MAKING SENSE: WEAKLY ELECTRIC FISH MODULATE SENSORY FEEDBACK VIA SOCIAL BEHAVIOR AND MOVEMENT by Sarah A. Stamper A dissertation submitted to Johns Hopkins University in conformity with the requirements for the degree of Doctor of Philosophy Baltimore, Maryland June, 2012 © 2012 Sarah Stamper All Rights Reserved Abstract Animals rely on sensory information for the control of their behavior. Understanding this process requires a detailed description of the sensory feedback that they receive, which is often determined by an animal’s proximity to conspecifics and its own movement within the environment. This dissertation examines the role of social behavior and movement for the modulation of electrosensory feedback in weakly electric fish. We made observations of weakly electric fish in their natural habitats and found that some species of fish, which typically have more complex social behaviors, are most often found in groups. These same species will preferentially approach a refuge with a social signal in the laboratory. As a result of social grouping these fish receive continuous electrosensory oscillations (amplitude and phase modulations) caused by the interactions from the electric fields of each individual. Interestingly, both social grouping and movement can produce higher order modulations (termed ‘envelopes’), which can have lower frequency content than the first order modulations. Curiously, we did not observe low frequency envelopes in the majority of our samples. To determine why that might be the case we tested the behavioral responses of weakly electric fish to envelope stimuli in controlled laboratory experiments. We found that Eigenmannia will increase or decrease their electric organ discharge (EOD) frequency in response to social envelope stimuli, termed the Social Envelope Response (SER). The strength of the SER was dependent on the initial envelope frequency and the stimulus amplitude, whereby lower frequency envelopes and higher stimulus amplitudes resulted in the strongest EOD changes. As a consequence of ii the EOD change the envelope frequency during the course of a trial was increased, suggesting that the SER may be a mechanism for avoiding low frequency social envelopes. These results may explain our field results that showed weakly electric fish do not typically produce low-frequency envelopes in natural social groups. These fish are not only processing electrosensory information from their social behavior but are also simultaneously process electrosensory information from their own movement and the movement of nearby objects in their environment. To investigate the relationship between movement and the modulation of sensory feedback we tested the ability of Eigenmannia to track a moving refuge under varied sensory conditions by changing the illumination (vision) and conductivity (electroreception) across trials. When the fish relied solely on electrosensory information during tracking they performed additional movements that consisted of whole-body oscillations and tail bends, which may be used to shape electrosensory feedback. Our results indicate that weakly electric fish continuously process two streams of information, one derived from social interactions and the other from movement, which are used for the independent control of the fish’s electric organ and the fish’s locomotor system. In addition, both social behavior and movement can be used to modulate electrosensory feedback. Future studies should examine sensory processing in the context of the animal’s social behavior and their movement within the environment, as it can categorically change the signals that the animal is receiving. Candidate: Sarah A. Stamper Readers: Gregory F. Ball, Amy J. Bastian, Noah J. Cowan, Eric S. Fortune (Advisor) and Rüdiger Krahe iii This thesis is dedicated to the fish: Martini, Tequila, Whiskey, Mojito, Sangria, Brandy & Sweetie iv Acknowledgements Although writing this dissertation really only happened in the last few months it was the culmination of years and years of work. And I don’t just mean the work I did writing it—the real work isn’t evident in these pages. This dissertation simply would not have been possible without a village of people on the sidelines who supported and encouraged me along the way. So, I’ll just start at the beginning. I would like to thank my parents who started loving me the minute I came out as a screaming, crying mess and have continued to do so even though not much has changed. My parents taught me to work hard, whether it was schoolwork or bargain shopping. Of course, both of these skills turn out to be essential for surviving graduate school. My parents also made efforts to encourage my interest in science by letting me play with ‘toys’ such as microscopes, chemistry sets, sea monkeys, and ant farms. And I can’t forget my favorite of all time, the “Diggin’ Up Dinosaurs” archeology set they bought me even though it was abundantly clear I’d never have enough patience for that! They also kept buying me critter after critter—fish (Cleo and Monstro), hamsters (Teddy, Rascal, Twinkie, and Sausage), hermit crabs (#1-4), a bird (Clyde), a turtle (Lilly Pad), a cat (Kitty Kitty Katra) and dogs (Lollipup, Max, and Lil Moo)—which instilled in me my love of animals and subsequently the study of animal behavior. So I would like to formally thank my parents for encouraging my interests even though it sometimes meant my mom had to pull slugs out of my throat or my dad had to stay up all night with me catching lightning bugs. I was also quite fortunate to have a series of great teachers throughout my early education. I would like to thank my 3rd grade teacher Mrs. Gaylin for not reporting me to v the authorities when I turned in my assignment called “It’s Sad But True” a picture book detailing the demise of all my aforementioned critters. That was a close call, and I think she was only slightly more certain that I was destined to become a scientist rather than a serial killer. I was also lucky to have Dr. DaRif as my 10th grade chemistry teacher. He sponsored my science fair project on blood splatter (back before CSI was all the rage), and again, correctly interpreted the topic of this project to indicate that I was scientifically curious and not necessarily a developing psychopath. In addition, Mrs. Robinson and Mrs. Barber, who taught keyboard and yearbook, respectively, ended up teaching me skills that have turned out to be instrumental in my career, especially with regards to the preparation of manuscripts, talks, and conference posters. Then I went to New College where I was fortunate enough to be advised by Dr. Gordon Bauer. Gordon was the exact right level of tough (except that time he threatened to break my kneecaps) paired with unwavering encouragement and support. He went out of his way to find research opportunities for me and gave me my early introduction to research with exotic creatures. I absolutely agree with his assertion that his formal title should read “Dr. Gordon B. Bauer, BFD” because I simply wouldn’t be where I am today without him. So let’s fast-forward to my time spent in graduate school at Hopkins. I’ve only been here 3.5 years but there was a small army’s worth of people that helped me get through the program. I am grateful to Lauren Jones for her friendship and ensuring that I occasionally eat balanced meals. I’d like to thank Dr. Amy Shelton who is incredibly helpful with respect to almost everything but especially my occasional stress-induced breakdowns. Dr. Steve Yantis, Dr. Peter Holland and Dr. Michela Gallagher provided me vi frequent and invaluable feedback on my progress as a graduate student. I should also thank Dr. Justin Halberda, who offered guidance that was transformative to the way I approach teaching. I would especially like to thank Dr. Gregory Ball, who practically adopted me as his advisee and has always made time to meet with me regarding all the major departmental requirements and pretty much anything else I wanted to talk about. Importantly, Greg also facilitated my newfound appreciation of Belgium beer. I would like to thank the graduate students and postdocs, and particularly Judith Asem, Steve Chang, Farrah Madison, Jeff Mayse, Melvin Rouse and Tyler Stevenson. I would also like to thank the members of the LiMBS Lab with special thanks to Manu Madhav, Eatai Roth and Eric Tytell who were a tremendous help not only with regards to my research but also my personal sanity (or insanity) in the lab. There are also so many things that wouldn’t have been possible without an awesome administration staff, especially Laura Dalrymple, Julie Feldmeyer, Lindsay Licari, Jen Newman, Hope Stein, and Jesse Warford. I also owe the biggest thank you possible to Jim Garmon, who kept my research afloat (sometimes literally) by building everything I needed. And finally, I would like to thank Melvin Bullock, who was always happy to have a quick chat (and kept me from being run over) as I crossed San Martin Drive. This was a nice end to my day after having just spent 14 hours in a basement staring at fish. Speaking of fish, for the last three years I’ve done my research on weakly electric fish, as evidenced by the topics in this dissertation. What you might not know is that the electric fish community is the absolute nicest and most helpful scientific community imaginable. I sincerely thank all the current and former electric fish PIs, post-docs, and graduate students, especially Dr. Len Maler, Dr. Maurice Chacron, and Dr. Rüdiger vii Krahe who have all provided invaluable feedback on just about every single one of my research projects. I owe an enormous debt of gratitude to my advisor Dr. Eric Fortune and my co- advisor Dr.