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Behavioral and Neuromodulatory Responses to Emotional BEHAVIORAL AND NEUROMODULATORY RESPONSES TO EMOTIONAL VOCALIZATIONS IN MICE A dissertation submitted to Kent State University in cooperation with Northeast Ohio Medical University in partial fulfillment of the requirements for the degree of Doctor of Philosophy by Zahra Ghasemahmad December 2020 © Copyright All rights reserve Dissertation written by Zahra Ghasemahmad B.Sc., Tehran University of Medical Sciences, 2005 M.Sc., Tehran University of Medical Sciences, 2009 Ph.D., Kent State University, 2020 Approved by , Chair, Doctoral Dissertation Committee Dr. Jeffrey J. Wenstrup , Members, Doctoral Dissertation Committee Dr. Brett R. Schofield , Dr. Merri J. Rosen , Dr. Rebecca Z. German , Dr. Karin G. Coifman Accepted by , Director, School of Biomedical Sciences Dr. Ernest Freeman , Interim Dean, College of Arts and Sciences Dr. Mandy Munro-Stasiuk Table of Contents Table of Contents ........................................................................................................ iii List of Figures and Tables ............................................................................................. vi Acknowledgments ..................................................................................................... viii CHAPTER I INTRODUCTION .......................................................................................... 1 Vocalization as a tool for emotional expression .............................................................................. 2 Vocal communication of emotions in mice ..................................................................................... 4 The effect of vocalizations on the receiver ...................................................................................... 7 Amygdala and emotional processing ............................................................................................... 9 Amygdala role in processing acoustic communication .................................................................. 11 Neuromodulation of auditory and emotional processing ............................................................. 14 Summary of specific aims of the dissertation ................................................................................ 17 CHAPTER II MATERIALS AND METHODS ..................................................................... 20 Animals........................................................................................................................................... 20 Acoustic methods .......................................................................................................................... 21 Vocalization recording ................................................................................................................... 21 Mating vocalization analysis .......................................................................................................... 22 Vocalization playback ..................................................................................................................... 26 Behavioral methods ....................................................................................................................... 28 iii Analysis of mating behaviors during vocal recordings .................................................................. 28 Vocal playback in behavioral experiment ...................................................................................... 29 Procedures related to microdialysis .............................................................................................. 32 Surgery ........................................................................................................................................... 32 Microdialysis .................................................................................................................................. 32 Verification of recording location .................................................................................................. 36 Statistical methods ........................................................................................................................ 37 CHAPTER III RESULTS .................................................................................................. 40 Experiment 1: Identifying acoustic features associated with intense mating interactions ........... 42 Experiment 2: Emotional vocalizations result in behavioral changes in mice ............................... 56 Experiment 3: Context- and state-dependent release of neuromodulators in the BLA ................ 62 CHAPTER IV DISCUSSION ............................................................................................ 73 Internal state modulates mouse vocal behavior ........................................................................... 74 Acoustic features of emotional expression in mice during mating interactions ........................... 75 Receiver behaviors are influenced by social vocalizations ............................................................ 80 Behavioral changes in male and female mice in response to restraint vocalizations ................... 82 Male and female behavioral responses to mating vocalizations ................................................... 86 Neuromodulator release in the basolateral amygdala in response to affective vocalizations ..... 88 Context-dependent modulation of sensory processing in BLA by acetylcholine and dopamine .. 90 Acetylcholine and hormonal changes ............................................................................................ 95 iv Other neuromodulators affecting valence processing in the BLA ................................................. 95 Summary and Conclusion .............................................................................................................. 96 General significance and future directions .................................................................................... 98 REFRENCES ................................................................................................................100 v List of Figures and Tables Figure 1.1 Four categories of vocalizations emitted by mice ............................................. 5 Figure 1.2 General connections of the amygdala. ........................................................... 10 Figure 1.3 An auditory-centric view of connections of the amygdala ............................. 12 Figure 2.1 Sample spectrogram of four categories of syllables emitted by mice ............ 24 Figure 2.2 Structure of stimuli in playback experiments. ................................................ 27 Table 2.1. Behaviors identified for categorizing lower and higher intensity of mating. .. 29 Figure 2. 3. Experimental design for behavioral experiments. ........................................ 30 Table 2.2. Behaviors analyzed during playback of mating and restraint vocalizations. ... 31 Figure 2.4 Experimental design for microdialysis. ........................................................... 34 Figure 3.1 Vocalizations are modulated by the intensity of mating interactions. ........... 44 Figure 3.2 Syllable composition and complexity change with mating intensity .............. 47 Figure 3.3 Inter-syllable-interval (ISI) decreases with increased intensity of mating ...... 49 Figure 3.4 Syllable duration increases with increased intensity of mating interaction .... 50 Figure 3.5 Peak-to-peak amplitude of emitted syllables increases with harmonicity ...... 52 Figure 3.6 Minimum frequency of syllables..................................................................... 53 Fig. 3.7 Spectrogram snapshot of some of the vocal sequences ..................................... 55 Figure 3.8 Self-grooming behavior in male and female mice. ......................................... 57 Figure 3.9 Abrupt attending ............................................................................................ 58 Figure 3.10 Stretch-attend posture in male and female mice ......................................... 59 Figure 3.11 Context-dependent modulation of flinching behavior ................................. 60 vi Figure 3.12 Pull-back posture.. ........................................................................................ 61 Figure 3.13 Microdialysis probe location. ........................................................................ 64 Figure 3.14 Mating and restraint vocalizations differentially change ACH and DA. ......... 66 Figure 3.15 Serotonergic activity in the BLA of male mice is not context dependent. .... 67 Figure 3.16 Patterns of ACH, but not DA release in the BLA of female mice.. ................. 68 Figure 3.17 Estrous- but not sex-dependent release pattern of ACH and DA. ................. 71 Figure 4.1 Proposed model for neuromodulation of salient vocalization.. ...................... 92 vii Acknowledgments This work would not have been possible without the unwavering guidance, encouragement, and support of the vast number of individuals. To all who have been on my side for this long and difficult journey, I am sincerely thankful. My special gratitude goes to my advisor, Dr. Jeff Wenstrup. From the moment you welcomed me to your lab despite my lack of neuroscience knowledge, and through your constant encouragement in testing my ideas, you taught me how not to be afraid of taking risks. I owe my professional growth in the last several years to you, who always supported inquisitiveness, creativity, and constructive idea exchange
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