Anatomy and physiology of a vocal learning circuit in the Bengalese finch Pubblico

Abstract

The basal ganglia are hypothesized to be involved in several aspects of motor control, including control of precise movement kinematics, motor sequencing, and motor learning. Chapter 1 of this dissertation provides a broad introduction to the structure and hypothesized functions of the basal ganglia, and discusses the strengths of the songbird as a model organism for studying the role of the basal ganglia in motor control and motor learning. In Chapter 2 we present new data on the neuroanatomy of the Bengalese finch dopamine system, a large population of putatively non-dopaminergic neurons spatially intermingled with dopaminergic neurons in the ventral tegmental area, the substantia nigra pars compacta, and the periaqueductal gray. In Chapter 3, we detail the results of in vivo electrophysiology experiments in Area X of the Bengalese finch. We first demonstrate that neurons in Area X of the Bengalese finch can be separated into striatal and pallidal subclasses. We next report for the first time that Area X single unit activity reflects information about song sequencing and phonology. Intriguingly, we find robust sequence representations and weak pitch representations. The implications of the results from Chapters 2 and 3, as well as future experiments, are then discussed at length in Chapter 4.

Table of Contents

1 Background and literature review: The basal ganglia, motor control,

and motor learning 1

1.1 Organizational principles of the basal ganglia . . . . . . . . . . . . . . 2

1.1.1 The direct and indirect pathways . . . . . . . . . . . . . . . . 2

1.1.2 The limbic-to-motor spiral . . . . . . . . . . . . . . . . . . . . 6

1.2 Songbirds as a model system for motor control and motor learning . . 8

1.2.1 The song-specialized basal ganglia nucleus Area X . . . . . . . 10

1.2.2 Relationship between songbird pallium and mammalian cortex 12

1.3 What do the basal ganglia contribute to motor control? . . . . . . . . 14

1.3.1 Insights from movement disorders . . . . . . . . . . . . . . . . 14

1.3.2 Hypotheses of basal ganglia motor function . . . . . . . . . . . 18

1.3.3 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23

1.4 Motor learning: the role of dopamine . . . . . . . . . . . . . . . . . . 24

1.4.1 Dopamine and associative learning: Computational hypotheses 25

1.4.2 How do dopaminergic signals drive motor learning? . . . . . . 29

1.4.3 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41

1.5 Dissertation Overview . . . . . . . . . . . . . . . . . . . . . . . . . . 42

2 Organization of the dopaminergic projections to a song-specialized

region of the basal ganglia in the Bengalese finch 43

2.1 Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43

2.2 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44

2.3 Materials and Methods . . . . . . . . . . . . . . . . . . . . . . . . . . 46

2.3.1 Subjects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 46

2.3.2 Tracer injections . . . . . . . . . . . . . . . . . . . . . . . . . 48

2.3.3 Histology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48

2.3.4 Microscopy, digital photography, image processing, and quanti

cation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 50

2.4 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51

2.4.1 Putative TH(-) neurons in primarily dopamine structures projecting

to Area X . . . . . . . . . . . . . . . . . . . . . . . . . 53

2.4.2 Distinct populations of dopamine neurons project to RA and X 55

2.5 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57

2.5.1 Identification of putative non-dopaminergic neurons projecting

to Area X . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57

2.5.2 What is the function of VTA and SNc non-dopaminergic projection

neurons? . . . . . . . . . . . . . . . . . . . . . . . . . . 60

2.5.3 Separation of dopaminergic populations projecting to song-specialized

basal ganglia and motor cortical nuclei . . . . . . . . . . . . . 61

3 Neural activity in a song-specialized basal ganglia nucleus re

ects

syllable sequencing and phonology 63

3.1 Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63

3.2 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64

3.3 Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68

3.3.1 Subjects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68

3.3.2 Microdrive implantation and data collection . . . . . . . . . . 68

3.3.3 Neural data analysis . . . . . . . . . . . . . . . . . . . . . . . 70

3.3.4 Behavioral analysis . . . . . . . . . . . . . . . . . . . . . . . . 71

3.3.5 Neuron-behavior correlations and significance testing . . . . . 72

3.4 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 74

3.4.1 Cell type identification . . . . . . . . . . . . . . . . . . . . . . 74

3.4.2 Area X neural activity varies based on sequential context . . . 79

3.4.3 Weak correlations between Area X activity and pitch . . . . . 81

3.5 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 84

3.5.1 Comparisons between the songbird basal ganglia to the songbird

vocal motor cortex . . . . . . . . . . . . . . . . . . . . . . 85

3.5.2 Is Area X activity involved in online acoustic control? . . . . . 86

3.5.3 How Area X neural activity could contribute to learning . . . 88

3.5.4 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91

4 Future Directions 92

4.1 Which neurotransmitters are used by TH- Area X projectors? . . . . 92

4.2 How does dopamine depletion affect neural activity in Area X? . . . . 94

4.3 What is the timescale of Area X neuron-behavior correlations? . . . . 97

4.4 What is the role of Area X neural activity in vocal learning? . . . . . 100

Bibliography 103

About this Dissertation

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School	Laney Graduate School
Department	Biological and Biomedical Sciences
Subfield / Discipline	Neuroscience
Degree	Ph.D.
Submission	Dissertation
Language	English
Research Field	Nanoscience
Parola chiave	motor control neuroanatomy neurophysiology songbird dopamine basal ganglia
Committee Chair / Thesis Advisor	Samuel Sober, Emory University
Committee Members	Michael Treadway, Emory University Dieter Jaeger, Emory University Jesse Goldberg, Cornell University Yoland Smith, Emory University

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