Involvement of the amygdala in declarative memories Restricted; Files Only
Krasney, Joshua (Fall 2023)
Abstract
A multitude of rodent and primate studies suggest that activity in the amygdala can modulate memory in other brain regions. In particular, activation of the amygdala can improve declarative memories, like memories of objects and object-context associations. Though the conventional function of the amygdala is processing emotional information, the region has also shown responses to novel information. Despite these findings, it remains uncertain whether amygdala activity is necessary to form declarative memories of novel objects. Further, the ways in which the amygdala modulates declarative memories across learning remains poorly understood. This dissertation includes two experiments to investigate the involvement of the amygdala in declarative memories. The first experiment tested monkeys with amygdala lesions on a battery of novelty-based recognition memory tasks. This experiment found that damage to the amygdala improved, rather than impaired, memory, likely due to a reduction in neophobia. The second experiment tested rats with electrophysiological recordings in the amygdala and hippocampus on an affective object-context association task. This experiment found that amygdala activity during memory retrieval was higher in the conditions with affective stimuli versus the control condition with no affective stimuli, and found that amygdala activity differed during memory retrieval of various affective categories. However, these differences in amygdala activity between conditions with or without affective stimuli did not translate to consistently better memory performance across the affective conditions versus the control condition. The disconnect between the differences in neural activity and behavior may have related to differences in distinguishability of the objects across conditions. These combined results suggest that the primary role of the amygdala is processing the affective properties elicited by stimuli, with damage to the amygdala producing better performance on novelty-based recognition memory tasks by promoting engagement with potentially threatening novel stimuli.
Table of Contents
Chapter I. General Introduction -- 1
Overview -- 2
Anatomy and functionality of the hippocampus-dependent memory system -- 2
Parahippocampal region -- 3
Hippocampus -- 6
Anatomy and functionality of the amygdala -- 8
Composition and connectivity of the amygdala -- 8
Functions of the amygdala -- 10
Emotional information -- 10
Socioemotional information -- 13
Novelty information -- 16
Parsimonious function of the amygdala: Salience dial -- 17
The amygdala, the hippocampus, and memory enhancement -- 18
Neural oscillations related to memory and emotion -- 20
Summary of experiments -- 22
References -- 23
Chapter II. Rhesus monkeys with damage to amygdala or orbitofrontal cortex perform well on novelty-based memory tasks -- 51
Author’s contribution and acknowledgement of reproduction -- 52
Abstract -- 54
Rhesus monkeys with damage to amygdala or orbitofrontal cortex perform well on novelty-based memory tasks -- 55
Method -- 57
Subjects -- 57
Neuroimaging and surgical procedures -- 57
Histology-based lesion assessment -- 60
Behavioral testing procedures -- 61
Apparatus and stimuli -- 61
Delayed non-matching-to-sample (DNMS) task -- 62
Visual paired-comparison (VPC) task -- 62
Object memory span (OMS) task -- 63
Spatial memory span (SMS) task -- 64
Data analysis -- 64
Results -- 65
Lesion extent -- 65
A-ibo and O-asp groups performed well on the DNMS task -- 66
A-ibo and O-asp groups performed well on the VPC task -- 67
A-ibo and O-asp groups performed well on the OMS task for novel and repeated objects -- 67
A-ibo and O-asp groups performed well on the SMS task for novel and repeated locations -- 68
Across tasks, A-ibo and O-asp groups performed better than the control group -- 69
Discussion -- 70
Amygdala lesions may have impacted reactions to novelty rather than novelty detection -- 71
OFC lesions may have attenuated positive associations with familiar stimuli or negative responses to novel stimuli -- 73
Anatomical subregions within the OFC and amygdala -- 74
Summary -- 75
References -- 77
Chapter III. Hippocampus-amygdala neural interactions underlying context-dependent affective memories -- 94
Abstract -- 95
Hippocampus-amygdala neural interactions underlying context-dependent affective memories -- 96
Method -- 98
Subjects -- 98
Surgery and histology -- 98
Affective object-context association task -- 99
Data acquisition -- 100
Data analyses -- 101
Video scoring and behavioral data analysis -- 101
Analysis of local field potentials during context exploration -- 102
Results -- 105
Behavioral performance differed across conditions -- 105
Spectral activity during context exploration differed between urine conditions and the control condition across learning -- 106
Spectral activity during empty context exploration similarly changed across the Learning Day for each condition -- 107
Context-cued memory differentially modulated spectral activity based on affective category -- 108
Differences in spectral activity between urine conditions and the control condition persisted after odor removal on the Retention Day -- 110
Distinct changes in BLA power, but not HIP power or BLA-HIP coherence, after removing odors of different affective categories -- 111
Context-cued memory consistently modulated spectral activity based on affective category after odor removal -- 112
Discussion -- 114
Affective stimuli differentially modulated slow and fast gamma activity along the BLA-HIP pathway versus nonaffective stimuli, but did not consistently improve performance -- 115
Decreased slow gamma power and increased slow gamma coherence for each condition across learning -- 118
Conclusion -- 120
References -- 122
Chapter IV. General Discussion -- 137
Summary of findings -- 138
Refinement of amygdala function -- 138
Valence coding in the amygdala -- 141
Affective salience and memory enhancement -- 142
Future research questions -- 143
Conclusion -- 144
References -- 146
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