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University of California, San Diego UC San Diego UC San Diego Electronic Theses and Dissertations Title Neural correlates of conspecific vocal recognition in the caudomedial nidopallium Permalink https://escholarship.org/uc/item/4qq4d0bc Author Thompson, Jason Venard Publication Date 2010 Peer reviewed|Thesis/dissertation eScholarship.org Powered by the California Digital Library University of California UNIVERSITY OF CALIFORNIA, SAN DIEGO Neural Correlates of Conspecific Vocal Recognition in the Caudomedial Nidopallium A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Neurosciences by Jason Venard Thompson Committee in charge: Professor Timothy Gentner, Chair Professor Henry Abarbanel, Co-Chair Professor Stephan Anagnostaras Professor Andrea Chiba Professor Rich Krauzlis 2010 The Dissertation of Jason Venard Thompson is approved, and it is acceptable in quality and form for publication on microfilm and electronically: Co-Chair Chair University of California, San Diego 2010 iii TABLE OF CONTENTS Signature Page…………………………………………………………………………………………………….iii Table of Contents………………………………………………………………………………………………...iv List of Figures……………………………………………………………………………………………………..vi List of Tables……………………………………………………………………………………………………...vii Acknowledgements……………………………………………………………………………………….......viii Vita…………………………………………………………………………………………………….........................x Abstract………………………………………………………………………………………………………………xi I. Introduction……………………………………………………………………………………………………...1 Vocal Recognition……………………………………………………………………………………...1 Songbirds………………………………………………………………………………………………….2 European starling song behavior………………………………………………........................5 Songbird auditory system………………………………………………………….......................8 Learning and the songbird auditory system……………………………………………...13 Mammalian auditory system……………………………………………………………………15 Learning and the mammalian auditory system…………………………………………19 Mechanisms of sensory plasticity……………………………………………………………..23 Inhibition and stimulus selectivity……………………………………………………………25 References……………………………………………………………………….................................27 II. Song recognition learning and stimulus-specific weakening of neural responses in the avian auditory forebrain……………………………………………………….41 Abstract……………………………………………………………………………………....................41 Introduction……………………………………………………………………………………………42 Methods……………………………………………………………………………………....................44 Results………………………………………………………………………………………...................53 Discussion…………………………………………………………………………………...................77 Supplementary Material.……………………………………………………………...................85 References………………………………………………………………………………………………94 III. Local inhibition inactivates learning-related plasticity in the songbird auditory forebrain…………………………………………………………………………100 Abstract………………………………………………………………………………………………...100 iv Introduction………………………………………………………………………………………….101 Methods………………………………………………………………………………………………..103 Results………………………………………………………………………………………………….110 Discussion……………………………………………………………………………………………..130 References…………………………………………………………………………………………….136 IV. Conclusion…………………………………………………………………………………………………..141 References…………………………………………………………………………………………….153 v LIST OF FIGURES Chapter 2: Figure 2.1 Auditory Diagram and song recognition training………….…….................54 Figure 2.2 Recording location………………….…………………………………………………….56 Figure 2.3 Preference for unfamiliar songs in single neurons………………………….58 Figure 2.4 Preference for unfamiliar songs in single neurons………………………….60 Figure 2.5 Preference for unfamiliar songs in NCM neurons.……………………. …….63 Figure 2.6 Song exposure does not cause weakened responses to learned songs in NCM.…………………………………………………………………..68 Figure 2.7 No evidence for firing rate adaptation during recording experiments………………………………………………………………….70 Figure 2.8 Motif-level contributions to song-level effects………………………………..75 Figure 2.S1 Comparison of NCM plasticity for Male and Female Starlings..………..90 Chapter 3: Figure 3.1 Song Recognition Training…………………………………………………………..111 Figure 3.2 Blocking GABA-A inhibition increases firing rates………………………...113 Figure 3.3 Blocking Inhibition Enhances Plasticity in Ventral NCM………………..115 Figure 3.4 Blocking Inhibition uncovers a preference for learned songs in dorsal NCM……………………………………………………………………118 Figure 3.5 Variable Release from Inhibition throughout songs………………………121 Figure 3.6 Blocking inhibition decreases selectivity……………………………………...124 Figure 3.7 Blocking inhibition uncovers robust responses…………………………….126 Figure 3.8 Effects of blocking inhibition on MID receptive fields……………………129 vi LIST OF TABLES Chapter 2: Table 2.S1 Behavioral performance for last 1000 trials…………………………………...91 Table 2.S2 Different threshold for spontaneous activity in ventral NCM motif analysis………………………………………………………..92 vii ACKNOWLEDGEMENTS I would like to acknowledge Professor Timothy Gentner for his support as my advisor and mentor. Tim was a constant source of excitement about data and science. I appreciate that Tim truly treats his students as collaborators. I’ve learned a lot from Tim about designing experiments, thinking about data and writing about science. This work would not have been possible without his guidance and support. I would also like to acknowledge the fellow graduate students in the lab: Micah Bregman, Emily Caporello, James Jeanne and Dan Knudsen. I was fortunate to be in a lab with some of the smartest people I’ve ever met. They contributed to my scientific development and made working in the lab a lot of fun. I owe a special thanks to James Jeanne and Dan Knudsen who I collaborated with on papers. I would like to thank my committee for their continued support and guidance, Drs. Henry Abarbanel, Stephan Anagnostaras,, Andrea Chiba and Rich Krauzlis. Finally, I am grateful to my family and especially my parents for their emotional support while I was at UCSD. I am particularly grateful to my partner Hope Williams. I probably would have given up long ago without her help and support. Chapter 2, in full, is a reprint of the material as it appears in The Journal of Neurophysiology 2010. Thompson, Jason V.; Gentner, Timothy Q., The American Physiological Society, 2010; doi:10.1152/jn.00885.2009 and is used with viii permission from The American Physiological Society. The dissertation author was the primary investigator and author of this paper. Chapter 3, in full, is being prepared for submission for publication of the material. Thompson, Jason V.; Jeanne, James M.; Gentner, Timothy Q. The dissertation author was the primary investigator and author of this material. ix VITA 2005 Bachelors of Science, University of Oklahoma 2006 Teaching Assistant, Department of Psychology University of California, San Diego 2009 Teaching Assistant, School of Medicine University of California, San Diego 2005-2010 Research Assistant, University of California, San Diego 2010 Doctor of Philosophy, University of California, San Diego PUBLICATIONS Thompson, J.V., Jeanne, J.M. and Gentner, T.Q. (in preparation) Local inhibition inactivates learning-related plasticity in the songbird auditory forebrain. Jeanne, J.M., Thompson, J.V., Sharpee, T.O. and Gentner, T.Q. (submitted) Learning enhances auditory information processing in a hierarchical neural circuit. Knudsen, D. P., Thompson, J.V. and Gentner, T.Q. (in press) Distributed recognition of natural songs by European starlings. Learning and Motivation. Thompson, J.V. and Gentner, T. Q. (2010) Song Recognition Learning and Stimulus- Specific Weakening of Responses in the Avian Auditory Forebrain. Journal of Neurophysiology 103, 1785-1797. Thompson, J.V., Sullivan, R.M. and Wilson, D.A. (2008). Developmental emergence of fear learning corresponds with changes in amygdala synaptic plasticity. Brain Research 1200, 58-65. Thompson, J.V., Best, A.R. and Wilson, D.A. (2005). Ontogeny of cortical synaptic depression underlying olfactory sensory gating in the rat. Developmental Brain Research 158, 107-110. Best, A.R., Thompson, J.V., Fletcher, M.L. and Wilson, D.A. (2005). Cortical metabotropic glutamate receptors contribute to habituation of a simple odor- evoked behavior. The Journal of Neuroscience 25, 2513-2517. x ABSTRACT OF THE DISSERTATION Neural Correlates of Conspecific Vocal Recognition in the Caudomedial Nidopallium by Jason Venard Thompson Doctor of Philosophy in Neurosciences University of California, San Diego, 2010 Professor Timothy Gentner, Chair Professor Henry Abarbanel, Co-Chair Vocal recognition is important for communication in several species, including humans. Songbirds learn to recognize the vocalizations of conspecifics for social behaviors such as mate attraction and territorial defense. We examined the role of the caudomedial nidopallium (NCM), a forebrain region analogous to secondary auditory cortices, in song recognition. We trained European starlings to recognize conspecific songs and recorded the activity of single neurons in NCM. In ventral NCM, neurons responded stronger to unfamiliar songs than to songs that starlings had learned to recognize. While in dorsal NCM, neurons responded xi similarly to learned and unfamiliar songs. In a second experiment we trained starlings to recognize songs and exposed them to an equal number of songs passively. Recognition learning weakened the firing rates to the learned songs, while passively hearing songs had no effect, indicating that the response suppression in NCM requires associative learning. These results show that song recognition learning weakens the responses to learned
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