Recognition memory signals in the macaque hippocampus Open Access
Jutras, Michael (2011)
Abstract
Abstract
Recognition memory signals in the macaque hippocampus
By Michael Joseph Jutras
Recognition memory, the ability to perceive recently encountered items as familiar, relies on structures in the medial temporal lobe, including the hippocampus. However, neurophysiological studies have thus far provided little evidence for the existence of recognition memory signals in the monkey hippocampus, despite the existence of such signals in surrounding cortical areas. Studies of the effects of hippocampal damage in monkey and humans have shown the visual paired comparison, or visual preferential looking task (VPLT), to be a test of recognition memory that is sensitive to hippocampal damage. Accordingly, to examine possible recognition memory signals in the hippocampus, I recorded hippocampal activity in rhesus monkeys as they performed the VPLT. Hippocampal neurons responded significantly to stimulus presentation relative to the baseline pre-stimulus period, and a substantial proportion of these visually-responsive neurons showed significant firing rate modulations that reflected whether stimuli were novel or familiar. Additionally, these firing rate modulations were correlated with recognition memory performance on the VPLT such that larger modulations by stimulus novelty were associated with better performance. I also observed an increase in temporally correlated activity across the hippocampus, i.e., neuronal synchronization, in the gamma frequency band during encoding that predicted the strength of subsequent recognition. Finally, I observed theta-band oscillations in hippocampal LFPs that were strongly coupled to the monkeys' eye movements, undergoing a phase resetting with each new fixation. The phase of the network theta oscillation at fixation onset and the degree of spike-field phase synchronization in the theta band across the trial were correlated with the strength of stimulus encoding. In addition, the amplitude of hippocampal gamma, which has been linked to successful memory formation, was modulated at theta frequency. Taken together, these findings suggest that neuronal activity in the hippocampus is organized at multiple levels, is related to the strength of memory formation, and is intimately connected to behavior. Findings from this research could be used to develop new criteria for identifying aberrant neural activity in humans exhibiting symptoms of memory loss. The possibility that a disruption in neuronal synchronization may underlie the memory impairment in these patients also suggests that therapies aimed at alleviating this disruption could be used to treat memory loss.
Table of Contents
Contents
Chapter 1. Introduction and Background...1
Overview...1
Background: Hebbian learning and memory formation...2
Memory systems in the brain...3
Recognition memory and the medial temporal lobe...6
The visual paired comparison (VPC) task...8
Hippocampal contribution to recognition memory...9
Hippocampal physiology - background...14
Hippocampal circuitry...15
Memory-related single neuron activity in the MTL...17
Local field potentials...20
Neuronal synchronization and memory formation...21
Gamma-band oscillations and memory formation...22
Coupling between gamma-band and theta-band oscillations...25
Phase resetting as a mechanism of processing...26
Hypothesis and Aims...29
Conclusion...30
Chapter 2. The activity of single neurons in the macaque hippocampus related to recognition memory...32
Introduction...32
Methods...35
Electrophysiological recording, data collection
and preprocessing...35
Data analysis...39
Results...44
Behavioral Results...44
Hippocampal neurons modulate their firing rate with stimulus
repetition...46
Discussion...55
Chapter 3. Gamma-band synchronization in the macaque hippocampus and memory formation...61
Introduction...61
Methods...63
Behavioral testing procedures...63
Visual preferential looking task...64
Electrophysiological recording methods...65
Data analysis...67
Correlating neuronal activity with memory performance...70
Correlations with memory and attention: binning analysis...74
Correlations with time within session: binning analysis...75
Results...76
Behavioral results...76
Neuronal activity in the hippocampus...77
Hippocampal gamma-band synchronization reflects recognition memory
performance...80
Relationship between Gamma-band Synchronization and Behavior:
Memory vs. Attention...84
Relationship between Local Field Potential and Behavior...91
Additional Behavioral Controls...93
Discussion...95
Chapter 4 Memory formation is predicted by theta-band phase-locking in the monkey hippocampus...101
Introduction...101
Methods...102
Behavioral testing procedures...102
Visual preferential looking task...103
Electrophysiological recording methods...104
Data analysis...106
Results...112
Discussion...123
Chapter 5 Discussion...125
Summary...125
Encoding is modulated through neuronal spiking and network
synchrony...127
Active sensing and the role of hippocampal theta in
memory...128
Future directions...132
References...134
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