Elucidating the role of dopamine in vocal learning in the Bengalese finch Open Access
Saravanan, Varun (Fall 2019)
Published
Abstract
All living organisms must learn to produce certain motor behaviors appropriate to the sensory stimuli encountered in their environment in order to survive. In complex organisms, such motor behavior produced is evaluated through further sensory feedback and is refined for future performance. This learning is referred to as sensorimotor learning. Sensorimotor learning can be distinguished into two broad categories – reinforcement learning that relies on external appetitive or aversive cues and sensorimotor adaptation in which the only feedback available to the organism is its own evaluation of the motor behavior performed. We have previously shown a role for dopamine in vocal reinforcement learning in Bengalese finches (Lonchura striata var. domestica). This dissertation again uses Bengalese finches, a highly accessible sensorimotor learner, to study the role of dopamine in sensorimotor adaptation.
We discovered, as we were analyzing data for a previous experiment, that some of the assumptions underlying the statistical tests we had used in the past were being violated due to the hierarchical nature of our data. When variability exists at multiple levels, as is the case with hierarchical data, the error has to be propagated appropriately in order to account for the total uncertainty in the measurement. We had previously been treating each data point independently in spite of the hierarchical structure which underestimates the total error. We show that using hierarchical bootstrapping, we can accurately quantify the uncertainty in the measurement. In addition, we show real world applications of the hierarchical bootstrap and demonstrate how it provides more accurate results than traditional statistical tests on hierarchical datasets. We then used hierarchical bootstrapping to show that birds displayed severe sensorimotor adaptation deficits following a dopamine lesion of Area X, a song-specific basal ganglia nucleus. Specifically, birds showed both an inability to shift their pitch adaptively to induced auditory feedback errors and a tendency to reduce pitch regardless of auditory error post-lesion. By building on the involvement of dopamine in reinforcement learning and showing its necessity for sensorimotor adaptation, this dissertation lays the foundation for uncovering the role of dopamine in sensorimotor learning.
Table of Contents
TABLE OF FIGURES .................................................................................................................. 3
LIST OF ABBREVIATIONS ...................................................................................................... 5
1 CHAPTER I: INTRODUCTION AND LITERATURE REVIEW ................................. 7
1.1 Sensorimotor Learning .................................................................................................. 8
1.1.1 Reinforcement Learning ........................................................................................... 8
1.1.2 Sensorimotor Adaptation ........................................................................................ 14
1.1.3 Other classifications of Sensorimotor Learning ..................................................... 17
1.2 A role for Dopamine in Sensorimotor Learning ....................................................... 21
1.2.1 Dopamine before Reward Prediction Error (RPE) ................................................. 21
1.2.2 Dopamine in Reinforcement Learning .................................................................... 22
1.2.3 Dopamine in Sensorimotor Adaptation .................................................................. 28
1.3 Songbirds as a model system ....................................................................................... 30
1.3.1 Overview ................................................................................................................. 30
1.3.2 Reinforcement Learning in Songbirds .................................................................... 31
1.3.3 Sensorimotor Adaptation in Songbirds ................................................................... 34
1.4 Error Propagation in Hierarchical Data .................................................................... 35
1.4.1 Problem Identification and Early Solutions ............................................................ 36
1.4.2 Linear Mixed Models (LMMs) as a Solution ......................................................... 38
1.4.3 Bootstrapping and other Resampling methods as a solution .................................. 40
1.5 Dissertation Overview .................................................................................................. 41
2 CHAPTER II: DOPAMINE DEPLETION AFFECTS VOCAL ACOUSTICS AND DISRUPTS SENSORIMOTOR ADAPTATION IN SONGBIRDS . 43
2.1 Abstract ......................................................................................................................... 43
2.2 Introduction .................................................................................................................. 44
2.3 Materials and Methods ................................................................................................ 46
2.3.1 Experimental design and Statistical Analysis ......................................................... 46
2.3.2 6-OHDA Lesions: ................................................................................................... 51
2.3.3 Headphones attachment and assembly: .................................................................. 51
2.3.4 Histology: ................................................................................................................ 52
2.3.5 Image and Lesion Analysis: .................................................................................... 53
2.3.6 Pitch Quantification: ............................................................................................... 54
2.3.7 Error quantification: ................................................................................................ 55
2.3.8 Hypothesis testing with Bootstrap: ......................................................................... 57
2.3.9 Validating our Results with Linear Mixed Models: ............................................... 58
2.4 Results ........................................................................................................................... 59
2.4.1 6-OHDA lesions reduce dopaminergic innervation of Area X: .............................. 59
2.4.2 6-OHDA lesioned birds reduce pitch even in the absence of auditory error: ......... 61
2.4.3 6-OHDA lesioned birds do not respond adaptively to pitch-shifted auditory error: 63
2.4.4 No correlations between lesion extent and changes in pitch: ................................. 68
2.4.5 Washout is impaired by dopamine depletion: ......................................................... 69
2.5 Discussion ...................................................................................................................... 74
3 CHAPTER III: APPLICATION OF THE HIERARCHICAL BOOTSTRAP TO MULTI-LEVEL DATA IN NEUROSCIENCE.. 79
3.1 Abstract ......................................................................................................................... 79
3.2 Introduction .................................................................................................................. 80
3.3 Materials and Methods ................................................................................................ 82
3.3.1 Traditional vs Summarized vs Bootstrap ................................................................ 82
3.3.2 Hypothesis testing using Bootstrap:........................................................................ 85
3.3.3 Design Effect (DEFF): ............................................................................................ 87
3.4 Results ........................................................................................................................... 88
3.4.1 Simulations ............................................................................................................. 88
3.4.2 Examples ................................................................................................................. 97
3.5 Discussion .................................................................................................................... 104
4 CHAPTER IV: CONCLUSIONS AND FUTURE DIRECTIONS .............................. 110
4.1 Dopamine as a multiplexed signal............................................................................. 110
4.2 New Techniques to understand brain function ....................................................... 114
4.3 The problem of Information in an Interconnected Network ................................. 116
4.4 Future Experimental Proposals ................................................................................ 119
4.5 Statistics and the Bootstrap ....................................................................................... 123
5 CHAPTER V: REFERENCES ........................................................................................ 126
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