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Social Context-Appropriate Vocal Communication and Opioids in Male European

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Social Context-Appropriate Vocal Communication and Opioids in Male European Social Context-Appropriate Vocal Communication and Opioids in male European Starlings (Sturnus vulgaris) By Cynthia A. Kelm-Nelson A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy (Zoology) at the UNIVERSITY OF WISCONSIN-MADISON 2012 Date of final oral examination: 12/05/2012 The dissertation is approved by the following members of the Final Oral Committee: Lauren V. Riters, Professor, Zoology Catherine J. Auger, Assistant Professor, Psychology Craig W. Berridge, Professor, Psychology Stephen C. Gammie, Professor, Zoology Charles T. Snowdon, Professor, Psychology ©Copyright by Cynthia A. Kelm-Nelson 2012 All Rights Reserved i Acknowledgment There are many people who deserve thanks for their varied contributions to my dissertation. I am grateful to my academic advisor and role model, Lauren Riters, for her acceptance, encouragement, mentorship, and friendship. I would also like to offer my appreciation to the members of my dissertation committee: Dr. Cathy Auger, Dr. Craig Berridge, Dr. Stephen Gammie and Dr. Charles Snowdon. They have generously given their time and expertise as well as valuable guidance and direction to better my scientific work. It has been a privilege to work with such scientists. I would also like to thank the members of the Riters’ lab (both past and present): Sarah Heimovics, Sarah Jane Alger, Ben Pawlisch, Jesse Ellis, and Melissa Cordes. I have been fortunate to interact with a variety of exceptional graduate students. And, many, many thanks to my friend and research collaborator, Sharon Stevenson. There have been many undergraduates who have helped assist the work descript in this dissertation. Those in need of special acknowledgment for technical work include: Griff Gessay and Rachel McCormick. The animal care staff in Birge Hall is exceptional and I must thank Kate Skogen and Chris Elliot for animal care. I also would like to thank Bill Feeny for his artistry and creation of conference posters, as well as the zoology department staff. Lastly, I must thank my family. My parents and my brother Pete have always been so loving and supportive throughout my many years of education. And, I must thank my husband Jim for providing love, encouragement, proof-reading and much patience. ii Table of Contents Acknowledgment ............................................................................................................................. i Table of Contents ............................................................................................................................ ii Abstract .......................................................................................................................................... iii Chapter I: General Introduction .................................................................................................... 1 Chapter II: Context-Dependent Links between Song Production and Opioid-Mediated Analgesia in Male European Starlings (Sturnus vulgaris) ............................................................ 24 Chapter III: Curvilinear relationships between mu-opioid receptor densities and undirected song in male European starlings (Sturnus vulgaris) ..................................................................... 54 Chapter IV: Mu-opioid receptor densities are depleted in regions implicated in agonistic and sexual behavior in male European starlings (Sturnus vulgaris) defending nest sites and courting females .......................................................................................................................................... 81 Chapter V: Modulation of male song by naloxone in the medial preoptic nucleus .................. 116 Chapter VI: Conclusions and General Discussion .................................................................... 138 iii Social Context-Appropriate Vocal Communication and Opioids in male European Starlings (Sturnus vulgaris) Cynthia A. Kelm-Nelson Under the supervision of Professor Lauren V. Riters At the University of Wisconsin-Madison Abstract Vocal communication is a necessity for successful social relationships and interactions as well as survival and reproductive success. The neural regulation of vocal behavior has been well studied using songbird model systems; yet, less is known about the neurochemical mechanisms regulating context-appropriate vocal behaviors. Endogenous opioid neuropeptides represent likely candidate modulators of vocal behavior as they are involved in a variety of social behaviors, including vocal behavior. The unifying element of this dissertation evaluates the role of mu-opioid receptors in vocal communication produced within distinct social contexts. Starlings use song to immediately influence a conspecific (directed) and also sing spontaneously at high rates in large flocks (undirected). Past work suggests that opioids play an important role in regulating song but that the role may differ depending upon the social context. In this dissertation I further explored this possibility. Using an indirect assay of opioid-mediated analgesia my first chapter supports the possibility that opioids may facilitate undirected song but inhibit directed song. In order to determine where in the brain opioids may act to influence song in distinct contexts and to further evaluate relationships between receptor densities within individuals, I examined relationships between immunolabeling for the mu-opioid receptor and iv both directed and undirected singing behavior. For undirected song, data showed links between low densities of mu-opioid receptors in the medial preoptic nucleus (and other areas in which mu receptors induce analgesia and regulate vocal communication) and both low and high rates of undirected singing behavior, whereas high receptor densities were associated with intermediate rates of undirected song. In males singing directed song, there was significantly higher mu- opioid immunolabeling in several brain regions, including the medial preoptic nucleus in males singing at low compared to high rates. This suggests that receptors may be acting to inhibit vocal communication in males singing low rates of directed song. This prediction was further supported by a site-specific pharmacology study that demonstrated that blocking receptors in the medial preoptic nucleus in low singing males stimulated directed song. Together, the results of this dissertation provide new insight into where and how opioids regulate context-appropriate vocal communication. 1 Chapter I: General Introduction For humans and multiple vertebrate species, vocal communication is a necessity for successful social relationships. Multiple mental health disorders in humans, including depression, anxiety, post-traumatic stress disorder and pervasive developmental disorders, are characterized by deficits in social communication, social withdrawal, or inappropriate responses to social signals [1]. For instance, Autism Spectrum Disorders (ASDs) are a complex class of pervasive developmental brain disorders diagnosed using an assessment of a triad of impairments: social interaction (lack of spontaneous seeking to share with others, failure to develop peer relationships), social communication (delay or lack of development of spoken language), and repetitive patterns of behavior (stereotyped or repetitive motor mannerisms) [2]. These deficits are often times context specific (i.e., communication deficits are seen in specific situations) [1,3,4] and may lead to social exclusion and / or difficulties maintaining relationships, deficits that persist into adulthood. Communication through the use of vocalizations is essential in both human and non-human animals to convey various forms of information. And, non-human models are an excellent way of studying the neural mechanisms of socially appropriate behavior where the methodology can later be translated to human research and potentially lead to novel clinical treatments and therapeutic (i.e. druggable) targets. Socially appropriate behavior is critical for successful social interactions within the animal kingdom and may dictate survival and reproductive success. Vocal communication is one way members of the same species convey information to one another, and it is critical that vocal communication be regulated and fine-tuned in response to the appropriate stimuli [5]. For example, in vervet monkeys (Cercopithecus aethiops) different acoustic alarm calls signal 2 predator danger and are specific to whether the danger is above or below the treeline [6]. Accurate signals must be made so the vervet population takes the proper actions (fleeing to the trees, looking above for the threat of eagles or looking down for snakes). Across species, vocal adjustments must be made to match the social context and what is socially appropriate for one individual is not necessarily appropriate for another. An example from human behavior: it may be appropriate to cheer raucously at a sporting event whereas it is inappropriate to do so in the quiet study section of the library. Songbirds are well known for their ability to regulate and fine-tune vocal behavior in response to specific social stimuli within functionally distinct social contexts [7] and, historically, both the function and neural regulation of vocal communication have been well studied using this model system [8]. However, less is known about the neurochemical mechanisms regulating context- appropriate vocal behavior. Recent evidence suggests that opioid neuropeptides
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