Complex sensorimotor processing and neural plasticity in the Bengalese finch song system during vocal learning and error correction Público
Hoffmann, Lukas (2017)
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
About this Dissertation
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