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

2018 ◽  
Vol 30 (11) ◽  
pp. 1646-1656 ◽  
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.

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

2017 ◽  
Author(s):  
Matthias J. Gruber ◽  
Liang-Tien Hsieh ◽  
Bernhard P. Staresina ◽  
Christian E. Elger ◽  
Juergen Fell ◽  
...  
Keyword(s):  
Prefrontal Cortex ◽  
Phase Synchronization ◽  
Theta Oscillations ◽  
Presurgical Evaluation ◽  
Human Hippocampus ◽  
Electrophysiological Recordings ◽  
Rhinal Cortex ◽  
Theta Phase ◽  
Oscillatory Mechanisms ◽  
Rare Opportunity

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.

scholarly journals Heartbeat evokes a dynamically changing cortical theta-synchronized network in the resting state

2019 ◽  
Author(s):  
Jaejoong Kim ◽  
Bumseok Jeong
Keyword(s):  
Resting State ◽  
Phase Synchronization ◽  
Human Subjects ◽  
Predictive Coding ◽  
Regional Level ◽  
Human Connectome Project ◽  
Cortical Responses ◽  
Theta Frequency ◽  
Theta Phase ◽  
Cortical Regions

AbstractIn the resting state, heartbeats evoke cortical responses called heartbeat-evoked responses (HERs). While previous studies reported regional level HERs, researchers have not determined how heartbeat is processed at the cortical network level. Using resting-state magnetoencephalography data from 87 human subjects of both genders provided by the Human Connectome Project, we first showed that heartbeat increases the phase synchronization between cortical regions in the theta frequency, which forms a network structure, and we called this network a heartbeat-evoked network (HEN). The HEN was not an artefactual increase in phase synchronization. The HEN was partitioned into three modules with connector hubs in each module. The first module contained major interoception-related regions and thus was called a visceromotor-interoceptive network (VIN) displaying the strongest synchronization among modules, suggesting a major role for the VIN in processing heartbeat information. Two modules contained regions involved in the default mode network (DMN). The HEN structure was not fixed, but dynamically changed. The most prominent change was observed at approximately 200 ms after R-peak of the electrocardiogram, which was quantified based on the ‘flexibility’ of the network. Furthermore, the strongest synchronization within VIN was observed before heartbeat stimulated the cortex, which might be related to the prediction of an afferent heartbeat signal, thus supporting an interoceptive coding framework. Based on our results, the heartbeat is processed at the network level, and this result provides a useful framework that may potentially explain previous results of the regional level HER modulation through network-level processing.Significance statementThe resting-state network is composed of several networks supporting different functions. However, although the heartbeat is processed in the cortical regions, even in the resting state, the network supporting this function is unknown. Thus, we identified and investigated the heartbeat-evoked network (HEN), a network composed of significantly increased theta-phase synchronization between cortical regions after a heartbeat. The HEN comprised three modules. In particularly, the visceromotor-interoceptive network was likely to play a major role in network-level heartbeat processing and displayed the strongest synchronization immediately before the heartbeat enters the CNS, which supports an interoceptive predictive coding framework. These results provide a novel framework that may improve our understanding of cortical heartbeat processing from a network perspective.

scholarly journals Cooling of medial septum reveals theta phase lag coordination of hippocampal cell assemblies

2019 ◽  
Author(s):  
Peter C. Petersen ◽  
György Buzsáki
Keyword(s):  
Spatial Navigation ◽  
Medial Septum ◽  
Neuronal Firing ◽  
Theta Oscillations ◽  
Phase Lag ◽  
Cell Assemblies ◽  
Theta Frequency ◽  
Theta Phase ◽  
Temperature Manipulation ◽  
Phase Coordination

SummaryHippocampal theta oscillations coordinate neuronal firing to support memory and spatial navigation. The medial septum (MS) is critical in theta generation by two possible mechanisms: either a unitary ‘pacemaker’ timing signal is imposed on the hippocampal system or it may assist in organizing target subcircuits within the phase space of theta oscillations. We used temperature manipulation of the MS to test these models. Cooling of the MS reduced both theta frequency and power, was associated with enhanced incidence of errors in a spatial navigation task but did not affect spatial correlates of neurons. MS cooling decreased theta frequency oscillations of place cells, reduced distance-time compression but preserved distance-phase compression of place field sequences within the theta cycle. Thus, septal computation contributes not only theta pacing but is also critical for sustaining precise theta phase-coordination of cell assemblies in the hippocampus.

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

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.

scholarly journals Flexible theta sequence compression mediated via phase precessing interneurons

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Angus Chadwick ◽  
Mark CW van Rossum ◽  
Matthew F Nolan
Keyword(s):  
Action Potentials ◽  
High Capacity ◽  
Theta Oscillations ◽  
Sequence Generation ◽  
Spike Sequences ◽  
Theta Frequency ◽  
Neural Substrate ◽  
Hippocampal Theta ◽  
Novel Model ◽  
Sequence Compression

Encoding of behavioral episodes as spike sequences during hippocampal theta oscillations provides a neural substrate for computations on events extended across time and space. However, the mechanisms underlying the numerous and diverse experimentally observed properties of theta sequences remain poorly understood. Here we account for theta sequences using a novel model constrained by the septo-hippocampal circuitry. We show that when spontaneously active interneurons integrate spatial signals and theta frequency pacemaker inputs, they generate phase precessing action potentials that can coordinate theta sequences in place cell populations. We reveal novel constraints on sequence generation, predict cellular properties and neural dynamics that characterize sequence compression, identify circuit organization principles for high capacity sequential representation, and show that theta sequences can be used as substrates for association of conditioned stimuli with recent and upcoming events. Our results suggest mechanisms for flexible sequence compression that are suited to associative learning across an animal’s lifespan.

scholarly journals Optogenetic activation of SST-positive interneurons restores hippocampal theta oscillation impairment induced by soluble amyloid beta oligomersin vivo

2018 ◽  
Author(s):  
Hyowon Chung ◽  
Kyerl Park ◽  
Hyun Jae Jang ◽  
Michael M Kohl ◽  
Jeehyun Kwag
Keyword(s):  
Learning And Memory ◽  
Peak Power ◽  
Pyramidal Neurons ◽  
Hippocampal Slices ◽  
Field Potential ◽  
Theta Oscillations ◽  
Ca1 Pyramidal Neurons ◽  
Theta Frequency ◽  
Hippocampal Theta

AbstractAbnormal accumulation of amyloid β oligomers (AβO) is a hallmark of Alzheimer’s disease (AD), which leads to learning and memory deficits. Hippocampal theta oscillations that are critical in spatial navigation, learning and memory are impaired in AD. Since GABAergic interneurons, such as somatostatin-positive (SST+) and parvalbumin-positive (PV+) interneurons, are believed to play key roles in the hippocampal oscillogenesis, we asked whether AβO selectively impairs these SST+ and PV+ interneurons. To selectively manipulate SST+ or PV+ interneuron activity in mice with AβO pathologyin vivo, we co-injected AβO and adeno-associated virus (AAV) for expressing floxed channelrhodopsin-2 (ChR2) into the hippocampus of SST-Cre or PV-Cre mice. Local field potential (LFP) recordingsin vivoin these AβO–injected mice showed a reduction in the peak power of theta oscillations and desynchronization of spikes from CA1 pyramidal neurons relative to theta oscillations compared to those in control mice. Optogenetic-activation of SST+ but not PV+ interneurons in AβO–injected mice fully restored the peak power of theta oscillations and resynchronized the theta spike phases to a level observed in control mice.In vitrowhole-cell voltage-clamp recordings in CA1 pyramidal neurons in hippocampal slices treated with AβO revealed that short-term plasticity of SST+ interneuron inhibitory inputs to CA1 pyramidal neurons at theta frequency were selectively disrupted while that of PV+ interneuron inputs were unaffected. Together, our results suggest that dysfunction in inputs from SST+ interneurons to CA1 pyramidal neurons may underlie the impairment of theta oscillations observed in AβO-injected micein vivo.Our findings identify SST+ interneurons as a target for restoring theta-frequency oscillations in early AD.

scholarly journals Learning to synchronize: Midfrontal theta dynamics during rule switching

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.

scholarly journals Thalamic theta phase alignment predicts human memory formation and anterior thalamic cross-frequency coupling

eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
Catherine M Sweeney-Reed ◽  
Tino Zaehle ◽  
Jürgen Voges ◽  
Friedhelm C Schmitt ◽  
Lars Buentjen ◽  
...  
Keyword(s):  
Human Memory ◽  
Gamma Oscillations ◽  
Memory Formation ◽  
Anterior Thalamic Nucleus ◽  
Memory Processing ◽  
Phase Alignment ◽  
Theta Frequency ◽  
Frequency Coupling ◽  
Theta Phase ◽  
Cross Frequency Coupling

Previously we reported electrophysiological evidence for a role for the anterior thalamic nucleus (ATN) in human memory formation (<xref ref-type="bibr" rid="bib29">Sweeney-Reed et al., 2014</xref>). Theta-gamma cross-frequency coupling (CFC) predicted successful memory formation, with the involvement of gamma oscillations suggesting memory-relevant local processing in the ATN. The importance of the theta frequency range in memory processing is well-established, and phase alignment of oscillations is considered to be necessary for synaptic plasticity. We hypothesized that theta phase alignment in the ATN would be necessary for memory encoding. Further analysis of the electrophysiological data reveal that phase alignment in the theta rhythm was greater during successful compared with unsuccessful encoding, and that this alignment was correlated with the CFC. These findings support an active processing role for the ATN during memory formation.

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