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A Comparative Analysis of the Neural Basis for Dorsal-Ventral Swimming in the Nudipleura

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A Comparative Analysis of the Neural Basis for Dorsal-Ventral Swimming in the Nudipleura Georgia State University ScholarWorks @ Georgia State University Biology Dissertations Department of Biology Summer 8-8-2012 A Comparative Analysis of the Neural Basis for Dorsal-Ventral Swimming in the Nudipleura Joshua L. Lillvis Georgia State University Follow this and additional works at: https://scholarworks.gsu.edu/biology_diss Recommended Citation Lillvis, Joshua L., "A Comparative Analysis of the Neural Basis for Dorsal-Ventral Swimming in the Nudipleura." Dissertation, Georgia State University, 2012. https://scholarworks.gsu.edu/biology_diss/119 This Dissertation is brought to you for free and open access by the Department of Biology at ScholarWorks @ Georgia State University. It has been accepted for inclusion in Biology Dissertations by an authorized administrator of ScholarWorks @ Georgia State University. For more information, please contact [email protected]. A COMPARATIVE ANALYSIS OF THE NEURAL BASIS FOR DORSAL-VENTRAL SWIMMING IN THE NUDIPLEURA by JOSHUA L. LILLVIS Under the Direction of Paul S. Katz ABSTRACT Despite having similar brains, related species can display divergent behaviors. Investi- gating the neural basis of such behavioral divergence can elucidate the neural mechanisms that allow behavioral change and identify neural mechanisms that influence the evolution of behav- ior. Fewer than three percent of Nudipleura (Mollusca, Opisthobranchia, Gastropoda) spe- cies have been documented to swim. However, Tritonia diomedea and Pleurobranchaea cali- fornica express analogous, independently evolved swim behaviors consisting of rhythmic, alter- nating dorsal and ventral flexions. The Tritonia and Pleurobranchaea swims are produced by central pattern generator (CPG) circuits containing homologous neurons named DSI and C2. Homologues of DSI have been identified throughout the Nudipleura, including in species that do not express a dorsal-ventral swim. It is unclear what neural mechanisms allow Tritonia and Pleurobranchaea to produce a rhythmic swim behavior using homologous neurons that are not rhythmic in the majority of Nudipleura species. Here, C2 homologues were also identified in species that do not express a dorsal-ventral swim. We found that certain electrophysiological properties of the DSI and C2 homologues were similar regardless of swim behavior. However, some synaptic connections differed in the non- dorsal-ventral swimming Hermissenda crassicornis compared to Tritonia and Pleurobranchaea. This suggests that particular CPG synaptic connections may play a role in dorsal-ventral swim expression. DSI modulates the strength of C2 synapses in Tritonia, and this serotonergic modulation appears to be necessary for Tritonia to swim. DSI modulation of C2 synapses was also found to be present in Pleurobranchaea. Moreover, serotonergic modulation was necessary for swim- ming in Pleurobranchaea. The extent of this neuromodulation also correlated with the swimming ability in individual Pleurobranchaea; as the modulatory effect increased, so too did the number of swim cycles produced. Conversely, DSI did not modulate the amplitude of C2 synapses in Hermissenda. This indicates that species differences in neuromodulation may account for the ability to produce a dorsal-ventral swim. The results indicate that differences in synaptic connections and neuromodulatory dy- namics allow the expression of rhythmic swim behavior from homologous non-rhythmic compo- nents. Additionally, the results suggest that constraints on the nervous system may influence the neural mechanisms and behaviors that can evolve from homologous neural components. INDEX WORDS: Evolution, Neuromodulation, Homology, Mollusc, Electrophysiology, Synapse A COMPARATIVE ANALYSIS OF THE NEURAL BASIS FOR DORSAL-VENTRAL SWIMMING IN THE NUDIPLEURA by JOSHUA L. LILLVIS A Dissertation Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in the College of Arts and Sciences Georgia State University 2012 Copyright by Joshua L. Lillvis 2012 A COMPARATIVE ANALYSIS OF THE NEURAL BASIS FOR DORSAL-VENTRAL SWIMMING IN THE NUDIPLEURA by JOSHUA L. LILLVIS Committee Chair: Paul S. Katz Committee: Ronald L. Calabrese Charles D. Derby Anne Z. Murphy Electronic Version Approved: Office of Graduate Studies College of Arts and Sciences Georgia State University August 2012 iv ACKNOWLEDGEMENTS Thank you to Paul Katz for all of your guidance, advice, and patience. You took a chance on me a few years back, and I do not take that for granted. Whatever ability I have in this field is directly attributable to you. That said whatever inability that remains is certainly not due to your lack of trying. Thank you to Ron Calabrese, Chuck Derby, and Anne Murphy for the great advice and suggestions I received from you all as members of my dissertation committee. The thoughtful input I received at our meetings was extremely valuable to the progression of this work and to my progression as a researcher. A number of past and current members of the Katz lab have helped me immensely and been good friends during my time at GSU. Bob Calin-Jageman, Jim Newcomb, and Evan Hill showed me the ropes when I first entered the lab. Moreover, they made it a really fun place to work. Akira did all those things as well, and continues to be an unbelievably talented and fun colleague. I feel very fortunate to have worked in a lab with Akira for so many years. Thank you also to Charuni Gunaratne who joined the lab a few years after my arrival. Charuni has been a great colleague, sounding board, and friend. I must recognize my undergraduate research advisors during my tenure at Ohio State. Julie Mustard and Jeri Wright were the first people to really get me excited about research. I walked into the bee lab looking for a fun job and walked out with new career aspirations. Thank you also to the great faculty at GSU for setting me on the right path. In particular, I would like to thank Tim Bartness, Don Edwards, Sarah Pallas, Vincent Rehder, and Bill Walthall for serving as teachers and committee members during my time at GSU. Also, thank you to all of my friends from Ashtabula to Atlanta and beyond that I have not yet mentioned. In particular thanks to Jack Barile, Laura Been, Kevin Bokoch, Irina Calin- Jageman, Dave DeWitt, Mike DeWitt, Chase Falivene, Ian Fides, Fro Hertzi, Joe Jamgochian, v Michelle Jamgochian, Josh Tuminella, and Todd Williams for keeping things fun. That is, after all, the most important thing. Thank you to my parents, Sue and Dean Lillvis. You guys are THE BEST. I appreciate you supporting my objectively weird decision to go to graduate school and research the neural mechanisms underlying sea slug behavior. Thank you to my sister, Kristen Lillvis, for being such a great sister and friend. I thought we were neck and neck on this thing for a bit, but you ended up lapping me. I guess I don’t run like the wind these days. vi TABLE OF CONTENTS ACKNOWLEDGEMENTS .............................................................................................. iv LIST OF ABBREVIATIONS .......................................................................................... vii LIST OF FIGURES ......................................................................................................... ix CHAPTER 1: INTRODUCTION ...................................................................................... 1 CHAPTER 2: NEUROCHEMICAL AND NEUROANATOMICAL IDENTIFICATION OF CENTRAL PATTERN GENERATOR NEURON HOMOLOGUES NUDIPLEURA MOLLUSCS ..................................................................................................................26 CHAPTER 3: COMPARATIVE ANALYSIS OF ELECTROPHYSIOLOGICAL PROPERTIES AND SYNAPTIC CONNECTIONS OF HOMOLOGOUS NEURONS RELATED TO BEHAVIOR IN NUDIPLEURA MOLLUSCS ..........................................48 CHAPTER 4: SEROTONGERGIC NEUROMODULATION INTRINSIC TO CENTRAL PATTERN GENERATORS UNDERLYING ANALOGOUS INDEPENDENTLY- EVOLVED MOTOR PATTERNS ...................................................................................76 CHAPTER 5: GENERAL DISCUSSION ...................................................................... 100 REFERENCES ............................................................................................................ 116 APPENDIX A: ELECTROPHYSIOLOGICAL PROPERTIES OF C2 MELIBE LEONINA AND FLAELLINA IODINEA ........................................................................................ 127 APPENDIX B: NEUROPEPTIDE EXPRESSION IN THE TRITONIA DIOMEDEA BRAIN ......................................................................................................................... 138 vii LIST OF ABBREVIATIONS 5-HT serotonin ASD antiserum diluent BWN body wall nerve C2 cerebral neuron 2 Ce cerebral ganglion CPG central pattern generator CPT cerebropleural ganglion triplets DA dopamine DMSO dimethyl sulfoxide DRI dorsal ramp interneuron DSI dorsal swim interneuron DV dorsal-ventral E excitatory E:I excitatory and inhibitory EOD electric organ discharge EPSP excitatory postsynaptic potential Flab Flabellina iodinea Herm Hermissenda crassicornis I inhibitory Ib Hermissenda Interneuron B IPSP inhibitory postsynaptic potential LR left-right JAR jamming avoidance response Mel Melibe leonina viii NO nitric oxide NOS nitric oxide synthase NSF National Science Foundation OT oxytocin PBS phosphate buffered saline Pd pedal ganglion PdN2 pedal nerve 2 PdN3 pedal nerve 3 Pl pleural ganglion Pleur Pleurobranchaea californica PP2 pedal-pedal commissure 2 PSP postsynaptic potential SCP small cardioactive
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