The roles of the hippocampus and amygdala in the formation of declarative memory Restricted; Files Only

Ahlgrim, Nathan (Summer 2019)

Permanent URL: https://etd.library.emory.edu/concern/etds/vd66w090s?locale=en
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Abstract

Declarative memory depends on the hippocampus. The basolateral complex of the amygdala (BLA) directly projects to the hippocampus and contributes to the modulation of declarative memories. This dissertation further characterized the independent roles and functional interaction of these two regions. In the first aim of this dissertation, the specificity with which the amygdala and hippocampus represent visual and memory-related stimulus characteristics was investigated by analyzing single-unit activity in the human hippocampus and amygdala during a recognition memory task. Specifically, evidence for sparse coding was investigated. Sparse coding could demonstrate a specificity of single-unit coding that cannot be observed by analyzing units independently or within a population. Both regions showed evidence of sparse coding, but the hippocampus and amygdala were tuned towards different stimulus characteristics. These coding patterns demonstrated that the amygdala encodes specific information relevant to declarative memory and can likely modulate hippocampal activity in a specific manner. However, these specific representations of stimuli are only relevant to memory if they are consolidated. Certain local field potential patterns, derived from coordinated neuronal activity, are known to prioritize consolidation in the hippocampus. Previous experiments that prioritized memory via BLA stimulation were thought to increase these oscillations beneficial to memory. In the second aim, the BLA was optogenetically stimulated in rats to determine what oscillatory activity in the BLA could increase pro-memory oscillatory activity in the hippocampus. Only stimulation that replicated a gamma wave (50 Hz) whose amplitude was modulated by the phase of a theta wave (8 Hz) was sufficient to increase pro-memory oscillations in the hippocampus. Taken together, the two aims of this dissertation demonstrate the distinct roles of the amygdala and hippocampus in how declarative memory is formed and consolidated. The amygdala can encode information relevant to memory with specific ensemble activity, but it also can coordinate hippocampal activity through specific modulation of ongoing oscillatory activity.

Table of Contents

CHAPTER 1: GENERAL INTRODUCTION 1

1.1. The hippocampus is critical for declarative memory 4

1.2. The amygdala: more than the emotion center of the brain 6

1.3. The amygdala and memory 9

1.3.1. The amygdala as a hippocampal modulator 10

1.3.2. The amygdala and cellular analogues of memory 13

1.4. Precisely controlling amygdala activity to modulate specific hippocampal memories 17

1.5. Neural states beneficial to memory 19

1.5.1. Inducing beneficial memory states by indirect modulation 22

1.6. Summary of experiments 23

1.7. References 27

CHAPTER 2: THE HIPPOCAMPUS AND THE AMYGDALA EMPLOY SPARSE CODING TO REPRESENT DISTINCT INFORMATION DURING A RECOGNITION MEMORY TASK 49

Abstract 50

2.1. Introduction 51

2.2. Materials and Methods 55

2.2.1. Subjects 55

2.2.2. Data Collection and Processing 56

2.2.3. Behavioral Task and Psychophysics 56

2.2.4. Data Analysis 57

2.2.4.1. Single-Unit Analyses 58

2.2.4.2. Population-Based Analyses 58

2.2.4.3. Pseudopopulation Analyses 60

2.3. Results 60

2.3.1. Identification and Properties of Selective Units 60

2.3.2. Population activity did not provide sufficient information to decode trial types 62

2.3.3. Sparse firing evident in the hippocampus and amygdala for different trial types 62

2.4. Discussion 65

2.4.1. Decoding hippocampal and amygdalar information via population-based analyses may require larger populations or deeper processing 66

2.4.2. Neural state at baseline is a critical factor in assessing event-related activity 68

2.4.3. The hippocampus and amygdala differentially encode mnemonic and image information 69

2.4.3.1. Repetition suppression interpretation 71

2.4.3.2. “Neither” selectivity interpretation 71

2.4.4 Evidence for a sparse-distributed network in the amygdala and hippocampus 73

2.5. Conclusions 73

2.6. References 75

CHAPTER 3: OPTOGENETIC STIMULATION OF THE BASOLATERAL AMYGDALA INCREASED THETA-MODULATED GAMMA OSCILLATIONS IN THE HIPPOCAMPUS 93

Author’s contribution and acknowledgement of reproduction 94

Abstract 95

3.1. Introduction 97

3.2. Materials and Methods 100

3.2.1. Subjects 100

3.2.2. Surgery and Drive Positioning 100

3.2.3. Optogenetic Stimulation 102

3.2.4. Histology 103

3.2.5 Data Acquisition and Analysis 103

3.3. Results 105

3.3.1. Histological verification of stimulation and recording locations 105

3.3.2. Effects of one-second optogenetic BLA stimulation on BLA and CA1 LFPs 106

3.3.3. Effects of one-second optogenetic BLA stimulation on the power spectra of the BLA and CA1 109

3.3.4. Theta-gamma comodulation during optogenetic stimulation 111

3.3.5. Temporal effects of optogenetic stimulation 111

3.4. Discussion 112

3.4.1. BLA projections to CA1 were among many potential BLA projections activated by stimulation 113

3.4.2. BLA stimulation modulated neuronal oscillations in CA1 115

3.4.3. Theta-modulated 50-Hz BLA stimulation was necessary to increase theta-modulated gamma oscillations in CA1 116

3.4.4. Comparing the effects of optogenetic BLA stimulation to those of electrical BLA stimulation 117

3.5. Conclusions and future directions 118

3.6. References 120

CHAPTER 4: GENERAL DISCUSSION 137

4.1. Summary of Findings 138

4.2. Sparse coding underlies representations of mnemonic and social information 140

4.3. Implications for specific memory modulation 142

4.4. Clinical and behavioral relevance to amygdala-mediated memory 143

4.5. Future directions for the laboratory and the clinic 146

4.6. References 149

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