Intrahippocampal Synchrony and Memory for Objects in Spatiotemporal Context Open Access

Abstract

The hippocampus is a region of the brain known to play a central role in declarative memory, or memory for facts and events, in humans and other mammals. In particular, the hippocampus is believed to be especially important in binding memories for items with memories for the spatial and temporal context in which they are encountered. The hippocampus is composed of multiple anatomically distinct subregions, including dentate gyrus, CA3, CA1, and subiculum. A fundamental question is how each subregion coordinates with the others to enable binding items and spatiotemporal context in service of declarative memory. Three experiments were conducted with rats to investigate this question. Neural data was recorded simultaneously from each of four hippocampal subregions as rats performed object recognition memory tasks that also tested memory for spatial and temporal contexts. In the first experiment, results demonstrate that the pattern of neural interactions throughout the hippocampal subregions during novel object exploration is distinct from patterns of neural interactions associated with locomotive states and in a manner that may facilitate memory encoding (Chapter 3). In experiment 2, analyses revealed differences in oscillatory interactions, particularly in the slow gamma range (30-55 Hz), at memory encoding relating to the degree to which rats remembered objects' spatial locations in addition to objects' identities (Chapter 4). Chapter 5 reports elevated slow gamma within the hippocampus at test that may relate to retrieval of an object memory cued by a repeated temporal context. The findings here demonstrate a relationship between slow gamma oscillations in the hippocampus and memory for items in spatiotemporal context and mark a significant advancement for the field, both with regard to technical approach and in further elucidating how the hippocampal subregional network state differs by behavioral state and memory state. The results described here advance our understanding more broadly of the brain mechanisms underlying memory for items in spatiotemporal context in humans and other mammals.

Table of Contents

Chapter 1: General Introduction---1

Anatomy of the Hippocampal Memory System---2

Hippocampal Function---3

Functional Anatomy of the Hippocampal Subregions6

Dentate Gyrus---4

CA3---8

CA1---9

Subiculum--11

Subregional Interactions--12

Summary---15

References---19

Chapter 2: General Method---31

Subjects---32

Behavioral Training for Object Recognition Memory Tasks---32

Objects---32

Surgery and Positioning of Recording Tetrodes---33

Data Acquisition---34

Histology---34

Statistical Reporting Format---35

Behavioral Analyses---35

Neural Data Analyses---35

Local Field Potential Analyses---36

Spectral Metrics---37

Statistical Analyses of Spectral Metrics by Frequency---37

Spiking Analyses---38

References---44

Chapter 3: Distinct Hippocampal Network State During Novel Object Exploration---46

Abstract---47

Introduction---48

Method---49

Subjects---49

Experimental Task---50

Segregation of Activity into Behavioral States---50

Data Analyses---50

Results---50

Speed of Locomotion---50

Firing Rate---51

Spike-Phase Modulation---51

Power and Coherence---53

Discussion---55

Slow Gamma During Novel Object Exploration---50

Hippocampal Theta During Location---57

Stationary Epochs Are Associated With Elevated Beta Activity---58

Conclusion---59

References---70

Chapter 4: Intrahippocampal Synchrony and Memory for… Spatial Context---75

Abstract---76

Introduction---77

Method---79

Subjects---79

Behavioral Task---79

Analyses---80

Results---80

Average Exploration Times by Lap and Trial Type---81

Neural Results for Lap 3 Object Exploration Split by Trial Type---81

Exploration Times by Subsequent Memory---82

Neural Results by Subsequent Memory--- 83

Neural Activity… by Exploration Duration ---84

Discussion---86

Slow Gamma At Test Reflects The Degree of Novelty---86

Hippocampal Gamma During Encoding---87

Gamma Oscillations Facilitate Associative Memory Encoding---88

Conclusion---77

References---105

Chapter 5: Intrahippocampal Synchrony and Memory for… Temporal Context---108

Abstract---109

Introduction---110

Method---113

Subjects---113

Behavioral Task---113

Neural Analyses---114

Results---114

Exploration Times---114

Neural Activity---115

Locomotion---115

Discussion---116

Slow Gamma Relates to Memory for… Spatiotemporal Context---116

Hippocampal Subregions and Temporal Context---117

Conclusion---118

References---125

Chapter 6: General Discussion---128

Summary of Results---129

Integrating the Present Work within the Field---129

Technical Advancement---131

Future Research Questions---132

Conclusion---133

References---134

About this Dissertation

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School	Laney Graduate School
Department	Psychology
Degree	PhD
Submission	Dissertation
Language	English
Research Field	Biology, Neuroscience Psychology, Physiological Psychology, Cognitive
Keyword	oscillations memory hippocampus
Committee Chair / Thesis Advisor	Manns, Joseph, Emory University
Committee Members	Liu, Robert C, Emory University Bachevalier, Jocelyne, Emory University Bauer, Patricia, Emory University Hampton, Robert, Emory University

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