New Behavioral Insights Into Home Range Orientation of the House Mouse (Mus Musculus) by Blythe E
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New Behavioral Insights Into Home Range Orientation of the House Mouse (Mus musculus) By Blythe E. Alexander Submitted to the graduate degree program in Ecology and Evolutionary Biology and the Graduate Faculty of the University of Kansas in partial fulfillment of the requirements for the degree of Doctor of Philosophy. ________________________________ Rudolf Jander ________________________________ Helen M. Alexander ________________________________ Kenneth B. Armitage ________________________________ Linda Trueb ________________________________ Stephen Egbert Date Defended: May 4, 2011 The Dissertation Committee for Blythe Alexander certifies that this is the approved version of the following dissertation: New Behavioral Insights Into Home Range Orientation of the House Mouse (Mus musculus) ________________________________ Rudolf Jander Date approved: ii Abstract Home‐range orientation is a necessity for an animal that maintains an area of daily activity. The ability to navigate efficiently among goals not perceived at the starting point requires the animal to rely on place recognition and vector knowledge. These two components of navigation allow the animal to dynamically update its current position and link that position with the locomotor distance and direction needed to reach a goal. In order to use place knowledge and vector knowledge the animal must learn and remember relevant spatial information obtained from the environment and from internal feedback. The research in this dissertation focuses on behavioral components of topographic orientation, using the house mouse as a model species. Specifically, this research made important discoveries in three main areas: 1) locomotor exploration behavior, 2) the use of learned spatial information for compass orientation, and 3) testable hypotheses based on the controversial cognitive map. In Chapter 1, I used a radial arm maze to find a systematic locomotor component to exploration behavior, which is typically described as random movement. Exploration refers to the learning process that occurs as an animal acquires relevant spatial information for home‐range orientation. I predicted that this process must have a systematic component; and the results revealed that in a radial arm maze, mice avoided exploring a place explored one and two visits prior. Therefore, locomotor exploration does have a systematic component. In Chapter 2, I trained mice to navigate to their home within a circular arena, with access to a visual beacon and an enriched visual background. The mice showed that to navigate home, they preferred to rely on the extra‐arena (background) cues for compass direction. However, when these extra‐arena cues became unreliable, the mice showed flexibility in their preference by ignoring the visual background and instead relying on the visual beacon to locate home. This flexibility in cue use negates a popular theory, called the snapshot theory, which does not allow for such flexibility in navigation. To further study the use of compass cues in mice, in Chapter 3, I utilized a plus‐maze to manipulate both allothetic (environmental) and idiothetic (internal) cues. The purpose was to determine which cue type predominated the directional choice of mice at the maze intersection while both leaving and returning home. Previous studies have ignored the potential difference in cue use during the complete roundtrip an animal would make within its home range. The results show that mice relied on different cues for the outward path and the homing path of a familiar complex roundtrip. Finally, I developed two testable hypotheses and a valid experimental design that can be used to test house mice, and other animals, for the so‐called cognitive map. An animal that has a cognitive map would be able to compute a novel shortcut to a goal relying exclusively on the flexibility of such a map, and not from the other two options of novel shortcutting: guidance orientation or path integration. Thus by designing my experiments to eliminate the potential for the mice to rely on a guiding cue to direct them home, and by eliminating the ability to compute a shortcut by summing the vectors previously walked, I was able to test mice for a iii truly novel, map‐based shortcut home. These two hypotheses were named viewpoint extrapolation and viewpoint interpolation and require pure visual exploration to acquire the necessary place and vector knowledge. Both experiments showed that mice were not capable of using pure visual exploration and therefore these studies provide no evidence that mice have a cognitive map. Overall, my research provides evidence that mice do have a mental route‐ based map and to build such a mental map, locomotor exploration is necessary and sufficient for acquiring relevant spatial knowledge to later use to efficiently navigate. iv Acknowledgements I would like to thank my advisor, Rudolf Jander, for his excellent advice with regards to my experimental designs, presentations and clarity of writing. His knowledge and advice were invaluable to my dissertation research. I would also like to thank my committee members, Helen Alexander, Ken Armitage, Linda Trueb, and Steve Egbert for their support and helpful comments on my manuscript. Many undergraduates helped me with data collection, especially Carla Burford, Cory Keene, Will Pass, David Richart, Running Wolf, Anssi Santanen, Ryan Townley, Najib Wardak, Brian Wyrowski, and Erin Zarr. Finally, my parents, James and Rosemary Alexander, provided me with much needed love, support, advice, and helped me maintain my sanity. I am also grateful to a great group of friends who were always there to support me, locally and from a far. To all of these people, I offer heartfelt thanks for helping me through to the end. v Table of Contents GENERAL INTRODUCTION.................................................................................................................. 1 CHAPTER 1: LOCOMOTOR PATTERNS IN THE EXPLORING HOUSE MOUSE (MUS MUSCULUS).............................................................................................................................................12 INTRODUCTION ....................................................................................................................................................... 13 METHODS................................................................................................................................................................. 14 RESULTS................................................................................................................................................................... 17 DISCUSSION ............................................................................................................................................................. 19 FIGURES.................................................................................................................................................................... 23 CHAPTER 2: FLEXIBLE PREFERENCE BETWEEN DISTAL VISUAL CUES OR A SALIENT, VISUAL BEACON AS DIRECTIONAL CUES FOR HOMING IN THE HOUSE MOUSE (MUS MUSCULUS).............................................................................................................................................28 INTRODUCTION ....................................................................................................................................................... 29 METHODS................................................................................................................................................................. 30 RESULTS................................................................................................................................................................... 34 DISCUSSION ............................................................................................................................................................. 35 FIGURES.................................................................................................................................................................... 41 CHAPTER 3: FEEDBACK CONTROL OF A NAVIGATING HOUSE MOUSE AWAY FROM HOME AND BACK: IDIOTHETIC OR ALLOTHETIC?....................................................................46 INTRODUCTION ....................................................................................................................................................... 47 SPECIAL METHODS AND RESULTS....................................................................................................................... 53 DISCUSSION ............................................................................................................................................................. 59 FIGURES.................................................................................................................................................................... 68 CHAPTER 4: THE SHORTCUT AND THE MAP IN THE RODENT NAVIGATION SYSTEM: EXPERIMENTS WITH THE HOUSE MOUSE (MUS MUSCULUS) ................................................72 INTRODUCTION ....................................................................................................................................................... 74 GENERAL METHODS .............................................................................................................................................. 76 EXPERIMENT 1: METHODS..................................................................................................................................