Hippocampal theta coordinates memory processing during visual exploration

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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Hippocampal theta coordinates memory processing during visual exploration

eLife ◽

10.7554/elife.52108 ◽

2020 ◽

Vol 9 ◽

Cited By ~ 4

Author(s):

James E Kragel ◽

Stephen VanHaerents ◽

Jessica W Templer ◽

Stephan Schuele ◽

Joshua M Rosenow ◽

...

Keyword(s):

Eye Movements ◽

Phase Locking ◽

Memory Task ◽

Sensory Information ◽

Visual Exploration ◽

Object Locations ◽

Neurosurgical Patients ◽

Phase Amplitude ◽

Hippocampal Theta ◽

Encoding And Retrieval

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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tACS Phase Locking of Frontal Midline Theta Oscillations Disrupts Working Memory Performance

Frontiers in Cellular Neuroscience ◽

10.3389/fncel.2016.00120 ◽

2016 ◽

Vol 10 ◽

Cited By ~ 26

Author(s):

Bankim S. Chander ◽

Matthias Witkowski ◽

Christoph Braun ◽

Stephen E. Robinson ◽

Jan Born ◽

...

Keyword(s):

Working Memory ◽

Phase Locking ◽

Memory Performance ◽

Theta Oscillations ◽

Frontal Midline Theta

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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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Effects of amnesia on processing in the hippocampus and default mode network during a naturalistic memory task: a case study

10.31234/osf.io/e9n8c ◽

2018 ◽

Author(s):

Christiane Oedekoven ◽

James L. Keidel ◽

Stuart Anderson ◽

Angus Nisbet ◽

Chris Bird

Keyword(s):

Functional Connectivity ◽

Episodic Memory ◽

Memory Performance ◽

Memory Task ◽

Structural Mri ◽

Brain Regions ◽

Left Hippocampus ◽

Cortical Regions ◽

The Right ◽

Encoding And Retrieval

Despite their severely impaired episodic memory, individuals with amnesia are able to comprehend ongoing events. Online representations of a current event are thought to be supported by a network of regions centred on the posterior midline cortex (PMC). By contrast, episodic memory is widely believed to be supported by interactions between the hippocampus and these cortical regions. In this MRI study, we investigated the encoding and retrieval of lifelike events (video clips) in a patient with severe amnesia likely resulting from a stroke to the right thalamus, and a group of 20 age-matched controls. Structural MRI revealed grey matter reductions in left hippocampus and left thalamus in comparison to controls. We first characterised the regions activated in the controls while they watched and retrieved the videos. There were no differences in activation between the patient and controls in any of the regions. We then identified a widespread network of brain regions, including the hippocampus, that were functionally connected with the PMC in controls. However, in the patient there was a specific reduction in functional connectivity between the PMC and a region of left hippocampus when both watching and attempting to retrieve the videos. A follow up analysis revealed that in controls the functional connectivity between these regions when watching the videos was correlated with memory performance. Taken together, these findings support the view that the interactions between the PMC and the hippocampus enable the encoding and retrieval of multimodal representations of the contents of an event.

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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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Maintaining fixation does not increase demands on working memory relative to free viewing

PeerJ ◽

10.7717/peerj.6839 ◽

2019 ◽

Vol 7 ◽

pp. e6839 ◽

Cited By ~ 6

Author(s):

Michael J. Armson ◽

Jennifer D. Ryan ◽

Brian Levine

Keyword(s):

Working Memory ◽

Eye Movements ◽

Response Times ◽

Memory Load ◽

Memory Performance ◽

Memory Task ◽

Oculomotor System ◽

Finger Tapping ◽

Long Term Memory ◽

Free Viewing

The comparison of memory performance during free and fixed viewing conditions has been used to demonstrate the involvement of eye movements in memory encoding and retrieval, with stronger effects at encoding than retrieval. Relative to conditions of free viewing, participants generally show reduced memory performance following sustained fixation, suggesting that unrestricted eye movements benefit memory. However, the cognitive basis of the memory reduction during fixed viewing is uncertain, with possible mechanisms including disruption of visual-mnemonic and/or imagery processes with sustained fixation, or greater working memory demands required for fixed relative to free viewing. To investigate one possible mechanism for this reduction, we had participants perform a working memory task—an auditory n-back task—during free and fixed viewing, as well as a repetitive finger tapping condition, included to isolate the effects of motor interference independent of the oculomotor system. As expected, finger tapping significantly interfered with n-back performance relative to free viewing, as indexed by a decrease in accuracy and increase in response times. By contrast, there was no evidence that fixed viewing interfered with n-back performance relative to free viewing. Our findings failed to support a hypothesis of increased working memory load during fixation. They are consistent with the notion that fixation disrupts long-term memory performance through interference with visual processes.

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Multiple and Dissociable Effects of Sensory History on Working-Memory Performance

10.1101/2021.10.31.466639 ◽

2021 ◽

Author(s):

Jasper E. Hajonides ◽

Freek van Ede ◽

Mark G. Stokes ◽

Anna C. Nobre ◽

Nicholas E. Myers

Keyword(s):

Working Memory ◽

Sensory Processing ◽

Memory Performance ◽

Memory Task ◽

Sensory Information ◽

Serial Dependence ◽

Neural Representations ◽

Sensory History ◽

Decision Making Processes

Behavioural reports of sensory information are biased by stimulus history. The nature and direction of such serial-dependence biases can differ between experimental settings - both attractive and repulsive biases towards previous stimuli have been observed. How and when these biases arise in the human brain remains largely unexplored. They could occur either via a change in sensory processing itself, post-perceptual maintenance or decision-making processes, or both. Here, we analysed behavioural and magnetoencephalographic data from a working-memory task in which participants were sequentially presented with two randomly oriented gratings, one of which was cued for recall at the end of the trial. Behavioural responses showed evidence for two distinct biases: 1) a within-trial repulsive bias away from the previously encoded orientation on the same trial, and 2) a between-trial attractive bias towards the task-relevant orientation on the previous trial. Multivariate classification of stimulus orientation revealed that neural representations during stimulus encoding were biased away from the previous grating orientation, regardless of whether we considered the within- or between-trial prior orientation - despite opposite effects on behaviour. These results suggest that repulsive biases occur at the level of sensory processing and can be overturned at post-perceptual stages to result in attractive biases in behaviour.

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Grid-like hexadirectional modulation of human entorhinal theta oscillations

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1805007115 ◽

2018 ◽

Vol 115 (42) ◽

pp. 10798-10803 ◽

Cited By ~ 20

Author(s):

Shachar Maidenbaum ◽

Jonathan Miller ◽

Joel M. Stein ◽

Joshua Jacobs

Keyword(s):

Spatial Memory ◽

Memory Performance ◽

Theta Oscillations ◽

Grid Cells ◽

Physiological Basis ◽

Grid Network ◽

Electrophysiological Recordings ◽

Neurosurgical Patients ◽

Spatial System ◽

Intracranial Recordings

The entorhinal cortex contains a network of grid cells that play a fundamental part in the brain’s spatial system, supporting tasks such as path integration and spatial memory. In rodents, grid cells are thought to rely on network theta oscillations, but such signals are not evident in all species, challenging our understanding of the physiological basis of the grid network. We analyzed intracranial recordings from neurosurgical patients during virtual navigation to identify oscillatory characteristics of the human entorhinal grid network. The power of entorhinal theta oscillations showed six-fold modulation according to the virtual heading during navigation, which is a hypothesized signature of grid representations. Furthermore, modulation strength correlated with spatial memory performance. These results demonstrate the connection between theta oscillations and the human entorhinal grid network and show that features of grid-like neuronal representations can be identified from population electrophysiological recordings.

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Multimodal determinants of phase-locked dynamics across deep-superficial hippocampal sublayers during theta oscillations

10.1101/2020.03.15.991935 ◽

2020 ◽

Cited By ~ 2

Author(s):

Andrea Navas-Olive ◽

Manuel Valero ◽

Teresa Jurado-Parras ◽

Adan de Salas-Quiroga ◽

Robert G Averkin ◽

...

Keyword(s):

Computational Models ◽

Phase Locking ◽

Memory Task ◽

Pyramidal Cells ◽

Theta Oscillations ◽

Ca1 Pyramidal Cells ◽

Cell Type Specific ◽

High Level ◽

Specific Phase ◽

Phase Preference

Theta oscillations play a major role in temporarily defining the hippocampal rate code by translating behavioural sequences into neuronal representations. However, mechanisms constraining phase timing and cell-type specific phase preference are unknown. Here, we employ computational models tuned with evolutionary algorithms to evaluate phase preference of individual CA1 pyramidal cells recorded in mice and rats not engaged in any particular memory task. We applied unbiased and hypothesis-free approaches to identify effects of intrinsic and synaptic factors, as well as cell morphology, in determining phase preference. We found that perisomatic inhibition delivered by complementary populations of basket cells interacts with input pathways to shape phase-locked specificity of deep and superficial pyramidal cells. Somatodendritic integration of fluctuating glutamatergic inputs defined cycle-by-cycle by unsupervised methods demonstrated that firing selection is tuneable across sublayers. Our data identify different mechanisms of phase-locking selectivity that are instrumental for high-level flexible dynamical representations.

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