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V2a Neurons Pattern Respiratory Muscle Activity in Health and Disease

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V2a Neurons Pattern Respiratory Muscle Activity in Health and Disease V2a Neurons Pattern Respiratory Muscle Activity in Health and Disease by Victoria N. Jensen A dissertation submitted to the University of Cincinnati in partial fulfillment of the requirements for the degree of Doctor of Philosophy University of Cincinnati College of Medicine Neuroscience Graduate Program December 2019 Committee Chairs Mark Baccei, Ph.D. Steven Crone, Ph.D. i Abstract Respiratory failure is the leading cause of death in in amyotrophic lateral sclerosis (ALS) patients and spinal cord injury patients. Therefore, it is important to identify neural substrates that may be targeted to improve breathing following disease and injury. We show that a class of ipsilaterally projecting, excitatory interneurons located in the brainstem and spinal cord – V2a neurons – play key roles in controlling respiratory muscle activity in health and disease. We used chemogenetic approaches to increase or decrease V2a excitability in healthy mice and following disease or injury. First, we showed that silencing V2a neurons in neonatal mice caused slow and irregular breathing. However, silencing V2a neurons in adult mice did not alter the regularity of respiration and actually increased breathing frequency, suggesting that V2a neurons play different roles in controlling breathing at different stages of development. V2a neurons also pattern respiratory muscle activity. Our lab has previously shown that increasing V2a excitability activates accessory respiratory muscles at rest in healthy mice. Surprisingly, we show that silencing V2a neurons also activated accessory respiratory muscles. These data suggest that two types of V2a neurons exist: Type I V2a neurons activate accessory respiratory muscles at rest whereas Type II V2a neurons prevent their activation when they are not needed. Moreover, altering the excitability of just cervical spinal neurons using viral strategies suggests that these two V2a subtypes are both located in the cervical spinal cord. The effect of increasing and decreasing V2a excitability on accessory respiratory muscle activity was also tested in ALS model mice. Increasing or decreasing V2a excitability activates accessory respiratory muscles throughout disease progression in SOD1(G93A) ALS model mice. Finally, we demonstrate that increasing V2a excitability promotes recovery of diaphragm function following a high level C2 hemisection spinal cord injury. Moreover, silencing V2a neurons two weeks following injury impairs recovery of diaphragm function. Thus, we conclude that V2a neurons control accessory respiratory muscle activity and promote recovery of respiratory muscle function following disease and spinal cord injury. ii iii Acknowledgments Many thanks to the following funding sources and personnel that have supported this research: Funding Sources University of Cincinnati University of Cincinnati Neuroscience Graduate Program T32NS5007453 University of Cincinnati Dean’s Dissertation Completion Fellowship University of Cincinnati/Kentucky Center for Clinical and Translational Science and Training Cincinnati Children’s Hospital Medical Center Dissertation Committee CCHMC Division of Neurosurgery CCHMC Trustee Award Mark Baccei, Ph.D. (Chair) CCHMC RIP Grant Steve Davidson, Ph.D. Steven Crone, Ph.D. External Funding Warren Alilain, Ph.D. Albert J. Ryan Fellowship Timothy Weaver, Ph.D. L.I.F.E Foundation Research Grant Amyotrophic Lateral Sclerosis Starter Grant Craig H. Neilson Foundation NINDS1RO1NS112255 Yutaka Yoshida Lab (CCHMC) Crone Lab (current and former members) Masaki Ueno Steven A. Crone (Mentor) Fumiyasu Imai Shannon Romer Kari Seedle Steve Danzer Lab (CCHMC) Sarah Turner Raymond Pun Emma Dwenger Candi LeSarge *Brooke Chastain Ashley Lengel Mark Baccei Lab (University of Cincinnati) *Azl Saeed Ji Lie *Omar Barazi Bailey Clark John Lorenz Lab (University of Cincinnati Kanika Segal Warren Alilain Lab (University of Kentucky) *These undergraduates worked directly on *Emily Huffman research projects presented in this thesis. Daimen Stoltz Aaron Silverstein Lydia Hager Rachel Jolly iv TABLE OF CONTENTS Page CHAPTER I: Introduction: Nervous System Control of Breathing A. Significance Statement 2 B. Role of Primary and Accessory Respiratory Muscles in Ventilation 2-4 C. Neural Control of Respiration 4-16 C1. Three brainstem oscillators interact to generate respiratory rhythm 5-6 C2. Descending input from the brainstem to the spinal cord generates rhythmic 6-7 contraction of the diaphragm during resting ventilation. C3. Chemosensory respiratory neurons alter ventilation to maintain physiological pH 8-11 C3.1 Peripheral chemoreceptors: The carotid bodies 8-9 C3.2 Central chemoreceptors: The Retrotrapezoid Nucleus 9-10 C3.3 Central chemoreception: C1 Neurons 10-11 C4. Spinal interneurons are important for breathing 11-12 C5. Sensory spinal neurons mediate sensory afferent feedback 12-14 C6. Coordinating ventilation to motor activity during exercise 14-19 C6.1 Central feed forward mechanism 14-19 C6.2 Neural interactions between locomotor and respiratory circuits 15-16 C6.3 Activation of accessory respiratory muscles 16-18 C6.3.1 Descending neural drive modulates activation of accessory 17 respiratory muscles C6.3.2 Sensory afferent feedback modulates accessory respiratory 18 muscle activity C6.3.3. Spinal interneurons control accessory respiratory muscle 18-19 activity D. Breathing is Impaired in Neuromuscular Diseases 19-27 D1. Respiratory deficits in ALS 19-23 D2. Compensatory plasticity in ALS 23-25 D3. Treatment for ALS: New Therapies are Needed 26-27 E. Breathing is Impaired Following High-Level Spinal Cord Injury 27-39 E1. Respiratory deficits following spinal cord injury 27-28 E2. Compensatory plasticity following spinal cord injury 29-37 E2.1 Compensatory plasticity following spinal cord injury: The Crossed 29-33 Phrenic Phenomenon E2.2 Interneurons play key roles in promoting respiratory plasticity following 33-36 spinal cord injury E2.3 Compensatory plasticity following spinal cord injury: Accessory 36-37 respiratory muscle activation E3. Treatment for high level spinal cord injury 38-39 F. V2a Neurons Control Locomotion and Breathing 39-47 v F1. Distinct classes of interneurons exist with distinct properties 39-40 F2. Properties of V2a interneurons 40-41 F3. V2a neurons coordinate locomotion 41-43 F4. V2a neurons modulate breathing 44-45 F5. V2a neurons may promote recovery of breathing following disease or injury 45-47 CHAPTER II: Brainstem and Spinal Cord V2a Neurons Regulate Respiratory Muscle Activity 47-88 and Ventilation in Healthy Mice 2.1 Introduction 48-50 2.2 Methods 50-58 2.3 Results 58-80 2.4 Discussion 80-88 CHAPTER III: Cervical Spinal V2a Neurons Control Respiratory Muscle Activity and Increase 89-120 Ventilation in Healthy Mice 3.1 Introduction 90-91 3.2 Methods 91-95 3.3 Results 95-113 3.4 Discussion 113-120 CHAPTER IV: Altering V2a Excitability Increases ARM Activity and Enhances Ventilation in 121-143 ALS Model Mice 4.1 Introduction 122-123 4.2 Methods 123-126 4.3 Results 126-137 4.4 Discussion 137-143 CHAPTER V: Increasing the Excitability of V2a Neurons Promotes Recovery of Respiratory 144-181 Muscle Activity Following Spinal Cord Injury 5.1 Introduction 145-147 5.2 Methods 147-152 5.3 Results 152-172 5.4 Discussion 172-181 CHAPTER VI: Conclusions and Future Directions 182-190 List of Abbreviations 191-192 References 193-208 vi Chapter Figure Figure Title Page Chapter Figure 1 Analyzing the respiratory cycle 3 I Figure 2 Complex interaction among brainstem and spinal cord respiratory structures 5 controls respiratory rhythm and pattern generation Figure 3 The Crossed Phrenic Phenomenon 31 Chapter Figure 1 (Gi)DREADD is expressed in V2a neurons in the spinal cord and brainstem of V2a- 61 II (Gi)DREADD mice Figure 2 Decreasing the excitability of V2a neurons causes irregular breathing in neonatal 64 V2a-(Gi)DREADD mice Figure 3 Decreasing the excitability of V2a neurons increases breathing frequency without 66 causing irregular breathing in adult V2a-(Gi)DREADD mice Figure 4 Decreasing the excitability of V2a neurons increases extradiaphragmatic respiratory 68 muscle activity Figure 5 Diaphragm EMG peak amplitude does not change during ARM bouts 70 Figure 6 Ventilation is increased during bouts of ARM activity 73 Figure 7 Decreasing V2a neuron excitability does not alter arterial oxygen saturation 75 Figure 8 Brainstem and spinal cord V2a neurons are sufficient but not necessary to increase 77 heart rate and blood pressur Figure 9 Increasing and decreasing the excitability of V2a neurons differentially affects 79 motor functions Figure 10 Hypothetical Model: V2a neuron diversity may explain how increasing or 80 decreasing the excitability can activate ARMs Chapter Figure 1 Cervical spinal V2a neurons express the excitatory (Gq)DREADD receptor in AAV- 96 III (Gq)DREADD mice Figure 2 Cervical spinal V2a neurons express the inhibitory (Gi)DREADD receptor in AAV- 98 (Gi)DREADD mice Figure 3 Cervical spinal V2a neurons express eGFP in non-DREADD expressing AAV-eGFP 99 mice Figure 4 Increasing or decreasing the excitability of cervical spinal V2a neurons increases 102 scalene ARM activity Figure 5 Cervical spinal V2a neurons are sufficient but not required for diaphragm activity 104 Figure 6 Increasing the excitability of cervical spinal V2a neurons increases ventilation 106 during bouts of ARM activity Figure 7 Decreasing the excitability of cervical spinal V2a neurons increases ventilation 109 during bouts of ARM activity Figure 8 Cervical spinal V2a neurons project to respiratory
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