Single-trial Phase Research Articles

Estimating Directed Phase-Amplitude Interactions from EEG Data through Kernel-Based Phase Transfer Entropy

Cross-frequency interactions, a form of oscillatory neural activity, are thought to play an essential role in the integration of distributed information in the brain. Indeed, phase-amplitude interactions are believed to allow for the transfer of information from large-scale brain networks, oscillating at low frequencies, to local, rapidly oscillating neural assemblies. A promising approach to estimating such interactions is the use of transfer entropy (TE), a non-linear, information-theory-based effective connectivity measure. The conventional method involves feeding instantaneous phase and amplitude time series, extracted at the target frequencies, to a TE estimator. In this work, we propose that the problem of directed phase-amplitude interaction detection is recast as a phase TE estimation problem, under the hypothesis that estimating TE from data of the same nature, i.e., two phase time series, will improve the robustness to the common confounding factors that affect connectivity measures, such as the presence of high noise levels. We implement our proposal using a kernel-based TE estimator, defined in terms of Renyi’s α entropy, which has successfully been used to compute single-trial phase TE. We tested our approach on the synthetic data generated through a simulation model capable of producing a time series with directed phase-amplitude interactions at two given frequencies, and on EEG data from a cognitive task designed to activate working memory, a memory system whose underpinning mechanisms are thought to include phase–amplitude couplings. Our proposal detected statistically significant interactions between the simulated signals at the desired frequencies for the synthetic data, identifying the correct direction of the interaction. It also displayed higher robustness to noise than the alternative methods. The results attained for the working memory data showed that the proposed approach codes connectivity patterns based on directed phase–amplitude interactions, that allow for the different cognitive load levels of the working memory task to be differentiated.

The pre-stimulus oscillatory alpha phase affects neural correlates of early visual perception

A growing number of studies suggest the phase of ongoing alpha oscillations in the brain influences visual perception. However, it remained largely unconsidered if this is associated with a phase dependence of neurophysiological processes especially in the visual cortex. Therefore, this study investigated the link between the pre-stimulus oscillatory alpha phase and neural correlates of early visual perception.In 64 subjects a 64-channel EEG system was used to examine the phase dependence of pattern-reversal visual evoked potentials (VEP) in a visual perception experiment. The pre-stimulus oscillatory phase over the primary visual cortex was determined for the individual alpha peak frequency (iAPF) as well as the frequency of maximal phase locking (PLFfmax). The phase dependence of VEP latency was determined using single-trial phase sorting.The results indicate a significantly shorter latency for the N75 and P100 components of the VEP between 40°–100° (p < 0.05) and 90°–120° (p < 0.05), respectively when trials were phase-sorted based on the iAPF. In contrast, the PLFfmax phase did not affect the N75 or P100 latency.The study indicates a link between the pre-stimulus alpha phase and neural correlates of early visual perception. These results extend previous behavioral findings to the neurophysiological level and support current models suggesting visual perception is modulated by ongoing alpha oscillations.

Single-Trial Phase Entrainment of Theta Oscillations in Sensory Regions Predicts Human Associative Memory Performance.

Episodic memories are rich in sensory information and often contain integrated information from different sensory modalities. For instance, we can store memories of a recent concert with visual and auditory impressions being integrated in one episode. Theta oscillations have recently been implicated in playing a causal role synchronizing and effectively binding the different modalities together in memory. However, an open question is whether momentary fluctuations in theta synchronization predict the likelihood of associative memory formation for multisensory events. To address this question we entrained the visual and auditory cortex at theta frequency (4 Hz) and in a synchronous or asynchronous manner by modulating the luminance and volume of movies and sounds at 4 Hz, with a phase offset at 0° or 180°. EEG activity from human subjects (both sexes) was recorded while they memorized the association between a movie and a sound. Associative memory performance was significantly enhanced in the 0° compared with the 180° condition. Source-level analysis demonstrated that the physical stimuli effectively entrained their respective cortical areas with a corresponding phase offset. The findings suggested a successful replication of a previous study (Clouter et al., 2017). Importantly, the strength of entrainment during encoding correlated with the efficacy of associative memory such that small phase differences between visual and auditory cortex predicted a high likelihood of correct retrieval in a later recall test. These findings suggest that theta oscillations serve a specific function in the episodic memory system: binding the contents of different modalities into coherent memory episodes.SIGNIFICANCE STATEMENT How multisensory experiences are bound to form a coherent episodic memory representation is one of the fundamental questions in human episodic memory research. Evidence from animal literature suggests that the relative timing between an input and theta oscillations in the hippocampus is crucial for memory formation. We precisely controlled the timing between visual and auditory stimuli and the neural oscillations at 4 Hz using a multisensory entrainment paradigm. Human associative memory formation depends on coincident timing between sensory streams processed by the corresponding brain regions. We provide evidence for a significant role of relative timing of neural theta activity in human episodic memory on a single-trial level, which reveals a crucial mechanism underlying human episodic memory.

Prediction of successful memory encoding based on single-trial rhinal and hippocampal phase information

Mediotemporal EEG characteristics are closely related to long-term memory formation. It has been reported that rhinal and hippocampal EEG measures reflecting the stability of phases across trials are better suited to distinguish subsequently remembered from forgotten trials than event-related potentials or amplitude-based measures. Theoretical models suggest that the phase of EEG oscillations reflects neural excitability and influences cellular plasticity. However, while previous studies have shown that the stability of phase values across trials is indeed a relevant predictor of subsequent memory performance, the effect of absolute single-trial phase values has been little explored. Here, we reanalyzed intracranial EEG recordings from the mediotemporal lobe of 27 epilepsy patients performing a continuous word recognition paradigm. Two-class classification using a support vector machine was performed to predict subsequently remembered vs. forgotten trials based on individually selected frequencies and time points. We demonstrate that it is possible to successfully predict single-trial memory formation in the majority of patients (23 out of 27) based on only three single-trial phase values given by a rhinal phase, a hippocampal phase, and a rhinal-hippocampal phase difference. Overall classification accuracy across all subjects was 69.2% choosing frequencies from the range between 0.5 and 50Hz and time points from the interval between −0.5s and 2s. For 19 patients, above chance prediction of subsequent memory was possible even when choosing only time points from the prestimulus interval (overall accuracy: 65.2%). Furthermore, prediction accuracies based on single-trial phase surpassed those based on single-trial power. Our results confirm the functional relevance of mediotemporal EEG phase for long-term memory operations and suggest that phase information may be utilized for memory enhancement applications based on deep brain stimulation.

Frontoparietal EEG alpha-phase synchrony reflects differential attentional demands during word recall and oculomotor dual-tasks.

To study the relationship between the varying degrees of cognitive load and long-range synchronization among neural networks, we utilized a dual-task paradigm combining concurrent word recall working memory tasks and oculomotor tasks that differentially activate the common frontoparietal (FP) network. We hypothesized that each dual-task combination would generate differential neuronal activation patterns among long-range connection during word retention period. Given that the FP alpha-phase synchronization is involved in attentional top-down processes, one would expect that the long-range synchronization pattern is affected by the degrees of dual-task demand. We measured a single-trial phase locking value in the alpha frequency (8-12 Hz) with electroencephalography in healthy participants. Single-trial phase locking value characterized the synchronization between two brain signals. Our results revealed that different amounts of FP alpha-phase synchronization were produced by different dual-task combinations, particularly during the early phase of the word retention period. These differences were dependent on the individual's working memory capacity and memory load. Our study shows that during dual-task, each oculomotor task, which is subserved by distinct neural network, generates different modulation patterns on long-range neuronal activation and FP alpha-phase synchronization seems to reflect these differential cognitive loads.

Dissociation between the experience-dependent development of hippocampal theta sequences and single-trial phase precession.

Theta sequences are circuit-level activity patterns produced when groups of hippocampal place cells fire in sequences that reflect a compressed behavioral order of place fields within each theta cycle. The high temporal coordination between place cells exhibited in theta sequences is compatible with the induction of synaptic plasticity and has been proposed as one of the mechanisms underlying the encoding of episodic memory of recently acquired experience. Yet how theta sequences develop with experience has not been directly addressed. Here we simultaneously recorded large numbers of cells in the dorsal hippocampal CA1 area from rats exploring on a novel linear track. Although place cell firing activities accurately represented the animal's current location, distinct theta sequences were absent on the first lap but emerged immediately thereafter and remained stable once established. The absence of theta sequences on the first lap was not due to place field instability, decreased overall excitability of place cells, behavior variables, or the absence of individual neuronal phase precession. We observed strong single-lap phase precession in a significant percentage of place fields on the first lap and throughout the recording. Individual neuronal phase precession was stable from the first lap to subsequent laps but, across neurons, phase precession became more synchronized after experience, suggesting a novel mechanism for the generation of theta sequences. These results suggest that experience-independent temporal coding in individual neurons is combined with rapid plasticity of hippocampal neural networks during experience to acquire predictive representations of the immediate future.

Coding of Information in the Phase of Local Field Potentials within Human Medial Temporal Lobe

There is increasing evidence that the phase of ongoing oscillations plays a role in neural coding, but its relative importance throughout the brain has yet to be understood. We assessed single-trial phase coding in four temporal lobe and four frontal lobe regions of the human brain using local field potentials (LFPs) recorded during a card-matching task. In the temporal lobe, classification of correct/incorrect matches based on LFP phase was significantly better than classification based on amplitude and comparable to the full LFP signal. Surprisingly, in these regions, the correct/incorrect mean phases became aligned to one another before they diverged and coded for trial outcome. Neural responses in the amygdala were consistent with a mechanism of phase resetting, while parahippocampal gyrus activity was indicative of evoked potentials. These findings highlight the importance of phase coding in human medial temporal lobe and suggest that different brain regions may represent information in diverse ways.

Single-Trial Phase Precession in the Hippocampus

During the crossing of the place field of a pyramidal cell in the rat hippocampus, the firing phase of the cell decreases with respect to the local theta rhythm. This phase precession is usually studied on the basis of data in which many place field traversals are pooled together. Here we study properties of phase precession in single trials. We found that single-trial and pooled-trial phase precession were different with respect to phase-position correlation, phase-time correlation, and phase range. Whereas pooled-trial phase precession may span 360 degrees , the most frequent single-trial phase range was only approximately 180 degrees. In pooled trials, the correlation between phase and position (r = -0.58) was stronger than the correlation between phase and time (r = -0.27), whereas in single trials these correlations (r = -0.61 for both) were not significantly different. Next, we demonstrated that phase precession exhibited a large trial-to-trial variability. Overall, only a small fraction of the trial-to-trial variability in measures of phase precession (e.g., slope or offset) could be explained by other single-trial properties (such as running speed or firing rate), whereas the larger part of the variability remains to be explained. Finally, we found that surrogate single trials, created by randomly drawing spikes from the pooled data, are not equivalent to experimental single trials: pooling over trials therefore changes basic measures of phase precession. These findings indicate that single trials may be better suited for encoding temporally structured events than is suggested by the pooled data.

Single-trial phase precession in the hippocampus

Single-trial phase precession in the hippocampus

Single-trial phase precession

Event Abstract Back to Event Single-trial phase precession Robert Schmidt1*, Kamran Diba2, Christian Leibold3, Dietmar Schmitz1, Györgi Buzsaki2 and Richard Kempter1 1 BCCN Berlin, Germany 2 Rutgers University, United States 3 BCCN Munich, Germany During the crossing of a place field, the firing phase of the hippocampal place cell decreases with respect to the theta rhythm. This phase precession is usually studied on the basis of trial averages, in which data from many place field traversals are pooled together. Here, we study properties of phase precession in single trials and compare them to properties of trial-average phase precession. We find that single-trial and trial-average phase precession are different with respect to three fundamental properties: phase range, phase-time correlation and phase-position correlation. On the basis of surrogate trials we demonstrate that single trials are not randomly drawn samples from the trial-averages. We propose that due to large trial-to-trial variability, phase precession pooled over trials is more variable. Conference: Bernstein Symposium 2008, Munich, Germany, 8 Oct - 10 Oct, 2008. Presentation Type: Poster Presentation Topic: All Abstracts Citation: Schmidt R, Diba K, Leibold C, Schmitz D, Buzsaki G and Kempter R (2008). Single-trial phase precession. Front. Comput. Neurosci. Conference Abstract: Bernstein Symposium 2008. doi: 10.3389/conf.neuro.10.2008.01.111 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 18 Nov 2008; Published Online: 18 Nov 2008. * Correspondence: Robert Schmidt, BCCN Berlin, 82152 Planegg-Martinsried, Germany, robert.schmidt@brainlinks-braintools.uni-freiburg.de Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Robert Schmidt Kamran Diba Christian Leibold Dietmar Schmitz Györgi Buzsaki Richard Kempter Google Robert Schmidt Kamran Diba Christian Leibold Dietmar Schmitz Györgi Buzsaki Richard Kempter Google Scholar Robert Schmidt Kamran Diba Christian Leibold Dietmar Schmitz Györgi Buzsaki Richard Kempter PubMed Robert Schmidt Kamran Diba Christian Leibold Dietmar Schmitz Györgi Buzsaki Richard Kempter Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

STUDYING SINGLE-TRIALS OF PHASE SYNCHRONOUS ACTIVITY IN THE BRAIN

This paper introduces a new method, single-trial phase locking statistics (S-PLS) to estimate phase locking in single trials of brain signals between two electrodes. The possibility of studying single trials removes an important limitation in the study of long-range synchrony in brain signals. S-PLS is closely related to our previous method, phase locking statistics (PLS) that estimates phase locking over a set of trials. The S-PLS method is described in detail and applied to human surface recordings during the task of face-recognition. We compare these results with those provided by PLS and show that they are qualitatively very similar, although S-PLS provides better discrimination of synchronic episodes.