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University of Pennsylvania ScholarlyCommons Publicly Accessible Penn Dissertations Winter 2009 Sensorimotor Integration an a Small Motor Circuit Nicholas D. DeLong University of Pennsylvania, [email protected] Follow this and additional works at: https://repository.upenn.edu/edissertations Part of the Systems Neuroscience Commons Recommended Citation DeLong, Nicholas D., "Sensorimotor Integration an a Small Motor Circuit" (2009). Publicly Accessible Penn Dissertations. 34. https://repository.upenn.edu/edissertations/34 This paper is posted at ScholarlyCommons. https://repository.upenn.edu/edissertations/34 For more information, please contact [email protected]. Sensorimotor Integration an a Small Motor Circuit Abstract Rhythmic motor patterns, which underlie behaviors such as mastication, respiration and locomotion, are generated by specialized neural circuits called central pattern generators (CPGs). Although CPGs can generate their rhythmic motor output in the absence of rhythmic input, these motor patterns are modified by rhythmic sensory feedback in vivo. Furthermore, although the importance of sensory feedback in shaping CPG output is well known, most systems lack the experimental access needed to elucidate the mechanisms underlying sensorimotor integration at the cellular and synaptic level. I am therefore examining this issue using the gastric mill CPG, a circuit which generates the rhythmic retraction and protraction motor activity that drives chewing by the teeth in the gastric mill compartment of the crustacean stomach. The gastric mill CPG is well defined and very accessible at the cellular level. Specifically, I am examining the mechanism by which the gastropyloric receptor (GPR), a phasically active proprioceptor, selectively prolongs one phase (retraction) of the gastric mill rhythm in the isolated nervous system when it is activated in a pattern that mimics its in vivo activity. I first demonstrate that GPR regulation of the gastric mill rhythm relies on its presynaptic inhibition of modulatory commissural neuron 1 (MCN1), a projection neuron that activates and drives this rhythm. I also demonstrate that the GPR inhibition of MCN1 regulates the gastric mill rhythm by selectively regulating peptidergic cotransmission by MCN1. Lastly, I demonstrate that a peptide hormone (crustacean cardioactive peptide) that only modestly modifies the gastric mill rhythm, strongly gates the GPR regulation of this rhythm. Mechanistically, it acts not by influencing GPR or MCN1, but yb activating the same excitatory current in the CPG neuron LG (lateral gastric) that is activated by MCN1-released peptide. This novel gating mechanism reduces GPR control over the amplitude of this excitatory current in LG. Thus, I have identified specific cellular mechanisms yb which (a) phase-specific egulationr of an ongoing motor pattern by a sensory input is accomplished, and (b) hormonal modulation gates that sensory input. These events are likely to reflect comparable ones occurring in the larger and less accessible vertebrate CNS. Degree Type Dissertation Degree Name Doctor of Philosophy (PhD) Graduate Group Neuroscience First Advisor Michael Nusbaum Keywords Neuromodulation, Sensory, Motor, Invertebrate, Central Pattern Generator, CPG Subject Categories Systems Neuroscience This dissertation is available at ScholarlyCommons: https://repository.upenn.edu/edissertations/34 SENSORIMOTOR INTEGRATION IN A SMALL MOTOR CIRCUIT Nicholas David DeLong A DISSERTATION in Neuroscience Presented to the Faculties of the University of Pennsylvania in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy 2009 ---------------------------------- Michael P. Nusbaum, Ph. D. Supervisor of Dissertation ---------------------------------- Rita Balice-Gordon, Ph. D. Graduate Group Chair Dissertation Committee: Marc Schmidt, Ph. D. (Committee Chair) Joshua Gold, Ph. D. Diego Contreras, Ph. D. Farzan Nadim, Ph. D. (Rutgers University, Dept. of Biology) Acknowledgements The years I have spent completing this thesis work could not have been possible without a lot of help and support from a lot of people. I am very thankful to all of them. Mikey: It has been a privilege to work with you. You taught me an incredible amount about science, writing, communication, presentation, problem solving and a lot of other things I’m probably not even aware of. I know that I could not have gotten that education anywhere else. The Nusbaum Lab: Thanks Aaron, for talking science, movies, politics and stand-up comedy with me for the past 6 years. Dawn, for always being there to answer my questions about anything and everything. Rachel and Jason, for making the whole experience of grad school a lot more fun, and always being there to share a beer (or 3) at SFN and NerveNet. My Family: Mom and Dad, I can’t thank you enough for the amazing support over the last six years. There is simply no possible way I could have done it without you. Sue and Holly, for encouraging me to do well since I was too young to remember, and for never calling me a nerd (wait, forget that last part). ii Madelyn: For always making me smile, no matter what, and for always being proud of her daddy. Sara: For making me happy and keeping me sane for the last few years, and for never complaining when I show up late for dinner. I am truly lucky to have you. iii Abstract SENSORIMOTOR INTEGRATION IN A SMALL MOTOR CIRCUIT Nicholas D. DeLong Advisor: Michael P. Nusbaum, Ph. D. Rhythmic motor patterns, which underlie behaviors such as mastication, respiration and locomotion, are generated by specialized neural circuits called central pattern generators (CPGs). Although CPGs can generate their rhythmic motor output in the absence of rhythmic input, these motor patterns are modified by rhythmic sensory feedback in vivo. Furthermore, although the importance of sensory feedback in shaping CPG output is well known, most systems lack the experimental access needed to elucidate the mechanisms underlying sensorimotor integration at the cellular and synaptic level. I am therefore examining this issue using the gastric mill CPG, a circuit which generates the rhythmic retraction and protraction motor activity that drives chewing by the teeth in the gastric mill compartment of the crustacean stomach. The gastric mill CPG is well defined and very accessible at the cellular level. Specifically, I am examining the mechanism by which the gastropyloric receptor (GPR), a phasically active proprioceptor, selectively prolongs one phase (retraction) of the gastric mill rhythm in the isolated nervous system when it is activated in a pattern that mimics its in vivo activity. I first demonstrate that GPR regulation of the iv gastric mill rhythm relies on its presynaptic inhibition of modulatory commissural neuron 1 (MCN1), a projection neuron that activates and drives this rhythm. I also demonstrate that the GPR inhibition of MCN1 regulates the gastric mill rhythm by selectively regulating peptidergic cotransmission by MCN1. Lastly, I demonstrate that a peptide hormone (crustacean cardioactive peptide) that only modestly modifies the gastric mill rhythm, strongly gates the GPR regulation of this rhythm. Mechanistically, it acts not by influencing GPR or MCN1, but by activating the same excitatory current in the CPG neuron LG (lateral gastric) that is activated by MCN1-released peptide. This novel gating mechanism reduces GPR control over the amplitude of this excitatory current in LG. Thus, I have identified specific cellular mechanisms by which (a) phase-specific regulation of an ongoing motor pattern by a sensory input is accomplished, and (b) hormonal modulation gates that sensory input. These events are likely to reflect comparable ones occurring in the larger and less accessible vertebrate CNS. v TABLE OF CONTENTS ACKNOWLEDGEMENTS ……………………………….…………………….. ii ABSTRACT ……………………………………………………………………… iv LIST OF TABLES ………………………………………………………………. vii LIST OF FIGURES ……………………………………………………………… viii CHAPTER 1: Introduction …………………………………………………….... 1 CHAPTER 2: Divergent Cotransmitter Actions Underlie Motor Pattern Activation by a Modulatory Projection Neuron ……………………………….. 32 CHAPTER 3: Proprioceptor Regulation of Motor Circuit Activity by Presynaptic Inhibition of a Modulatory Projection Neuron …………………… 92 CHAPTER 4: Presynaptic Inhibition Selectively Weakens Peptidergic Cotransmission in a Small Motor System …………………………………....... 152 CHAPTER 5: Parallel Regulation of a Modulator-Activated Current via Distinct Dynamics Underlies Co-Modulation of Motor Circuit Output ………. 209 CHAPTER 6: Hormonal Modulation of Sensorimotor Integration ………….. 266 CHAPTER 7: Conclusion ……………………………………………………….. 298 vi LIST OF TABLES Chapter 3: 1. Parameters used in dynamic clamp experiments .…………………… 103 2. Parameters used to incorporate GPR synapses into an existing model of the gastric mill rhythm ………………………………………… 104 Chapter 5: 1. The values used for IMI-MCN1 and IMI-CCAP in the computational model of the MCN1-elicited gastric mill rhythm ………………………………. 222 vii LIST OF FIGURES Chapter 1: 1. Schematic of the isolated STNS and the MCN1-elicited gastric mill rhythm ……………………………………………………………………. 3 2. The gastropyloric receptor (GPR) is a muscle stretch receptor neuron which regulates the gastric mill rhythm ……………………… 17 Chapter 2: 1. Selective stimulation of the projection neuron MCN1 elicits the gastric mill rhythm (GMR) in the isolated stomatogastric nervous system …………………………………………………………………... 43 2. MCN1 stimulation excites the gastric
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