NEURAL DISCRIMINATION OF COMMUNICATION SIGNALS IN THE AVIAN AUDITORY SYSTEM: ROLES OF SEX, ESTROGENS, AND SOCIAL EXPERIENCE by KATHLEEN MARIE YODER A dissertation submitted to the Graduate School-New Brunswick Rutgers, The State University of New Jersey In partial fulfillment of the requirement for the degree of Doctor of Philosophy Graduate Program in Psychology Written under the direction of David S. Vicario, PhD. And approved by _______________________________ _______________________________ _______________________________ _______________________________ New Brunswick, New Jersey May 2012 ABSTRACT OF THE DISSERTATION Neural Discrimination of Vocal Communication Signals in the Avian Auditory System: Roles of Sex, Estrogens, and Social Experience By KATHLEEN MARIE YODER Dissertation Director: David S. Vicario Songs are learned in songbirds, much as speech is acquired in human infants, and serve social and reproductive functions. In most songbirds studied to date, males produce learned vocalizations while females do not and the male brain contains a more developed forebrain vocal control pathway. Males use song both in interactions with other males and in courtship displays to varying degrees in different species. In the zebra finch, the male sings to court females, who do not sing, but use this signal in the process of mate selection. Thus this species provides a model of sexual dimorphism in the use of song. An avian forebrain auditory area, NCM, seems to be specialized to discriminate and remember the unique songs of other individuals, through a process of stimulus-specific adaptation, but sex differences in NCM function have not been ii described. The present study compares neurophysiological responses recorded in NCM of adult male and female zebra finches that were either raised in the general aviary by their parents, or reared in individual isolation with an artificial song tutor. Extra-cellular multi-unit recordings were made at multiple sites bilaterally in NCM of awake, restrained adult birds during song playback to assess auditory responses, stimulus- specific adaptation, preference for conspecific song, and song recognition memory for the tutor song as well as songs heard in adulthood. In a subset of these birds, estradiol levels were manipulated pharmacologically to compare the role of this hormone – which is known to be synthesized in the brain - in auditory responses in the two sexes. The results in untreated birds show differences between males and females in adaptation to song playback in NCM, although absolute responses do not differ between the sexes. Estradiol depletion in both males and females interfered with the memory for recently heard songs, although it had no clear effect on the memory for the tutor song heard in development. In addition, in females, but not males, estradiol depletion disrupted the typical neural response bias for conspecific song. These results are consistent with evolving ideas about the dynamic effects of sex steroids on sensory brain function beyond the established role of these hormones in reproductive behavior. The observations further suggest how, in females in the sexually receptive state, estradiol production in addition to its production in the brain itself, may influence the way the songs of potential suitors are discriminated, remembered and compared in the brain, thus contributing to the process of mate selection. iii Acknowledgments First, I would like to thank my advisor for his support and encouragement throughout the past few years. Without it I more than likely would not have stayed on to finish my degree. I would also like to thank my committee members for their guidance. I thank Mimi Phan, who contributed the data from experiments in which untreated animals were compared and on whose work the developmental experiments were based. I am indebted to Dr. Luke Remage-Healey for helping me to FINALLY get a reliable measure of estradiol in zebra finch tissue. I am especially grateful to members of my lab, who have both assisted me in labwork and kept me laughing through the roughest of times, especially Manda Pierce, Utsav Aiya, and Arielle Urman. I consider myself truly lucky to have met Mike Tomasini in these last few years of school. His love, understanding, and patience continue to amaze me and are what I thought one could only wish for in a significant other. Finally, I dedicate this dissertation to my mother, who introduced me to the world of experimental psychology as she was completing her Masters program, taking my brother and me to feed the rats through many a snowstorm. Love you Mom. iv Table of Contents Title Page ........................................................................................................................................... i Abstract ............................................................................................................................................ ii Acknowledgements......................................................................................................................... iv Table of Contents ............................................................................................................................. v List of Figures .................................................................................................................................. vi Chapter 1: Introduction and Background ........................................................................................ 1 Chapter 2: General Methods Used for All Experiments ................................................................ 20 Chapter 3: Effects of Sex on Song Processing in NCM ................................................................... 38 Chapter 4: Effects of Estradiol Manipulation on Song Processing in NCM .................................... 52 Chapter 5: Examination of Tutor Song Memory in Box-reared Birds ............................................ 71 Chapter 6: Discrimination of Conspecific Song .............................................................................. 77 Chapter 7: Conclusions and General Discussion of Results ........................................................... 86 References ................................................................................................................................... 108 v List of Figures Figure 1.1: Structure of the Songbird Brain ..................................................................................... 5 Figure 1.2: Song Selectivity in NCM: Electrophysiological Measures .............................................. 6 Figure 1.3: Song Selectivity in NCM: IEG Responses ........................................................................ 7 Figure 1.4: NCM: Stimulus Specific Adaptation .............................................................................. 8 Figure 1.5: IEG Response to Tutor Song in Females ...................................................................... 10 Figure 1.6: Sex Differences in Song Discrimination Tasks ............................................................ 13 Figure 1.7: Discrimination of Calls: Sex Differences ...................................................................... 13 Figure 1.8: Potential Sex Differences in NCM Response Characteristics ....................................... 14 Figure 2.1: Recording Multiunit Activity in NCM .......................................................................... 24 Figure 2.2: Calculation of the Familiarity Index ............................................................................. 25 Figure 2.3: Example: Cumulative Frequency Distribution of Familiarity Indices ........................... 26 Figure 2.4: Example: Cumulative Frequency Distribution of FI, exclusions ................................... 27 Figure 2.5: Box-Tutoring Experimental Design .............................................................................. 30 Figure 2.6: Fadrozole effects on Brain Estradiol Levels ................................................................. 34 Figure 2.7: Example Lesion in NCM ............................................................................................... 36 Figure 3.1: Overview of Subjects Included in All Experiments ...................................................... 40 Figure 3.2: Response Magnitude: Male v Females ........................................................................ 41 Figure 3.3: Response Magnitude: Male v Female, Aviary .............................................................. 42 Figure 3.4: Response Magnitude: Male v Female, Box-tutored .................................................... 42 Figure 3.5: Adaptation Rate: Male v Female ................................................................................. 43 Figure 3.6: Adaptation Rate: Male v Female, Aviary ..................................................................... 44 Figure 3.7: Adaptation Rate: Male v Female, Box-tutored ............................................................ 44 Figure 3.8: Familiarity Index: Male v Female ................................................................................. 45 Figure 3.9: Familiarity Index: Male v Female, Aviary ..................................................................... 46 Figure 3.10: Familiarity Index: Male v Female, Box-tutored.......................................................... 46 Figure 3.11: Response Magnitude: Aviary v Box-tutored, Male .................................................... 47 Figure