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State-Dependent Control of Neural Activity in the Olfactory Cortex

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State-Dependent Control of Neural Activity in the Olfactory Cortex STATE-DEPENDENT CONTROL OF NEURAL ACTIVITY IN THE OLFACTORY CORTEX by KAITLIN S. CARLSON Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy Thesis Advisor: Dr. Daniel Wesson Department of Neurosciences CASE WESTERN RESERVE UNIVERSITY August, 2018 CASE WESTERN RESERVE UNIVERSITY SCHOOL OF GRADUATE STUDIES We hereby approve the dissertation of Kaitlin S. Carlson candidate for the degree of Doctor of Philosophy* Committee Chair……………………………………………... Ben W. Strowbridge, Ph.D. Member………………………………………………………… Daniel W. Wesson, Ph.D. Member…………………………………………………………… Evan S. Deneris, Ph.D. Member……………………………………………………… Brian M. McDermott, Ph.D. Date of Defense May 30th, 2018 *We also certify that written approval has been obtained for any proprietary material contained herein. i Table of Contents List of Figures…………………………………………………………………….......... iv Acknowledgments…………………………………………………………………….. viii Abstract………………………………………………………………………………...... 1 CHAPTER 1: INTRODUCTION……………………………………………………. 3 1.1 Sensory Systems………………………………………………………………… 3 1.1.1 Why we need sensory systems……………………………………………… 3 1.1.2 The mammalian olfactory system………………………………………….. 6 1.2 State-Dependent Influences on Sensory Processing…………………………….. 8 1.2.1 Arousal, sleep, anesthesia, and the olfactory system………………………. 8 1.3 Cognitive Influences on Sensory Systems………………………………………. 10 1.3.1 Historical context…………………………………………………….......... 10 1.3.2 Attention…………………………………………………………………… 12 1.3.3 Modulation in vision and audition…………………………………………. 14 1.3.4 Modulation in chemosensory systems……………………………………… 16 1.4 Network vs Single-Unit Activity………………………………………………... 17 1.5 Olfactory Cortex Anatomy……………………………………………………… 19 1.5.1 The olfactory tubercle……………………………………………………… 19 1.6 Studying Attention in Non-Human Animal Models……………………….......... 21 1.6.1 Types of attention…………………………………………………………... 21 1.6.2 Psychophysics and attention in olfaction…………………………………... 21 1.6.3 Techniques to study attention in rodents…………………………………… 22 1.7 Questions and Hypotheses: State Influences on Network and SUA…………….. 24 1.7.1 State-dependent local network level modulation…………………………… 24 1.7.2 Attentional influences on behavior………………………………………… 26 1.7.3 Attention-dependent changes in neural coding……………………………. 26 CHAPTER 2: ODOR- AND STATE-DEPENDENT OLFACTORY TUBERCLE LOCAL FIELD POTENTIAL DYNAMICS IN AWAKE RATS…………………... 33 2.1 Abstract……………………………………………………………………....... 33 2.2 Introduction……………………………………………………………………... 34 2.3 Results…………………………………………………………………………... 37 2.3.1 Theta-band power dominates spontaneous network activity………………. 37 2.3.2 Odor stimulation evokes beta- and gamma-band increases in the OT……………………………………………………………………........... 38 2.3.3 Spontaneous and odor-evoked LFP activity within the OT is similar to the upstream OB……………………………………………………………. 40 2.3.4 Both spontaneous and odor-evoked activity correspond with functional coherence across all spectral bands……………………………………….. 42 2.3.5 Inhalation-triggered OT theta cycles lag behind those of the OB……….. 42 2.3.6 Sleep-like and anesthesia-dependent modulation of spontaneous activity……………………………………………………………………… 43 2.3.7 Limited influences of sleep-like states and anesthesia on odor-evoked activity……………………………………………………………………… 43 2.4 Discussion………………………………………………………………………. 47 2.5 Conclusions……………………………………………………………………. 53 2.6 Methods……………………………………………………………………......... 54 ii 2.7 Acknowledgments……………………………………………………………... 62 CHAPTER 3: SELECTIVE ATTENTION CONTROLS OLFACTORY DECISIONS AND THE NEURAL ENCODING OF ODORS…………………….. 83 3.1 Abstract………………………………………………………………………... 83 3.2 Introduction……………………………………………………………………... 84 3.3 Results…………………………………………………………………………. 86 3.3.1 Individual rat behavioral shaping on the CAT…………………………….. 87 3.3.2 Rats can selectively attend to odors, which dictates discrimination accuracy………………………………………………………………........ 87 3.3.3 Rats improve their ability to shift attention to odors with experience……… 88 3.3.4 Increased perceptual difficulty delays odor-directed shifts in attention…. 90 3.3.5 Additional influences of enhanced cognitive demand, trial congruency, and multisensory input on behavioral responses…………………………… 90 3.3.6 Odor-directed selective attention bi-directionally sculpts the encoding of odors in the OT………………………………………………………… 93 3.3.7 Odor-excited neurons increase their FRs, while odor-inhibited neurons further decrease their FRs with odor-directed attention…………………… 93 3.3.8 Odor-directed attention enhances the signal-to-noise ratio of odor- evoked units……………………………………………………………….. 96 3.3.9 FRs of units unmodulated by odor are not significantly different with attention……………………………………………………………………. 97 3.4 Discussion……………………………………………………………………... 98 3.5 Methods………………………………………………………………………... 102 3.6 Acknowledgments............................................................................................. 114 CHAPTER 4: DISCUSSION………………………………………………………... 139 4.1 Major Conclusions……………………………………………………………. 139 4.2 Influences of Selective Attention on Odor Coding…………………………….. 140 4.3 Caveats……………………………………………………………………........ 143 4.3.1 CAT design………………………………………………………………. 143 4.3.2 Attention and reward……………………………………………………... 147 4.3.3 Limits of extracellular techniques……………………………………….. 148 4.4 Future Directions………………………………………………………………. 150 4.4.1 Influences of increased attentional demand……………………………... 150 4.4.2 Multimodal influences……………………………………………………. 152 4.4.3 Active sampling………………………………………………………...... 152 4.4.4 Neuromodulatory influences……………………………………………. 153 4.4.6 Goal cells………………………………………………………………… 156 Bibliography………………………………………………………………………….. 169 iii List of Figures Figure 1-1. Hypotheses: Odor- and state-dependent modulation of local field potential activity within the OB and OT…………………………………………………29 Figure 1-2. Hypotheses: Odor-directed selective attention modulates performance accuracy, shapes sampling durations, and sculpts the underlying odor coding………….31 Figure 2-1. Experimental timeline and electrode tip locations for olfactory tubercle (OT) and olfactory bulb (OB) recordings...………...……………………………………63 Figure 2-2. Physiological classification of sleep state for state-dependent analysis...….65 Figure 2-3. OT LFP activity in awake rats……………………………………………...67 Figure 2-4. Odor-evoked modulation of OT LFP activity in awake rats…..…………...69 Figure 2-5. Spontaneous LFP activity within the OT compared with the upstream OB……………………………………………………………………………………….71 Figure 2-6. Similar odor-evoked power in the OT and OB………………………….....73 Figure 2-7. Spectral coherence of OT and OB LFP activity………………………...…75 iv Figure 2-8. Temporal dynamics of theta cycles in the OT and OB relative to respiration…………………………………………………………………………..…..77 Figure 2-9. Behavioral and anesthetic state impact the spontaneous LFP activity in the OT………….………………………………………………………………..……...79 Figure 2-10. Impact of anesthetic state on odor-evoked LFP in the OT….………...…81 Figure 3-1. Odor-directed attention dictates discrimination accuracy….………...…..115 Figure 3-2. Rats make fewer incongruent errors as they shift their attention, which leads to increased performance accuracy………………………………………..……117 Figure 3-3. OT units are bidirectionally modulated by odor-directed attention….….119 Figure 3-4. Odor-directed attention controls odor coding…………………….....…..121 Figure 3-5. Attention yields enhanced signal-to-noise among odor coding neurons…………………………………………………………………………….....123 Figure S3-1. Detailed structure of CAT shaping phases………………………….....125 Figure S3-2. Behavioral performance during task shaping…………………….........127 v Figure S3-3. Shifting to odor-directed attention is delayed when perceptual demand is enhanced…..…………………………………...…………………..……129 Figure S3-4. Selective attention influences subtle, yet critical aspects of olfactory behavior…………………………………….…………………..…….…..131 Figure S3-5. The majority of odor-unmodulated units have firing rate and signal-to-noise ratios that remain unchanged by attention…………………..….….133 Table S3-1. Total number of blocks and sessions to reach criterion across shaping phases 1-4…………………………………………………………..……..135 Table S3-2. Total number of blocks and sessions to reach criterion across multimodal and attention phases………………..…………………………..……..136 Table S3-3. Descriptive summary of single-neuron data used for analyses…...….137 Table S3-4. Body weights (bwts) during shaping and performance………..…….138 Figure 4-1. Future experiment: Task structure for elucidating neural effects of increased attentional demand……………………………………………...………159 vi Figure 4-2. The frequency of theta cycles increases during anticipatory hold and odor across task types………………………………….…..…………...…….161 Figure 4-3. Proposed experiment: Inhibiting cholinergic input from the HDB to the OT during performance of the CAT…………………………...…………..163 Figure 4-4. Example of a goal-directed unit that increases its FR with leftward movement toward the reward port……...……………………………….…..……165 Figure 4-5. Goal-directed units within the OT encode leftward movement…..…167 vii Acknowledgments I am deeply grateful to my advisor, Dr. Daniel Wesson, for his guidance, advice, and assistance throughout my doctoral studies. I was fortunate to have been able to train under his supervision and to have shared his enthusiasm for science. In the first few years, Dan offered an enriching laboratory environment, wherein he eagerly provided me with all of the tools and training I needed to succeed in his lab. This hands-on instruction was crucial to my development as a scientist, and no doubt, allowed
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