Measuring and Understanding Muscular Control of Vocal Production in Songbirds (The neuromuscular dynamics of avian karaoke) Pubblico

Pack, Andrea R. (Fall 2022)

Permanent URL: https://etd.library.emory.edu/concern/etds/6969z2326?locale=it
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Abstract

Motor control requires the brain to rapidly process sensory signals and coordinate precise patterns of muscle activity. A central objective in neuroscience is to establish how the brain controls muscle activity and modifies muscle output during motor skill learning. Our prior work in songbirds quantified the timescale at which patterns of neural and muscle activity control vocal and respiratory behavior and demonstrated that millisecond-scale variations in spike patterning in cortical neurons and respiratory muscle fibers are correlated with the upcoming motor output (Srivastava et al., 2017; Tang et al., 2014). However, it is still unknown whether and how muscle fibers transform these precisely timed spikes patterns into variations in behavior. The first set of experiments mentioned above targeted a larger, superficial muscle in the songbird which controls the exhalation phase in a breathing cycle (i.e., expiratory muscle group). My dissertation extends this line of inquiry by investigating whether millisecond-scale differences in activation patterns to vocal organ muscles affect motor output (e.g., singing). Conventional implantable fine-wire electrodes and non-invasive surface skin electrodes are not capable of recording electromyography (EMG) activity from the muscles of interest due to the small size of vocal organ muscles and the deep, internal location of the songbird’s vocal organ. To address these limitations, we developed an innovative bipolar electrode array made from extremely flexible and strong carbon nanotube fibers (CNTFs) to simultaneously measure EMG activity from multiple small vocal organ muscles in songbirds during an acute experimental paradigm. As detailed in Chapter 2, the new bipolar CNTF electrode array recordings successfully recorded single-unit spike trains and yielded multi-unit recordings with higher signal-to-noise ratios compared to stainless steel electrodes. We then experimentally induced two- and three-pulse stimulation patterns in fiber bundles from a vocal organ muscle in vitro and measured and compared the corresponding changes in force output to determine whether millisecond-scale differences in muscle stimulation patterns modulate force output. These experiments demonstrated that songbird vocal organ muscles exhibit strong timing-based nonlinear force output during short interpulse intervals (IPIs; i.e., IPIs < 15 ms), and suggest that these nonlinearities, along with nonlinearities we have previously described in songbird respiratory muscles, are a crucial feature of vocal behavior. These results will guide future studies to examine how muscle activity is organized across time and space as a skilled behavior is learned, offering new insights into motor control.

Table of Contents

Chapter 1 

Introduction and Literature Review.. 1

1.1       The neurobiology of motor control 1

1.1.1    What is motor control?. 1

1.1.2    Dissertation objectives. 4

1.2       Songbirds as a model system for vocal control and sensorimotor learning. 5

1.2.1    Motivations to study bird vocal production. 5

1.2.2    Overview of song system circuitry. 7

1.2.3    Vocal organ anatomy and function. 10

1.2.4    Superfast muscles. 13

1.2.5    Calcium dynamics. 14

1.2.6    Vocal organ mechanisms in birds. 16

1.2.7    Similarities and differences in vocal behavior between birds and humans. 17

1.3       Muscles. 20

1.3.1    Motor Units. 21

1.3.2    Sliding filament model of muscle contraction. 23

1.3.3    Force generation in muscles. 24

1.4       Electromyography. 26

1.4.1    Current EMG methods. 27

1.4.2    Challenges. 29

1.4.3    New Technology. 30

1.4.4    Project 1: Develop new EMG technology to record from small, deep muscles. 32

1.5       Understanding how patterns of activity produce motor behavior 33

1.5.1    Defining patterns of muscle activity. 34

1.5.2    Project 2: Determine whether muscles of the songbird vocal organ are sensitive to milli-second spike timing. 36

Chapter 2 

A flexible carbon nanotube electrode array for acute in vivo EMG recordings. 38

2.1       Abstract 38

2.2       Introduction. 39

2.3       Methods. 42

2.3.1    Animals. 42

2.3.2    Carbon nanotube fiber fabrication. 43

2.3.4    Carbon nanotube fibers array construction. 44

2.3.5    Mechanical testing of array flexibility. 47

2.3.6    EMG data collection. 47

2.3.7    Acute EMG surgery. 48

2.3.8    EMG data analysis. 50

2.4       Results. 54

2.5       Discussion. 57

Chapter 3 

Millisecond-scale differences in songbird vocal muscle stimulation patterns modulate motor output. 63

3.1       Abstract 63

3.2       Introduction. 64

Activation timing in vocal organ muscles. 67

3.3       Methods. 69

3.3.1    Animals. 69

3.3.2    In vitro muscle preparation. 69

3.3.3    In vitro muscle stimulation. 70

3.3.4    Data analysis. 71

3.4       Results. 75

3.5       Discussion. 79

Chapter 4 

Discussion and Future Directions. 84

4.1       Thesis discussion. 84

4.1.2    Chapter 2 - Extended discussion. 85

4.2.2    Chapter 3 - Extended discussion. 87

4.2       Future directions. 88

4.2.1    Sensorimotor learning. 88

4.2.2    How is neural activity translated into muscular coordination during motor learning? 90

References  99

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