Shared mechanisms of auditory and non-auditory vocal learning in the songbird brain Público

Abstract

The brain uses sensory feedback to guide changes in motor output. This process, known as sensorimotor learning, underlies the ability to learn complex skills neces- sary for animal survival, such as speech. A variety of sensory sources (auditory and non-auditory) of information are crucial for guiding vocal learning in both humans and songbirds. Also, a specialized neural pathway that underlies vocalizations has evolved in both species. However, the neural mechanisms that process non-auditory sensory information to guide vocal learning are unknown. Here, we study whether the specialized vocal neural circuit in songbirds processes exclusively auditory infor- mation to guide adaptive changes in vocal motor output. We do so by assessing the necessity of specific songbird brain regions within this vocal learning pathway for auditory and non-auditory vocal learning. We found that songbirds are capable of adapting elements of their song in response to non-auditory sensory signals. We also found that a cortical-basal ganglia circuit and its dopaminergic input are required for non-auditory vocal learning. Thus, the specialized neural circuitry for vocal learning in songbirds does not process exclusively auditory feedback. Instead, it processes sen- sory information from a variety of different sources to drive adaptive changes in vocal motor output. Due to the numerous analogies between human and songbird vocal neural pathways, we believe that this work improves our knowledge of how neural circuits underlie sensorimotor learning across species. 

Table of Contents

1 Introduction 1

1.1 Sensorimotor Learning .......................... 1

1.1.1 Sensorimotor learning in mammalian systems . . . . . . . . . 3

1.1.2 Neural circuits for sensorimotor learning in mammals . . . . . 7

1.1.3 Human speech: behavior and neural circuits . . . . . . . . . . 18

1.2 Songbirds as a model system for studying sensorimotor learning . . . 25

1.2.1 Auditory feedback plays a particularly important role in shaping songbird vocal output .................... 28

1.2.2 Non-auditory sensory information can shape songbird behavior 34

1.3 Songbird neural circuitry for sensorimotor learning . . . . . . . . . . 40

1.3.1 Songbird neuroanatomy and the song system . . . . . . . . . . 41

1.3.2 Songbird neural circuitry for processing auditory feedback to drive vocal learning........................ 45

1.3.3 Songbird neural circuitry for processing non-auditory sensory feedback.............................. 54

1.4 Summary ................................. 59

2 Shared mechanisms of auditory and non-auditory vocal learning in the songbird brain 61

2.1 Abstract.................................. 61

2.2 Introduction................................ 62

2.3 Materials and Methods.......................... 66

2.3.1 Delivery of non-auditory sensory feedback . . . . . . . . . . . 67

2.3.2 Vocal learning paradigm and song analysis . . . . . . . . . . . 67

2.3.3 Analysis of Variability in Syllable Pitch. . . . . . . . . . . . . 72

2.3.4 LMAN Lesions .......................... 72

2.3.5 6-OHDA Lesions ......................... 73

2.3.6 Histology ............................. 74

2.3.7 Tyrosine Hydroxylase Stain ................... 75

2.3.8 Nissl Stain............................. 75

2.3.9 NeuN Antibody Stain ...................... 76

2.3.10 LesionAnalysis .......................... 76

2.3.11 StatisticalTesting......................... 77

2.4 Results................................... 79

2.4.1 Non-auditory feedback is sufficient to drive adult vocal learning 79

2.4.2 LMAN is required for non-auditory vocal learning . . . . . . . 83

2.4.3 Dopaminergic input to Area X is required for non-auditory vocal learning ............................ 87

2.5 Discussion................................. 90

2.6 Supplemental Figures........................... 94

3 Extended Discussion and Future Directions 101

3.1 Pathways for auditory and non-auditory information to reach the AFP 102

3.2 How non-auditory information may guide ethological behaviors . . . . 104

3.3 Future directions ............................. 106

3.3.1 VTA neuron encoding of auditory and non-auditory feedback . 106

3.3.2 Dopamine release in Area X as a mechanism for electric shock and white noise learning ..................... 109

3.3.3 Neural correlates of individual variability in learning . . . . . 111

3.3.4 Studying other neural systems involved in sensorimotor learning 113

Bibliography 116 

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	Biology, Neuroscience
Palabra Clave	Songbird Neuroscience Vocal learning Dopamine Motor learning Basal ganglia
Committee Chair / Thesis Advisor	Samuel Sober, Emory University
Committee Members	Gordon Berman, Emory University Robert Liu, Emory University Michael Brainard, University of California San Francisco Brian Dias, Emory University

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