posterior direction. The configuration of the field was found to be similar for a number of experiments in which the source of inhibition was located in various positions on the eye. Control experiments show that the diminution of the inhibitory effect near the center of the field is not an artifact of the measuring technique and cannot be readily explained by local competing excitatory processes. IV The ommatidial inhibitory fields enhance visual contrast. Borders and steep intensity gradients in the retinal image are accentuated by maxima and minima (Mach bands) in the response pattern of the optic nerve. A theoretical analysis of the contrast phenomena indicates that the shape of the Mach bands is determined by the configuration of the inhibitory field. Patterns of the optic nerve activity in response to simple, stationary patterns of illumination were measured and compared to theoretically calculated response patterns. The features common to the experimental and calculated response patterns are directly correlated to the most prominent characteristic of the inhibitory field: a diminution in the inhibitory effect near the center of the field. There are, however, some significant discrepancies between theory and experiment resulting most likely from the restriction of the theoretical model to a one-dimensional array of receptors. Preliminary studies using a more realistic two- dimensional representation of the eye are in somewhat better agreement with the experimental results. TABLE OF CONTENTS Page Preface ii Summary iii INTRODUCTION 1 CHAPTER I. THE LIMULUS LATERAL EYE 4 Anatomy 4 The Ommatidium as a Receptor Unit 9 Lateral Inhibition 11 The Lateral Spread of Inhibition and the Enhancement of Contrast , . 19 CHAPTER II. METHODS 23 Biological Preparations 23 Fiber Optics Illumination System 25 a) General Description 25 b) Single Fiber Instrument 27 c) Fiber Bundles 32 d) Mach Band Instrument 35 e) Rigid Optics vs. Fiber Optics 36 f) Manipulators 37 Data Collection and Processing 39 Measuring The Inhibitory Coefficient 40 CHAPTER III. INHIBITORY FIELDS 43 Introduction 43 A Mapping Experiment 45 Configuration of the Inhibitory Field 50 Inhibitory Thresholds 59 Interpretation of the Inhibitory Field 60 A) Scattered Light ..... 61 B) Local Neural Excitation 64 C) Conclusion 66 Receptive Fields: Limulus vs. Vertebrate 67 Discussion 72 VI Page CHAPTER IV. MACH BANDS 73 Introduction , 73 Theoretical Calculations 77 Experimental Measurements 89 Comparison 95 Summary 102 Two-dimensional Model: Preliminary Results 103 APPENDIX I. THE DEPENDENCE OF THE INHIBITORY COEFFICIENT ON THE LEVEL OF EXCITATION 105 APPENDIX II. THE PHYSIOLOGICAL RANGE OF THE OMMATIDIA IN THE LIMULUS EYE 117 APPENDIX III. THE PROJECTION OF THE OPTIC NERVE ON THE RETINAL MOSAIC 122 BIBLIOGRAPHY 127 INTRODUCTION Nervous inhibition in the retina and other sensory systems has received much attention in recent years by students of neurophysiology, psychophysics, and behavior. It is becoming increasingly evident that the interaction of nervious elements and the integration of inhibitory and excitatory influences play an important role in processing sensory information at various levels of the nervous system. The role of nervous inhibition in sensory physiology however is not new. Nearly one hundred years ago Ernst Mach (1865) investigated the long-known ability of the visual system to accentuate contours and borders. With remarkable insight he concluded that the ability must originate in a reciprocal inhibitory interaction of neighboring elements in the retina. More recently, Bekesy (1928) hypothesized a similar mechanism for enhancing frequency discrimination in the auditory system. These speculations based primarily on indirect evidence from psychophysical experiments have since been supported by the direct observation of the responses of single nerve cells located at various levels in the sensory system. Early evidence on the role of neural inhibition in sensory physiology was obtained by Hartline (1938 and 1940) who recorded complex retinal responses from the optic nerve fibers in the vertebrate eye. He attributed the complexity of the responses to the integrated effects of excitatory and inhibitory influences mediated over pathways that interconnect the ganglion cells and the photoreceptors. A similar Observation on the opposed influences in the vertebrate retina was made by Granit (for reviews see Granit, 1947 and 1955). Moreover, neural inhibition has been observed in single auditory nerve fibers (Galambos and Davis, 1944), in higher auditory centers (Suga, 1965), and in the cutaneous system (Mountcastle and Powell, 1959), In each instance there is strong evidence to suggest that the inhibitory interaction depends on the separation of the elements in the receptor mosaic, which is exactly what Mach postulated to account for the enhancement of visual contrast at contours. If in the visual system the inhibitory interaction is stronger for near neighbors in the receptor mosaic than for more widely separated ones, then the contrast effects will be greatest in the vicinity of sharp dis­ continuities in light intensity in the retinal image. That is, certain features of the retinal image such as outlines of objects and edges of shadows will tend to be emphasized at the expense of accurate information concerning the intensity of light at each point in the image. A more accurate description of the visual contrast effects requires a knowledge of the lateral spread of inhibition across the receptor mosaic. In particular, the strength