NEURAL PROCESSING OF MAGNETIC INTENSITY CUES BY LESIONED HOMING PIGEONS (COLUMBA LIVIA) IN A MAGNETIC CONDITIONING PARADIGM Merissa L. Acerbi A Thesis Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of MASTER OF ARTS May 2017 Committee: Verner P. Bingman, Advisor Anne K. Gordon William H. O'Brien ii ABSTRACT Dr. Verner P. Bingman, Advisor The ability to orient in an environment has been shown for centuries to be an important behavior in reproduction and survival. Many scientists agree the avian hippocampal formation (HF) is a brain structure involved in learning and memory tasks. Specifically, one type of learning and memory task, known as true navigation, defined as an animal’s ability to return home even when navigating in a novel environment. Previous research has shown one way birds are able to successfully complete true navigation is via the earth’s magnetic field. The question of what information is gathered with this geomagnetic sensitivity and where in the brain it is stored has remained unanswered. Currently, scientists theorize there are a number of avian species to use information about magnetic inclination via transduction by way of the Wulst area of the forebrain. However, few scientists have explored the role of magnetic intensity and what brain area(s) may be involved in order to successfully navigate. The current study illustrates the role of the HF as well as the Wulst during a novel magnetic conditioning paradigm where homing pigeons (Columba livia) experienced two different currents in magnetic intensity. Pigeons (N = 8) were trained, tested preoperatively and underwent one of two previously assigned experimental lesion surgeries (an electrolytic HF lesion, N = 4 or an aspirated Wulst lesion, N = 4). Postoperative data indicates the HF-lesioned pigeons were no longer able to discriminate magnetic intensity while the Wulst-lesioned pigeons continued performing significantly above chance level. Additionally, the Wulst lesions were substantially larger in size versus the HF lesions, suggesting most of the Wulst is not necessary when gathering information iii about magnetic intensity. The results draw attention to a divide in magnetic inclination versus magnetic intensity, and the possible difference in underlying neural mechanisms involved. iv There is no one else I could dedicate my thesis to besides the one who showed me what behavioral neuroscience is all about. v ACKNOWLEDGMENTS Above all, I could not have completed the research and writing for this thesis if it weren’t for my advisor, Dr. Vern Bingman. All of his encouragements, strong beliefs in my success, and continually challenging me to reach my goals gave me the courage to become a scientist and pursue research as a career. I would also like to thank Dr. Cordula Mora for being the kindest of mentors. Without any prior experience, she took me in as an undergraduate and walked me through all the steps of applying technique and detail to science. Throughout the years, I have had a number of truly exceptional research assistants that all helped me stay on top of what it takes to work with pigeons on a daily basis. This includes Mike Brooks, Lindsey Cunningham, Stephanie Davis, Mary Flaim, Natasha Flesher, Greg Grecco, Will Gyurgyik, Serena Foor, Stephanie Hylinski, Ashley Meehan, Imani Oliver, Amy Ruthenburg, Connie Santaigo, Jessica Sharp, Preston Stevenson, Sarah Tolfo, Jazmin Williams and Anna Wittmer. I also am incredibly thankful for my research colleagues, including Jared Branch, Vincent Coppola, Brittany Halverstadt, Dr. Robert Kirk, Diana Klimas, Mark McCoy, Lynzee Murray, Timothy Patrick, Josh Ricker and Brittany Sizemore. Additionally, I am beyond grateful for my committee members, Dr. Anne Gordon and Dr. Bill O’Brien, for their comments and questions during my proposal and defense meetings. I also received a valuable mentorship from Dr. Linda Rinaman. To add, I would like to thank Andy Wickiser for building all experimental equipment, Jeni Baranski/University of Animal Facilities staff for keeping a watchful eye on the pigeons, Dr. Susan Orosz as BGSU’s veterinarian and Russell Mora for writing the virtual map software used throughout the experiments. Lastly, countless appreciation goes to Christian Jacob Pemberton. Thank you. vi TABLE OF CONTENTS Page INTRODUCTION ........................................................................................................... 1 Avian Navigation ....................................................................................................... 1 Compass Mechanism ................................................................................................. 2 Map Mechanism......................................................................................................... 3 The Earth’s Magnetic Field ....................................................................................... 4 Processing Map Information ...................................................................................... 5 Processing Compass Information .............................................................................. 7 Current Study ........................................................................................................... 9 METHODS ........................................................................................................... 10 Subjects ........................................................................................................... 10 Experimental Setup .................................................................................................... 10 Magnetic Intensity Stimulus ...................................................................................... 11 Pre-Training Procedure .............................................................................................. 12 Preoperative Magnetic Conditioned Choice Training: Correction Trials .................. 13 Preoperative Magnetic Conditioned Choice Training without Corrections .............. 13 Postoperative Training ............................................................................................... 14 Wulst Aspiration Lesions ........................................................................................... 14 Hippocampal Formation Electrolytic Lesions ........................................................... 15 Wulst Control Series .................................................................................................. 15 Wulst and Hippocampal Formation Histology and Lesion Damage Reconstruction 16 Statistical Data Analysis ............................................................................................ 16 vii RESULTS ........................................................................................................... 18 Lesion Reconstruction ............................................................................................... 18 Behavior ........................................................................................................... 18 Pre- and Postoperative Learning Curve ......................................................... 18 Sessions to Criteria ........................................................................................ 20 Session Contrasts ........................................................................................... 20 Anti-Parallel/Parallel Control Series .............................................................. 21 DISCUSSION ........................................................................................................... 22 Preoperative Magnetic Conditioned Choice Training ............................................... 24 Preoperative Magnetic Conditioned Choice Training without Correction ................ 24 Postoperative Training ............................................................................................... 25 Anti-Parallel/Parallel Control Series .......................................................................... 25 Interpreting Results .................................................................................................... 26 Sham Lesion Group ................................................................................................... 27 Conclusion ........................................................................................................... 28 REFERENCES ...................................................................................................................... 29 APPENDIX A. FIGURES .................................................................................................... 37 APPENDIX B. INSTITUTIONAL ANIMAL CARE AND USE COMMITTEE APPROVAL LETTER .......................................................................................................... 50 1 INTRODUCTION Animal navigation is an increasingly popular field of study. Over the past 50 years, researchers have used behavioral measures to answer questions about navigation. Today, many questions require answers at a neurological level: what mechanisms are involved to produce the perception, cognition and behavior exhibited by navigating animals. Avian Navigation The ability to navigate to a goal location has been observed across a wide range of animal taxa, including (but not limited to) insects, fish, turtles, birds, and mammals (Able, 1982; Benhamou et al., 2011; Mouritsen, Atema, Kingsford & Gerlach, 2013; Müller & Wehner, 1988; Phillips