Complex sensorimotor processing and neural plasticity in the Bengalese finch song system during vocal learning and error correction Open Access

Hoffmann, Lukas (2017)

Permanent URL: https://etd.library.emory.edu/concern/etds/ns064676b?locale=en
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Abstract

A major goal of neuroscience is to understand how the brain learns to change motor behavior in response to sensory input. Moreover, the ability to learn and adapt complex vocalizations is critical for communication. Although the brain uses auditory feedback to calibrate vocal performance, the neural substrates of vocal learning remain unclear. Therefore, to fully understand the mechanisms of vocal plasticity, we must determine how the brain learns to change vocal motor output using auditory feedback. This dissertation uses Bengalese finches (Lonchura striata), a vocal learning species, to answer three questions: the rules of generalization in adaptive error correction, whether dopamine in the learning-specialized basal ganglia nucleus Area X is required for vocal learning, and how dopamine affects Area X's neural activity.
We first showed that adaptive error correction of a vocal gesture (song syllable) in a sequence of gestures generalized to other gestures. Using miniaturized headphones, we perturbed pitch in real time as birds were singing a particular song syllable, which gradually caused compensatory pitch changes. Then, we measured generalization by quantifying pitch changes in non-perturbed syllables. We found that learning to change pitch on one gesture generalized to the same type of gesture produced in other contexts, learning generalized anti-adaptively to different gestures, and the magnitude of generalization decreased with increasing sequential distance. Next, we demonstrated that learning to change pitch depends on intact dopamine signaling in Area X, a basal ganglia nucleus critical for vocal learning. We drove pitch changes on single song syllables with negative reinforcement (aversive blasts of white noise when pitch was above or below a threshold). Finally, we performed preliminary experiments to investigate how partial loss of dopamine inputs to Area X affected its spontaneous and song-playback-evoked neural firing and local field potential. This is a first step towards investigating how dopamine guides neural firing changes during vocal learning. By finding that generalization depends on vocal gestures' type and position within a sequence and that intact dopamine signaling is required for negative-reinforcement-driven vocal learning, this dissertation lays a foundation for future studies into the rules of vocal learning and the role of dopamine.

Table of Contents

TABLE OF CONTENTS

LIST OF ABBREVIATIONS ........................................................................................................... 1

CHAPTER 1: INTRODUCTION AND LITERATURE REVIEW .................................................................. 4

1.1 Songbirds as a model system .............................................................................................. 5

1.2 Generalization of motor learning .......................................................................................... 6

1.3 Dopamine and vocal learning ............................................................................................... 7

1.4 The song system and Area X .............................................................................................. 12

1.5 Clinical significance ........................................................................................................... 17

CHAPTER 2: DISSERTATION OVERVIEW ...................................................................................... 20

2.1 Study 1: Quantify the behavioral rules for songbird vocal error correction .............................. 20

2.2 Study 2: Determine dopamine's contribution to songbird vocal learning ................................. 21

2.3 Study 3: Identify dopamine-dependent features of basal ganglia neural activity

.............................................................................................................................................. 22

CHAPTER 3: VOCAL GENERALIZATION DEPENDS ON GESTURE IDENTITY AND SEQUENCE

.............................................................................................................................................. 25

3.1 Abstract ............................................................................................................................ 25

3.2 Introduction ...................................................................................................................... 26

3.3 Materials and Methods ....................................................................................................... 27

3.4 Results ............................................................................................................................. 34

3.5 Discussion ......................................................................................................................... 44

CHAPTER 4: DOPAMINERGIC CONTRIBUTIONS TO VOCAL LEARNING ............................................... 51

4.1 Abstract ............................................................................................................................ 51

4.2 Introduction ...................................................................................................................... 51

4.3 Materials and Methods ....................................................................................................... 53

4.4 Results .............................................................................................................................. 69

4.5 Discussion ......................................................................................................................... 80

CHAPTER 5: DOPAMINE-DEPENDENT FEATURES OF BASAL GANGLIA NEURAL ACTIVITY

............................................................................................................................................... 86

5.1 Introduction ....................................................................................................................... 86

5.2 Materials and Methods ........................................................................................................ 89

5.3 Results .............................................................................................................................. 98

5.4 Discussion ....................................................................................................................... 107

CHAPTER 6: CONCLUSIONS AND FUTURE DIRECTIONS ................................................................. 111

6.1 Conclusions ...................................................................................................................... 111

6.2 Future directions beyond Study 1 ....................................................................................... 115

6.3 Future directions beyond Study 2 ....................................................................................... 118

6.4 Future directions beyond Study 3 ....................................................................................... 121

REFERENCES .......................................................................................................................... 125

LIST OF FIGURES AND TABLES

Table 1: Injection parameters for 6-OHDA-lesioned birds .......................................................... 60

Table 2: Injection parameters for sham-lesioned birds .............................................................. 61

Table 3: Acute electrophysiology dataset size .......................................................................... 98

Figure 1.1: Song syllables and the song system ........................................................................ 10

Figure 1.2: Comparison of mammalian BG and Area X circuitry ................................................... 11

Figure 3.1: Technique for manipulating auditory feedback during individual vocal gestures

.............................................................................................................................................. 28

Figure 3.2: Example of pitch-shift learning on a targeted vocal gesture and generalization to

other contexts ........................................................................................................................ 35

Figure 3.3: Pitch-shift learning on targeted vocal gestures generalizes to other gestures .............

.............................................................................................................................................. 38

Figure 3.4: Two patterns of generalization in vocal learning ........................................................ 39

Figure 3.5: A vocal gesture's acoustic similarity to targeted gesture does not predict

learning transfer ..................................................................................................................... 42

Figure 3.6: Transfer of learning across vocal gestures in a stereotyped sequence depends on

sequential distance ................................................................................................................. 43

Figure 4.1: A song-specific BG nucleus receives strong DAergic input .......................................... 53

Figure 4.2: Lesions of DAergic inputs to Area X .......................................................................... 63

Figure 4.3: Alternate method of quantifying loss of TH label ........................................................ 71

Figure 4.4: Concentrations of DA and NE in 6-OHDA- and sham-lesioned tissue ............................ 73

Figure 4.5: 6-OHDA injections do not lead to neuron loss within Area X ........................................ 74

Figure 4.6: Removal of DA inputs to Area X does not degrade song quantity or quality .................. 75

Figure 4.7: Removal of DA inputs to Area X impairs reinforcement-driven vocal learning ...............

.............................................................................................................................................. 78

Figure 4.8: Removal of DA inputs to Area X does not impair pitch restoration ................................ 81

Figure 5.1: Histological verification of electrode placement in a sham lesioned section

stained for TH ......................................................................................................................... 97

Figure 5.2: Example Area X pallidal units showing slightly higher firing rates during

playback stimuli in both sham- and 6-OHDA-lesioned Area X ...................................................... 99

Figure 5.3: Responses to playback stimuli for Area X pallidal units do not differ between

sham- and 6-OHDA-lesioned Area X ........................................................................................ 100

Figure 5.4: Spontaneous LFP beta power does not differ between sham- and 6-OHDA-

lesioned Area X ...................................................................................................................... 104

Figure 5.5: There is a trend towards slightly increased beta power during playback stimuli

in sham- and 6-OHDA-lesioned Area X ..................................................................................... 106

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