Hippocampal theta coordinates memory processing during visual exploration

The hippocampus supports memory encoding and retrieval, which may occur at distinct phases of the theta cycle. These processes dynamically interact over rapid timescales, especially when sensory information conflicts with memory. The ability to link hippocampal dynamics to memory-guided behaviors has been limited by experiments that lack the temporal resolution to segregate encoding and retrieval. Here, we simultaneously tracked eye movements and hippocampal field potentials while neurosurgical patients performed a spatial memory task. Phase-locking at the peak of theta preceded fixations to retrieved locations, indicating that the hippocampus coordinates memory-guided eye movements. In contrast, phase-locking at the trough of theta followed fixations to novel object-locations and predicted intact memory of the original location. Theta-gamma phase amplitude coupling increased during fixations to conflicting visual content, but predicted memory updating. Hippocampal theta thus supports learning through two interleaved processes: strengthening encoding of novel information and guiding exploration based on prior experience.

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Hippocampal theta coordinates memory processing during visual exploration

10.1101/629451 ◽

2019 ◽

Cited By ~ 2

Author(s):

James E. Kragel ◽

Stephen VanHaerents ◽

Jessica W. Templer ◽

Stephan Schuele ◽

Joshua M. Rosenow ◽

...

Keyword(s):

Eye Movements ◽

Phase Locking ◽

Memory Performance ◽

Memory Task ◽

Sensory Information ◽

Visual Exploration ◽

Theta Oscillations ◽

Neurosurgical Patients ◽

Phase Amplitude ◽

Encoding And Retrieval

SummaryThe hippocampus supports memory encoding and retrieval, with distinct phases of theta oscillations modulating the amplitude of gamma-band activity during each process. Encoding and retrieval operations dynamically interact over rapid timescales, especially when sensory information conflicts with memory. The ability to link hippocampal dynamics to specific memory-guided behaviors has been limited by experiments that lack the temporal resolution to segregate when encoding and retrieval occur. To resolve this issue, we simultaneously tracked eye movements and hippocampal field potentials while neurosurgical patients performed a spatial memory task. Novelty-driven fixations increased phase-locking to the theta rhythm, which predicted successful memory performance. Theta to gamma phase amplitude coupling increased during these viewing behaviors and predicted forgetting of conflicting memories. In contrast, theta phase-locking preceded fixations initiated by memory retrieval, indicating that the hippocampus coordinates memory-guided eye movements. These findings suggest that theta oscillations in the hippocampus support learning through two interleaved processes: strengthening the encoding of novel information and guiding exploration based on prior experience.

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Theta power and theta-gamma coupling support spatial memory retrieval

10.1101/732735 ◽

2019 ◽

Cited By ~ 1

Author(s):

Umesh Vivekananda ◽

Daniel Bush ◽

James A Bisby ◽

Sallie Baxendale ◽

Roman Rodionov ◽

...

Keyword(s):

Spatial Memory ◽

Task Performance ◽

Memory Function ◽

Memory Task ◽

Theta Oscillations ◽

Theta Power ◽

Human Epilepsy ◽

Phase Amplitude ◽

Hippocampal Theta

AbstractHippocampal theta oscillations have been implicated in spatial memory function in both rodents and humans. What is less clear is how hippocampal theta interacts with higher frequency oscillations during spatial memory function, and how this relates to subsequent behaviour. Here we asked ten human epilepsy patients undergoing intracranial EEG recording to perform a desk-top virtual reality spatial memory task, and found that increased theta power in two discrete bands (‘low’ 2-5Hz and ‘high’ 6-9Hz) during cued retrieval was associated with improved task performance. Similarly, increased coupling between ‘low’ theta phase and gamma amplitude during the same period was associated with improved task performance. These results support a role of theta oscillations and theta-gamma phase-amplitude coupling in human spatial memory function.

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Single neurons throughout human memory regions phase-lock to hippocampal theta

10.1101/2020.06.30.180174 ◽

2020 ◽

Author(s):

Daniel R. Schonhaut ◽

Ashwin G. Ramayya ◽

Ethan A. Solomon ◽

Nora A. Herweg ◽

Itzhak Fried ◽

...

Keyword(s):

Phase Locking ◽

Human Memory ◽

Phase Lock ◽

Functional Connections ◽

Hippocampal Activity ◽

Neurosurgical Patients ◽

Multiple Regions ◽

Theta Phase ◽

Episodic Memories ◽

Hippocampal Theta

AbstractFunctional interactions between the hippocampus and cortex are critical for episodic memory. Neural oscillations are believed to coordinate these interactions, and in rodents, prefrontal neurons phase-lock to hippocampal theta oscillations during memory-guided behavior. We assessed inter-regional phase-locking to hippocampal oscillations in humans by recording 1,233 cortical and amygdala neurons and simultaneous hippocampal local field potentials in 18 neurosurgical patients. We identified 362 neurons (29.4%) from multiple regions that phase-locked to rhythmic hippocampal activity, predominantly at theta (2-8Hz) frequencies. Compared to baseline spiking, strong theta phase-locking coincided with regionally-specific increases in hippocampal theta power, local and hippocampal high frequency activity, and cross-frequency power correlations between the hippocampus and a phase-locked neuron’s local region. These results reveal that spike-time synchrony with hippocampal theta is a defining feature of cortico-hippocampal functional connections in humans. We propose that theta phase-locking could mediate flexible inter-regional communication to shape the content and quality of episodic memories.

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12. Human hippocampal theta oscillations show performance-dependent phase-locking during a working memory task

Clinical Neurophysiology ◽

10.1016/j.clinph.2010.03.046 ◽

2011 ◽

Vol 122 (1) ◽

pp. e5

Author(s):

Jonathan Kleen ◽

Barbara Jobst ◽

Kandan Kulandaivel ◽

Terrance Darcey ◽

Gregory Holmes ◽

...

Keyword(s):

Working Memory ◽

Phase Locking ◽

Memory Task ◽

Theta Oscillations ◽

Hippocampal Theta

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Faculty Opinions recommendation of Prefrontal phase locking to hippocampal theta oscillations.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1025239.347416 ◽

2005 ◽

Author(s):

Michael E Hasselmo

Keyword(s):

Phase Locking ◽

Theta Oscillations ◽

Hippocampal Theta

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Faculty Opinions recommendation of Prefrontal phase locking to hippocampal theta oscillations.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1025239.299002 ◽

2005 ◽

Author(s):

Edvard I Moser

Keyword(s):

Phase Locking ◽

Theta Oscillations ◽

Hippocampal Theta

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Faculty Opinions recommendation of Prefrontal phase locking to hippocampal theta oscillations.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1025239.298807 ◽

2005 ◽

Author(s):

Wolf Singer

Keyword(s):

Phase Locking ◽

Theta Oscillations ◽

Hippocampal Theta

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Brain Activity-Based Metrics for Assessing Learning States in VR under Stress among Firefighters: An Explorative Machine Learning Approach in Neuroergonomics

Brain Sciences ◽

10.3390/brainsci11070885 ◽

2021 ◽

Vol 11 (7) ◽

pp. 885

Author(s):

Maher Abujelala ◽

Rohith Karthikeyan ◽

Oshin Tyagi ◽

Jing Du ◽

Ranjana K. Mehta

Keyword(s):

Machine Learning ◽

Environmental Conditions ◽

Brain Activity ◽

Memory Task ◽

Classification Problem ◽

Brain Regions ◽

Training Data ◽

Information Encoding ◽

Machine Learning Approach ◽

Encoding And Retrieval

The nature of firefighters` duties requires them to work for long periods under unfavorable conditions. To perform their jobs effectively, they are required to endure long hours of extensive, stressful training. Creating such training environments is very expensive and it is difficult to guarantee trainees’ safety. In this study, firefighters are trained in a virtual environment that includes virtual perturbations such as fires, alarms, and smoke. The objective of this paper is to use machine learning methods to discern encoding and retrieval states in firefighters during a visuospatial episodic memory task and explore which regions of the brain provide suitable signals to solve this classification problem. Our results show that the Random Forest algorithm could be used to distinguish between information encoding and retrieval using features extracted from fNIRS data. Our algorithm achieved an F-1 score of 0.844 and an accuracy of 79.10% if the training and testing data are obtained at similar environmental conditions. However, the algorithm’s performance dropped to an F-1 score of 0.723 and accuracy of 60.61% when evaluated on data collected under different environmental conditions than the training data. We also found that if the training and evaluation data were recorded under the same environmental conditions, the RPM, LDLPFC, RDLPFC were the most relevant brain regions under non-stressful, stressful, and a mix of stressful and non-stressful conditions, respectively.

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The Effect of Divided Attention on Encoding and Retrieval in Episodic Memory Revealed by Positron Emission Tomography

Journal of Cognitive Neuroscience ◽

10.1162/089892900562093 ◽

2000 ◽

Vol 12 (2) ◽

pp. 267-280 ◽

Cited By ~ 89

Author(s):

Tetsuya Iidaka ◽

Nicole D. Anderson ◽

Shitij Kapur ◽

Roberto Cabez ◽

Fergus I. M. Craik

Keyword(s):

Positron Emission Tomography ◽

Prefrontal Cortex ◽

Episodic Memory ◽

Divided Attention ◽

Memory Performance ◽

Memory Task ◽

Anterior Cingulate ◽

Emission Tomography ◽

Positron Emission ◽

Encoding And Retrieval

The effects of divided attention (DA) on episodic memory encoding and retrieval were investigated in 12 normal young subjects by positron emission tomography (PET). Cerebral blood flow was measured while subjects were concurrently performing a memory task (encoding and retrieval of visually presented word pairs) and an auditory tone-discrimination task. The PET data were analyzed using multivariate Partial Least Squares (PLS), and the results revealed three sets of neural correlates related to specific task contrasts. Brain activity, relatively greater under conditions of full attention (FA) than DA, was identified in the occipital-temporal, medial, and ventral-frontal areas, whereas areas showing relatively more activity under DA than FA were found in the cerebellum, temporo-parietal, left anterior-cingulate gyrus, and bilateral dorsolateral-prefrontal areas. Regions more active during encoding than during retrieval were located in the hippocampus, temporal and the prefrontal cortex of the left hemisphere, and regions more active during retrieval than during encoding included areas in the medial and right-prefrontal cortex, basal ganglia, thalamus, and cuneus. DA at encoding was associated with specific decreases in rCBF in the left-prefrontal areas, whereas DA at retrieval was associated with decreased rCBF in a relatively small region in the right-prefrontal cortex. These different patterns of activity are related to the behavioral results, which showed a substantial decrease in memory performance when the DA task was performed at encoding, but no change in memory levels when the DA task was performed at retrieval.

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