Theta phase synchronization between the human hippocampus and the prefrontal cortex supports learning of unexpected information

AbstractEvents that violate predictions are thought to not only modulate activity within the hippocampus and prefrontal cortex, but also to enhance communication between the two regions. Several studies in rodents have shown that synchronized theta oscillations facilitate communication between the prefrontal cortex and hippocampus during salient events, but it remains unclear whether similar oscillatory mechanisms support interactions between the two regions in humans. Here, we had the rare opportunity to conduct simultaneous electrophysiological recordings from the human hippocampus and prefrontal cortex from two patients undergoing presurgical evaluation for pharmaco-resistant epilepsy. Recordings were conducted during a task that involved encoding of contextually expected and unexpected visual stimuli. Across both patients, hippocampal-prefrontal theta phase synchronization was significantly higher during encoding of unexpected study items, compared to contextually expected study items. In contrast, we did not find increased theta synchronization between the prefrontal cortex and rhinal cortex. Our findings are consistent with the idea that theta oscillations orchestrate communication between the hippocampus and prefrontal cortex during the processing of contextually salient information.

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Theta Phase Synchronization between the Human Hippocampus and Prefrontal Cortex Increases during Encoding of Unexpected Information: A Case Study

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_01302 ◽

2018 ◽

Vol 30 (11) ◽

pp. 1646-1656 ◽

Cited By ~ 13

Author(s):

Matthias J. Gruber ◽

Liang-Tien Hsieh ◽

Bernhard P. Staresina ◽

Christian E. Elger ◽

Juergen Fell ◽

...

Keyword(s):

Phase Synchronization ◽

Theta Oscillations ◽

Pharmacoresistant Epilepsy ◽

Intracranial Eeg ◽

Human Hippocampus ◽

Electrophysiological Recordings ◽

Theta Frequency ◽

Rhinal Cortex ◽

Theta Phase

Events that violate predictions are thought to not only modulate activity within the hippocampus and PFC but also enhance communication between the two regions. Scalp and intracranial EEG studies have shown that oscillations in the theta frequency band are enhanced during processing of contextually unexpected information. Some theories suggest that the hippocampus and PFC interact during processing of unexpected events, and it is possible that theta oscillations may mediate these interactions. Here, we had the rare opportunity to conduct simultaneous electrophysiological recordings from the human hippocampus and PFC from two patients undergoing presurgical evaluation for pharmacoresistant epilepsy. Recordings were conducted during a task that involved encoding of contextually expected and unexpected visual stimuli. Across both patients, hippocampal–prefrontal theta phase synchronization was significantly higher during encoding of contextually unexpected study items, relative to contextually expected study items. Furthermore, the hippocampal–prefrontal theta phase synchronization was larger for contextually unexpected items that were later remembered compared with later forgotten items. Moreover, we did not find increased theta synchronization between the PFC and rhinal cortex, suggesting that the observed effects were specific to prefrontal–hippocampal interactions. Our findings are consistent with the idea that theta oscillations orchestrate communication between the hippocampus and PFC in support of enhanced encoding of contextually deviant information.

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Theta oscillations decrease spike synchrony in the hippocampus and entorhinal cortex

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2012.0530 ◽

2014 ◽

Vol 369 (1635) ◽

pp. 20120530 ◽

Cited By ~ 31

Author(s):

Kenji Mizuseki ◽

György Buzsaki

Keyword(s):

Entorhinal Cortex ◽

Slow Wave Sleep ◽

Temporal Distribution ◽

Theta Oscillations ◽

Spike Synchrony ◽

Wide Range ◽

Multiple Cell ◽

Theta Phase ◽

Oscillatory Mechanisms ◽

Phase Preference

Oscillations and synchrony are often used synonymously. However, oscillatory mechanisms involving both excitation and inhibition can generate non-synchronous yet coordinated firing patterns. Using simultaneous recordings from multiple layers of the entorhinal–hippocampal loop, we found that coactivation of principal cell pairs (synchrony) was lowest during exploration and rapid-eye-movement (REM) sleep, associated with theta oscillations, and highest in slow wave sleep. Individual principal neurons had a wide range of theta phase preference. Thus, while theta oscillations reduce population synchrony, they nevertheless coordinate the phase (temporal) distribution of neurons. As a result, multiple cell assemblies can nest within the period of the theta cycle.

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Different theta connectivity patterns underlie pleasantness evoked by familiar and unfamiliar music

Scientific Reports ◽

10.1038/s41598-021-98033-5 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Alberto Ara ◽

Josep Marco-Pallarés

Keyword(s):

Present Experiment ◽

Phase Synchronization ◽

Temporal Dynamics ◽

Oscillatory Activity ◽

Connectivity Patterns ◽

Theta Phase ◽

Oscillatory Mechanisms ◽

The Brain ◽

Healthy Participants

AbstractMusic-evoked pleasantness has been extensively reported to be modulated by familiarity. Nevertheless, while the brain temporal dynamics underlying the process of giving value to music are beginning to be understood, little is known about how familiarity might modulate the oscillatory activity associated with music-evoked pleasantness. The goal of the present experiment was to study the influence of familiarity in the relation between theta phase synchronization and music-evoked pleasantness. EEG was recorded from 22 healthy participants while they were listening to both familiar and unfamiliar music and rating the experienced degree of evoked pleasantness. By exploring interactions, we found that right fronto-temporal theta synchronization was positively associated with music-evoked pleasantness when listening to unfamiliar music. On the contrary, inter-hemispheric temporo-parietal theta synchronization was positively associated with music-evoked pleasantness when listening to familiar music. These results shed some light on the possible oscillatory mechanisms underlying fronto-temporal and temporo-parietal connectivity and their relationship with music-evoked pleasantness and familiarity.

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Coherent coding of spatial position mediated by theta oscillations in hippocampus and prefrontal cortex

10.1101/520585 ◽

2019 ◽

Author(s):

Mark C. Zielinski ◽

Justin D. Shin ◽

Shantanu P. Jadhav

Keyword(s):

Prefrontal Cortex ◽

Spatial Memory ◽

Spatial Information ◽

Cell Activity ◽

Memory Task ◽

Physiological Mechanism ◽

Spatial Position ◽

Theta Oscillations ◽

Male Rats ◽

Theta Phase

ABSTRACTInteractions between the hippocampus (area CA1) and prefrontal cortex (PFC) are crucial for memory-guided behavior. Theta oscillations (~8 Hz) underlie a key physiological mechanism for mediating these coordinated interactions, and theta oscillatory coherence and phase-locked spiking in the two regions have been shown to be important for spatial memory. Hippocampal place cell activity associated with theta oscillations encodes spatial position during behavior, and theta-phase associated spiking is known to further mediate a temporal code for space within CA1 place fields. Although prefrontal neurons are prominently phase-locked to hippocampal theta oscillations in spatial memory tasks, whether and how theta oscillations mediate processing of spatial information across these networks remains unclear. Here, we addressed these questions using simultaneous recordings of dorsal CA1 – PFC ensembles and population decoding analyses in male rats performing a continuous spatial working memory task known to require hippocampal-prefrontal interactions. We found that in addition to CA1, population activity in PFC can also encode the animal’s current spatial position on a theta-cycle timescale during memory-guided behavior. Coding of spatial position was coherent for CA1 and PFC ensembles, exhibiting correlated position representations within theta cycles. In addition, incorporating theta-phase information during decoding to account for theta-phase associated spiking resulted in a significant improvement in the accuracy of prefrontal spatial representations, similar to concurrent CA1 representations. These findings indicate a theta-oscillation mediated mechanism of temporal coordination for shared processing and communication of spatial information across the two networks during spatial memory-guided behavior.

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Modulation of Sustained Attention by Theta-tACS over the Lateral and Medial Frontal Cortices

Neural Plasticity ◽

10.1155/2021/5573471 ◽

2021 ◽

Vol 2021 ◽

pp. 1-12

Author(s):

Jinwen Wei ◽

Zhiguo Zhang ◽

Ziqing Yao ◽

Dong Ming ◽

Peng Zhou

Keyword(s):

Sustained Attention ◽

Sham Group ◽

Phase Synchronization ◽

Regions Of Interest ◽

Theta Oscillations ◽

Time Interval ◽

Time Frequency ◽

Transcranial Alternating Current Stimulation ◽

Theta Phase ◽

Frequency Power

Theta oscillations over the posterior medial frontal cortex (pMFC) and lateral prefrontal cortex (LPFC) play vital roles in sustained attention. Specifically, pMFC power and pMFC-LPFC synchronization correlate with cognitive control in sustained-attention-related tasks, but the causal relationships remain unknown. In the present study, we first analyzed the correlation between EEG theta oscillations (characterized by time-frequency power and phase-based connectivity) and the level of sustained attention (Experiment 1) and then utilized transcranial alternating current stimulation (tACS) to modulate theta oscillations and in turn observed its effects on sustained attention (Experiment 2). In Experiment 1, two time-frequency regions of interest (ROIs) were determined, in which high/low time-frequency power and high/low phase-based connectivity corresponded to high/low-level sustained attention. In Experiment 2, time-frequency power and phase-based connectivity of theta oscillations were compared between the sham and tACS groups within the time-frequency ROIs determined in Experiment 1. Results showed that phase-based connectivity between pMFC and LPFC significantly decreased in the tACS group compared with the sham group during the first five minutes of the poststimulation period. Moreover, a marginal trend existed that sustained attention was downregulated by tACS in the same time interval, suggesting that theta phase synchronization between pMFC and LPFC may play a causal role in sustained attention.

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Faculty Opinions recommendation of Low-frequency theta oscillations in the human hippocampus during real-world and virtual navigation.

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

10.3410/f.727303818.793528735 ◽

2017 ◽

Author(s):

James Knierim

Keyword(s):

Real World ◽

Low Frequency ◽

Theta Oscillations ◽

Virtual Navigation ◽

Human Hippocampus

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Learning to synchronize: Midfrontal theta dynamics during rule switching

10.1101/2020.06.01.127175 ◽

2020 ◽

Author(s):

Pieter Verbeke ◽

Kate Ergo ◽

Esther De Loof ◽

Tom Verguts

Keyword(s):

Negative Feedback ◽

Human Subjects ◽

Learning Task ◽

Theta Oscillations ◽

Prediction Errors ◽

Hierarchical Learning ◽

Theta Power ◽

Negative Prediction ◽

Theta Phase ◽

The Brain

AbstractIn recent years, several hierarchical extensions of well-known learning algorithms have been proposed. For example, when stimulus-action mappings vary across time or context, the brain may learn two or more stimulus-action mappings in separate modules, and additionally (at a hierarchically higher level) learn to appropriately switch between those modules. However, how the brain mechanistically coordinates neural communication to implement such hierarchical learning, remains unknown. Therefore, the current study tests a recent computational model that proposed how midfrontal theta oscillations implement such hierarchical learning via the principle of binding by synchrony (Sync model). More specifically, the Sync model employs bursts at theta frequency to flexibly bind appropriate task modules by synchrony. 64-channel EEG signal was recorded while 27 human subjects (Female: 21, Male: 6) performed a probabilistic reversal learning task. In line with the Sync model, post-feedback theta power showed a linear relationship with negative prediction errors, but not with positive prediction errors. This relationship was especially pronounced for subjects with better behavioral fit (measured via AIC) of the Sync model. Also consistent with Sync model simulations, theta phase-coupling between midfrontal electrodes and temporo-parietal electrodes was stronger after negative feedback. Our data suggest that the brain uses theta power and synchronization for flexibly switching between task rule modules, as is useful for example when multiple stimulus-action mappings must be retained and used.Significance StatementEveryday life requires flexibility in switching between several rules. A key question in understanding this ability is how the brain mechanistically coordinates such switches. The current study tests a recent computational framework (Sync model) that proposed how midfrontal theta oscillations coordinate activity in hierarchically lower task-related areas. In line with predictions of this Sync model, midfrontal theta power was stronger when rule switches were most likely (strong negative prediction error), especially in subjects who obtained a better model fit. Additionally, also theta phase connectivity between midfrontal and task-related areas was increased after negative feedback. Thus, the data provided support for the hypothesis that the brain uses theta power and synchronization for flexibly switching between rules.

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