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The Giant Interneuron Pathways and Escape Reflexes of the Aquatic Oligochaete, Branchiura Sowerbyi Mark Joseph Zoran Iowa State University

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The Giant Interneuron Pathways and Escape Reflexes of the Aquatic Oligochaete, Branchiura Sowerbyi Mark Joseph Zoran Iowa State University Iowa State University Capstones, Theses and Retrospective Theses and Dissertations Dissertations 1987 The giant interneuron pathways and escape reflexes of the aquatic oligochaete, Branchiura sowerbyi Mark Joseph Zoran Iowa State University Follow this and additional works at: https://lib.dr.iastate.edu/rtd Part of the Zoology Commons Recommended Citation Zoran, Mark Joseph, "The giant interneuron pathways and escape reflexes of the aquatic oligochaete, Branchiura sowerbyi " (1987). Retrospective Theses and Dissertations. 8604. https://lib.dr.iastate.edu/rtd/8604 This Dissertation is brought to you for free and open access by the Iowa State University Capstones, Theses and Dissertations at Iowa State University Digital Repository. It has been accepted for inclusion in Retrospective Theses and Dissertations by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. INFORMATION TO USERS While the most advanced technology has been used to photograph and reproduce this manuscript, the quality of the reproduction is heavily dependent upon the quality of the material submitted. For example: • Manuscript pages may have indistinct print. In such cases, the best available copy has been filmed. • Manuscripts may not always be complete. In such cases, a note will indicate that it is not possible to obtain missing pages. • Copyrighted material may have been removed from the manuscript. In such cases, a note will indicate the deletion. Oversize materials (e.g., maps, drawings, and charts) are photographed by sectioning the original, beginning at the upper left-hand corner and continuing from left to right in equal sections with small overlaps. 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Other University Microfilms International 0 The giant interneuron pathways and escape reflexes of the aquatic oligochaete, Branchiura sowerbyi by Mark Joseph Zoran A Dissertation Submitted to the Graduate Faculty in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY Department; Zoology Major; Zoology (Neurobiology) Approved: Signature was redacted for privacy. In Charge of Major Work Signature was redacted for privacy. For the Major Degœrtment Signature was redacted for privacy. uate College Iowa State University Ames, Iowa 1987 ii TABLE OF CONTENTS Page GENERAL INTRODUCTION 1 Evolution of Annelid Giant Fiber Systems 1 Biology of Branchiura sowerbyi 3 Explanation of Dissertation Format 5 CHAPTER I. RAPID ESCAPE REFLEXES IN AQUATIC 7 OLIGOCHAETES: VARIATIONS IN DESIGN AND FUNCTION OF EVOLUTIONARILY CONSERVED GIANT FIBER SYSTEMS Introduction 7 Materials and Methods 9 Animals and maintenance 9 Anatomy 10 Electrophysiology 11 Results 15 Giant fiber morphology 15 Electrophysiological correlates of rapid escape 27 reflexes Escape reflex function in the Lumbriculida 34 Escape reflex function in the Tubificida 38 Discussion 40 Conservation of giant fiber design and function 40 Divergence of aquatic and terrestrial 41 escape systems Adaptive significance of giant fiber systems 42 All-or-none versus graded escape responses 46 Acknowledgments 48 iii References 48 CHAPTER II. THE LATERAL GIANT INTERNEURONS OF THE 53 TUBIFICID WORM, BRANCHIURA SOWERBYI; STRUCTURAL AND FUNCTIONAL ASYMMETRY OF A PAIRED GIANT FIBER SYSTEM Introduction 53 Materials and Methods 54 Animals and maintenance 54 Histological procedures 54 Microdissection procedures 55 Lucifer yellow procedures 56 Horseradish peroxidase procedures 57 Ferric ion-ferrocyanide staining procedures 57 Electrophysiological procedures 58 Results 59 Anatomy of the LGF system 59 Electrophysiology of the LGF system 72 Discussion 80 LGF spike initiation 83 LGF spike propagation 84 Acknowledgments 89 References 89 CHAPTER III. THE RAPID TAIL WITHDRAWAL REFLEX OF THE 93 TUBIFICID WORM, BRANCHIURA SOWERBYI; ADAPTATIONS FOR SPEED AND EFFICACY IN AN ALL-OR-NONE ESCAPE RESPONSE Introduction 93 Materials and Methods 94 Animals and maintenance 94 iv Non-invasive recordings 94 Semi-intact preparations 95 Videotape and cinematography of escape 97 sequences Results 98 Videotaped escape responses 98 Afferent timing and transmission 101 Central conduction 104 Efferent timing and transmission 104 In situ escape reflex timing 112 Discussion 118 Acknowledgments 122 References 123 GENERAL SUMMARY 125 GENERAL REFERENCES 128 APPENDIX A 131 APPENDIX B 133 APPENDIX C 135 GENERAL ACKNOWLEDGMENTS 136 1 GENERAL INTRODUCTION Study of the giant nerve fibers of many animals, most notably the squid (Young, 1936; Hodgkins, 1964), has extensively contributed to our knowledge of fundamental cellular neurophysiology. Nevertheless, the specific role of giant fibers in many animal groups is less well understood, but is generally presumed to involve the mediation of rapid escape or startle reflexes. The obvious survival advantage conferred by giant fibers is a more rapid impulse conduction along the body and, therefore, a faster and more effective escape. Evolution of Annelid Giant Fiber Systems Although giant fiber systems are found in nearly half of the major animal groups (phyla), these systems have evolved independently and are for the most part examples of convergent evolution. Also, giant fiber systems have arisen independently within single phyla (e.g., Annelida) and even within classes (e.g., Polychaeta). Timm (1979) suggested that as the seas of the Carboniferous period withdrew, drying large marine marshes, some ancestral annelids began to adapt to more terrestrial conditions. The divergence of the sea-dwelling polychaetes and the terrestrial and freshwater oligochaetes (see Appendix A, Fig. 1) is reflected in comparative studies of modern 2 annelid giant fiber systems. The divergence and subsequent radiation of the polychaetes has produced considerable diversity in the number and design of giant nerve fibers (Nicol, 1948; Bullock, 1948; Bullock and Horridge, 1965). In contrast, there has been an evolutionary conservation in giant fiber number and arrangements among oligochaetes (Chapter I). All free-living oligochaetes studied to date, including the Lumbricida, Tubificida, and Lumbriculida possess three dorsal giant fibers (see Appendix B, Table 1). In these worms, the giant fibers function as two distinct escape reflex systems: a medial giant fiber (MGF) system activated by sensory input from anterior segments and a lateral giant fiber (LGF) system consisting of two, electrically-coupled fibers activated by input from posterior segments (Drewes, 1984). This dichotomous arrangement of MGF and LGF systems provides the opportunity to investigate the influence of various factors such as habitat (aquatic versus terrestrial), lifestyle (errant versus sedentary), and predatory pressure (anterior vulnerability versus posterior vulnerability) on the design and function of oligochaete giant fiber systems. The rapid escape reflexes of many terrestrial oligochaetes have been well documented (for reviews see Dorsett, 1978; Drewes, 1984). In addition, it is well known that many aquatic oligochaetes, such as tubificids, rapidly withdraw in response to vibrational or tactile stimuli (Stephenson, 1930); 3 however, there has been no correlated anatomical, physiological, and behavioral study of an aquatic oligochaete escape reflex. The present dissertation is the first correlated examination of such a reflex in the tubificid worm, Branchiura sowerbyi. Biology of Branchiura sowerbyi Branchiura sowerbyi (Beddard, 1892) is a mud-dwelling tubificid worm widely distributed throughout freshwaters of the world. The species is generally limited to the benthos of shallow littoral zones of lakes, most often collected in water depths of 5 m or less (Causey, 1953). Burrowers like Branchiura invest the majority of their time foraging in the top 2-8 cm of sediment, rarely venturing into the substrate beyond a depth of 20 cm (McCall, 1982). They derive the bulk of their nutritional requirements from micro-organisms
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