Theta-band Oscillations Research Articles

Temporally and spatially distinct theta oscillations dissociate a language-specific from a domain-general processing mechanism across the age trajectory

The cognitive functionality of neural oscillations is still highly debated, as different functions have been associated with identical frequency ranges. Theta band oscillations, for instance, were proposed to underlie both language comprehension and domain-general cognitive abilities. Here we show that the ageing brain can provide an answer to the open question whether it is one and the same theta oscillation underlying those functions, thereby resolving a long-standing paradox. While better cognitive functioning is predicted by low theta power in the brain at rest, resting state (RS) theta power declines with age, but sentence comprehension deteriorates in old age. We resolve this paradox showing that sentence comprehension declines due to changes in RS theta power within domain-general brain networks known to support successful sentence comprehension, while low RS theta power within the left-hemispheric dorso-frontal language network predicts intact sentence comprehension. The two RS theta networks were also found to functionally decouple relative to their independent internal coupling. Thus, both temporally and spatially distinct RS theta oscillations dissociate a language-specific from a domain-general processing mechanism.

149 Human Subthalamic Nucleus Neurons Exhibit Increased Theta-band Phase-locking During High-conflict Decision Making

Abstract INTRODUCTION The subthalamic nucleus (STN) is thought to be preferentially engaged during high-conflict decision making in humans. The population neuronal spike rate in the STN has been reported to increase during decision conflict. Conflict and feedback-related activity is also reflected in theta-band (4-8 Hz) oscillations in the STN. It remains unknown how single-neuron activity and theta-band local field potentials (LFP) oscillations interact to support decision making. METHODS We simultaneously recorded single-neuron spike activity and LFP from the STN of eight Parkinson's disease (PD) patients while they performed a novel Aversion-Reward conflict (ARC) task. Subjects decide whether to accept an offer of a monetary reward paired with a variable risk of an aversive air puff to the eye. By varying the reward and risk, we are able to study approach-avoidance decision making across a range of conflict. Using this task, we examined the mechanism of how theta-frequency oscillation and entrained single neurons involve humans' integration of cost and benefit and decision at various conflict statuses. RESULTS >The ARC task reveals diverse risk-reward tradeoff strategies of patients. Consistent across patients, there is a positive correlation between the degree of decision conflict and reaction time (e.g., higher conflict offers require longer for subjects to decide). During high-conflict decisions, LFP in STN had increased activity of sub-theta oscillation, while increased activity of theta was found during low-conflict decisions. Single-trial STN theta-band power was correlated with degree of decision conflict. Interestingly, the decision to take or forgo the reward is predicted by theta-frequency phase-locked of STN neurons. CONCLUSION Our findings support the hypothesis that theta-band oscillations in single-neurons reflect the engagement of STN during conflict decision making. Furthermore, STN neurons with theta-band entrainment correlate with willingness to approach risk to pursue reward.

Inter-trial coherence of medial frontal theta oscillations linked to differential feedback processing in youth and young adults with autism

BackgroundImpairment in prediction and appreciation for choice outcomes could contribute to several core symptoms of ASD. We examined electroencephalography (EEG) oscillations in 27 youth and young adults diagnosed with autism spectrum disorder (ASD) and 22 IQ-matched neurotypical controls while they performed a chance-based reward prediction task. MethodWe re-analyzed our previously published ERP data (Larson et al., 2011) and examined theta band oscillations (4–8Hz) at frontal midline sites, within a timing window that overlaps with the feedback-related negativity (FRN). We focused on event-related changes after presentation of feedback for reward (WIN) and punitive (LOSE) outcomes, both for spectral power and inter-trial phase coherence. ResultsIn our reward prediction task, for both groups, medial frontal theta power and phase coherence were greater following LOSE compared to WIN feedback. However, compared to controls, inter-trial coherence of medial frontal theta was significantly lower overall (across both feedback types) for individuals with ASD. Our results indicate that while individuals with ASD are sensitive to the valence of reward feedback, comparable to their neurotypical peers, they have reduced synchronization of medial frontal theta activity during feedback processing. ConclusionsThis finding is consistent with previous studies showing neural variability in ASD and suggest that the processes underlying decision-making and reinforcement learning may be atypical and less efficient in ASD.

Genetic influences on functional connectivity associated with feedback processing and prediction error: Phase coupling of theta-band oscillations in twins

Detection and evaluation of the mismatch between the intended and actually obtained result of an action (reward prediction error) is an integral component of adaptive self-regulation of behavior. Extensive human and animal research has shown that evaluation of action outcome is supported by a distributed network of brain regions in which the anterior cingulate cortex (ACC) plays a central role, and the integration of distant brain regions into a unified feedback-processing network is enabled by long-range phase synchronization of cortical oscillations in the theta band. Neural correlates of feedback processing are associated with individual differences in normal and abnormal behavior, however, little is known about the role of genetic factors in the cerebral mechanisms of feedback processing. Here we examined genetic influences on functional cortical connectivity related to prediction error in young adult twins (age 18, n=399) using event-related EEG phase coherence analysis in a monetary gambling task. To identify prediction error-specific connectivity pattern, we compared responses to loss and gain feedback. Monetary loss produced a significant increase of theta-band synchronization between the frontal midline region and widespread areas of the scalp, particularly parietal areas, whereas gain resulted in increased synchrony primarily within the posterior regions. Genetic analyses showed significant heritability of frontoparietal theta phase synchronization (24 to 46%), suggesting that individual differences in large-scale network dynamics are under substantial genetic control. We conclude that theta-band synchronization of brain oscillations related to negative feedback reflects genetically transmitted differences in the neural mechanisms of feedback processing. To our knowledge, this is the first evidence for genetic influences on task-related functional brain connectivity assessed using direct real-time measures of neuronal synchronization.

The functional role of human right hippocampal/parahippocampal theta rhythm in environmental encoding during virtual spatial navigation.

Low frequency theta band oscillations (4-8 Hz) are thought to provide a timing mechanism for hippocampal place cell firing and to mediate the formation of spatial memory. In rodents, hippocampal theta has been shown to play an important role in encoding a new environment during spatial navigation, but a similar functional role of hippocampal theta in humans has not been firmly established. To investigate this question, we recorded healthy participants' brain responses with a 160-channel whole-head MEG system as they performed two training sets of a virtual Morris water maze task. Environment layouts (except for platform locations) of the two sets were kept constant to measure theta activity during spatial learning in new and familiar environments. In line with previous findings, left hippocampal/parahippocampal theta showed more activation navigating to a hidden platform relative to random swimming. Consistent with our hypothesis, right hippocampal/parahippocampal theta was stronger during the first training set compared to the second one. Notably, theta in this region during the first training set correlated with spatial navigation performance across individuals in both training sets. These results strongly argue for the functional importance of right hippocampal theta in initial encoding of configural properties of an environment during spatial navigation. Our findings provide important evidence that right hippocampal/parahippocampal theta activity is associated with environmental encoding in the human brain. Hum Brain Mapp 38:1347-1361, 2017. © 2016 Wiley Periodicals, Inc.

Reduced frontal theta oscillations indicate altered crossmodal prediction error processing in schizophrenia.

Our brain generates predictions about forthcoming stimuli and compares predicted with incoming input. Failures in predicting events might contribute to hallucinations and delusions in schizophrenia (SZ). When a stimulus violates prediction, neural activity that reflects prediction error (PE) processing is found. While PE processing deficits have been reported in unisensory paradigms, it is unknown whether SZ patients (SZP) show altered crossmodal PE processing. We measured high-density electroencephalography and applied source estimation approaches to investigate crossmodal PE processing generated by audiovisual speech. In SZP and healthy control participants (HC), we used an established paradigm in which high- and low-predictive visual syllables were paired with congruent or incongruent auditory syllables. We examined crossmodal PE processing in SZP and HC by comparing differences in event-related potentials and neural oscillations between incongruent and congruent high- and low-predictive audiovisual syllables. In both groups event-related potentials between 206 and 250 ms were larger in high- compared with low-predictive syllables, suggesting intact audiovisual incongruence detection in the auditory cortex of SZP. The analysis of oscillatory responses revealed theta-band (4-7 Hz) power enhancement in high- compared with low-predictive syllables between 230 and 370 ms in the frontal cortex of HC but not SZP. Thus aberrant frontal theta-band oscillations reflect crossmodal PE processing deficits in SZ. The present study suggests a top-down multisensory processing deficit and highlights the role of dysfunctional frontal oscillations for the SZ psychopathology.

Genetic influences on phase synchrony of brain oscillations supporting response inhibition

Phase synchronization of neuronal oscillations is a fundamental mechanism underlying cognitive processing and behavior, including context-dependent response production and inhibition. Abnormalities in neural synchrony can lead to abnormal information processing and contribute to cognitive and behavioral deficits in neuropsychiatric disorders. However, little is known about genetic and environmental contributions to individual differences in cortical oscillatory dynamics underlying response inhibition. This study examined heritability of event-related phase synchronization of brain oscillations in 302 young female twins including 94 MZ and 57 DZ pairs performing a cued Go/No-Go version of the Continuous Performance Test (CPT). We used the Phase Locking Index (PLI) to assess inter-trial phase clustering (synchrony) in several frequency bands in two time intervals after stimulus onset (0–300 and 301–600ms). Response inhibition (i.e., successful response suppression in No-Go trials) was characterized by a transient increase in phase synchronization of delta- and theta-band oscillations in the fronto-central midline region. Genetic analysis showed significant heritability of the phase locking measures related to response inhibition, with 30 to 49% of inter-individual variability being accounted for by genetic factors. This is the first study providing evidence for heritability of task-related neural synchrony. The present results suggest that PLI can serve as an indicator of genetically transmitted individual differences in neural substrates of response inhibition.

PM370. Mismatch negativity and theta band oscillation in schizophrenia and rodent NMDAR models

PM370. Mismatch negativity and theta band oscillation in schizophrenia and rodent NMDAR models

The Functional Role of Neural Oscillations in Non-Verbal Emotional Communication.

Effective interpersonal communication depends on the ability to perceive and interpret nonverbal emotional expressions from multiple sensory modalities. Current theoretical models propose that visual and auditory emotion perception involves a network of brain regions including the primary sensory cortices, the superior temporal sulcus (STS), and orbitofrontal cortex (OFC). However, relatively little is known about how the dynamic interplay between these regions gives rise to the perception of emotions. In recent years, there has been increasing recognition of the importance of neural oscillations in mediating neural communication within and between functional neural networks. Here we review studies investigating changes in oscillatory activity during the perception of visual, auditory, and audiovisual emotional expressions, and aim to characterize the functional role of neural oscillations in nonverbal emotion perception. Findings from the reviewed literature suggest that theta band oscillations most consistently differentiate between emotional and neutral expressions. While early theta synchronization appears to reflect the initial encoding of emotionally salient sensory information, later fronto-central theta synchronization may reflect the further integration of sensory information with internal representations. Additionally, gamma synchronization reflects facilitated sensory binding of emotional expressions within regions such as the OFC, STS, and, potentially, the amygdala. However, the evidence is more ambiguous when it comes to the role of oscillations within the alpha and beta frequencies, which vary as a function of modality (or modalities), presence or absence of predictive information, and attentional or task demands. Thus, the synchronization of neural oscillations within specific frequency bands mediates the rapid detection, integration, and evaluation of emotional expressions. Moreover, the functional coupling of oscillatory activity across multiples frequency bands supports a predictive coding model of multisensory emotion perception in which emotional facial and body expressions facilitate the processing of emotional vocalizations.

Dissociation of the functional relevance of different pre-stimulus oscillatory activity for memory formation

The state of a neural assembly preceding an incoming stimulus modulates the processing of that subsequently presented stimuli. For human memory formation, the role of oscillatory brain activity within different frequency ranges has been discussed but a more functional relation could not be established. In the present Experiment I, an increase of pre-stimulus theta- (3–7Hz) and beta- (13–17Hz) band oscillations during encoding for later remembered stimuli was observed. To establish a more direct functional relation, we adopted a novel brain–computer-interface (BCI) method to selectively detect oscillatory activity in real-time combined with an adaptive stimulus presentation at different levels of activity. Therefore, in the second experiment the BCI was used to present the visual stimuli with a high temporal resolution directly within defined brain states of beta- or theta-band activity. The quality of the subsequent processing of the stimuli was assessed at the behavioral level with a surprise recognition task. Results revealed a variation of memory performance in direct relation to the amount of pre-stimulus beta- but not theta-band oscillations, suggesting a functional relevance of beta-band oscillations for memory encoding. Thus, the BCI method enabled a more functional differentiation of the effective role of ongoing oscillatory activity.

Behavioral oscillation in priming: competing perceptual predictions conveyed in alternating theta-band rhythms

The brain constantly creates perceptual predictions about forthcoming stimuli to guide perception efficiently. Abundant studies have demonstrated that perceptual predictions modulate sensory activities depending on whether the actual inputs are consistent with one particular prediction. In real-life contexts, however, multiple and even conflicting predictions might concurrently exist to be tested, requiring a multiprediction coordination process. It remains largely unknown how multiple hypotheses are conveyed and harmonized to guide moment-by-moment perception. Based on recent findings revealing that multiple locations are sampled alternatively in various phase of attentional rhythms, we hypothesize that this oscillation-based temporal organization mechanism may also underlie the multiprediction coordination process. To address the issue, we used well established priming paradigms in combination with a time-resolved behavioral approach to investigate the fine temporal dynamics of the multiprediction harmonization course in human subjects. We first replicate classical priming effects in slowly developing trends of priming time courses. Second, after removing the typical priming patterns, we reveal a new theta-band (∼4 Hz) oscillatory component in the priming behavioral data regardless of whether the prime was masked. Third, we show that these theta-band priming oscillations triggered by congruent and incongruent primes are in an out-of-phase relationship. These findings suggest that perceptual predictions return to low-sensory areas not continuously but recurrently in a theta-band rhythm (every 200-300 ms) and that multiple predictions are dynamically coordinated in time by being conveyed in different phases of the theta-band oscillations to achieve dissociated but temporally organized neural representations.

Human brain mapping of theta-band behavioral oscillations in masked priming

Human brain mapping of theta-band behavioral oscillations in masked priming

Neural correlates of time-resolved behavioral responses reveal theta-band oscillations in the fusiform face area and parahippocampal place area

Neural correlates of time-resolved behavioral responses reveal theta-band oscillations in the fusiform face area and parahippocampal place area

Synergy of direct and indirect cholinergic septo-hippocampal pathways coordinates firing in hippocampal networks.

The medial septum/diagonal band of Broca complex (MSDB) is a key structure that modulates hippocampal rhythmogenesis. Cholinergic neurons of the MSDB play a central role in generating and pacing theta-band oscillations in the hippocampal formation during exploration, novelty detection, and memory encoding. How precisely cholinergic neurons affect hippocampal network dynamics in vivo, however, has remained elusive. In this study, we show that stimulation of cholinergic MSDB neurons in urethane-anesthetized mice acts on hippocampal networks via two distinct pathways. A direct septo-hippocampal cholinergic projection causes increased firing of hippocampal inhibitory interneurons with concomitantly decreased firing of principal cells. In addition, cholinergic neurons recruit noncholinergic neurons within the MSDB. This indirect pathway is required for hippocampal theta synchronization. Activation of both pathways causes a reduction in pyramidal neuron firing and a more precise coupling to the theta oscillatory phase. These two anatomically and functionally distinct pathways are likely relevant for cholinergic control of encoding versus retrieval modes in the hippocampus.

Neural mechanisms of infant learning: differences in frontal theta activity during object exploration modulate subsequent object recognition.

Investigating learning mechanisms in infancy relies largely on behavioural measures like visual attention, which often fail to predict whether stimuli would be encoded successfully. This study explored EEG activity in the theta frequency band, previously shown to predict successful learning in adults, to directly study infants' cognitive engagement, beyond visual attention. We tested 11-month-old infants (N = 23) and demonstrated that differences in frontal theta-band oscillations, recorded during infants' object exploration, predicted differential subsequent recognition of these objects in a preferential-looking test. Given that theta activity is modulated by motivation to learn in adults, these findings set the ground for future investigation into the drivers of infant learning.

Functional role of delta and theta band oscillations for auditory feedback processing during vocal pitch motor control.

The answer to the question of how the brain incorporates sensory feedback and links it with motor function to achieve goal-directed movement during vocalization remains unclear. We investigated the mechanisms of voice pitch motor control by examining the spectro-temporal dynamics of EEG signals when non-musicians (NM), relative pitch (RP), and absolute pitch (AP) musicians maintained vocalizations of a vowel sound and received randomized ± 100 cents pitch-shift stimuli in their auditory feedback. We identified a phase-synchronized (evoked) fronto-central activation within the theta band (5–8 Hz) that temporally overlapped with compensatory vocal responses to pitch-shifted auditory feedback and was significantly stronger in RP and AP musicians compared with non-musicians. A second component involved a non-phase-synchronized (induced) frontal activation within the delta band (1–4 Hz) that emerged at approximately 1 s after the stimulus onset. The delta activation was significantly stronger in the NM compared with RP and AP groups and correlated with the pitch rebound error (PRE), indicating the degree to which subjects failed to re-adjust their voice pitch to baseline after the stimulus offset. We propose that the evoked theta is a neurophysiological marker of enhanced pitch processing in musicians and reflects mechanisms by which humans incorporate auditory feedback to control their voice pitch. We also suggest that the delta activation reflects adaptive neural processes by which vocal production errors are monitored and used to update the state of sensory-motor networks for driving subsequent vocal behaviors. This notion is corroborated by our findings showing that larger PREs were associated with greater delta band activity in the NM compared with RP and AP groups. These findings provide new insights into the neural mechanisms of auditory feedback processing for vocal pitch motor control.

Behavioral oscillation in priming: competing perceptual predictions conveyed in alternating theta-band rhythms.

The brain constantly creates perceptual predictions about forthcoming stimuli to guide perception efficiently. Abundant studies have demonstrated that perceptual predictions modulate sensory activities depending on whether the actual inputs are consistent with one particular prediction. In real-life contexts, however, multiple and even conflicting predictions might concurrently exist to be tested, requiring a multiprediction coordination process. It remains largely unknown how multiple hypotheses are conveyed and harmonized to guide moment-by-moment perception. Based on recent findings revealing that multiple locations are sampled alternatively in various phase of attentional rhythms, we hypothesize that this oscillation-based temporal organization mechanism may also underlie the multiprediction coordination process. To address the issue, we used well established priming paradigms in combination with a time-resolved behavioral approach to investigate the fine temporal dynamics of the multiprediction harmonization course in human subjects. We first replicate classical priming effects in slowly developing trends of priming time courses. Second, after removing the typical priming patterns, we reveal a new theta-band (∼4 Hz) oscillatory component in the priming behavioral data regardless of whether the prime was masked. Third, we show that these theta-band priming oscillations triggered by congruent and incongruent primes are in an out-of-phase relationship. These findings suggest that perceptual predictions return to low-sensory areas not continuously but recurrently in a theta-band rhythm (every 200-300 ms) and that multiple predictions are dynamically coordinated in time by being conveyed in different phases of the theta-band oscillations to achieve dissociated but temporally organized neural representations.

Cortical EEG components that reflect inverse effectiveness during visuotactile integration processing

Multisensory integration is required to interpret information from multiple senses and then produce the appropriate behavioral output. Inverse effectiveness, a phenomenon in which weaker stimuli induce greater activation of multisensory neurons than do stronger stimuli, is an essential component of multisensory integration. The superior colliculus is especially abundant in multisensory neurons with properties of inverse effectiveness. However, multisensory neurons are distributed throughout the brain, suggesting that a wide range of brain regions are involved in generating multisensory behavior in addition to the superior colliculus. In this study, we aimed to use scalp EEG to elucidate the cortical responses that respond to multisensory stimuli according to the principle of inverse effectiveness. By modulating the intensity of the tactile aspect of a simultaneous visuotactile stimulus, we explored the time–frequency component of scalp EEG waveforms produced during multi-sensory stimulation. Using this method, we determined the relative values and temporal dynamics of the increment of power spectrum (event-related spectrum perturbation) and phase coherence across trials (e.g., inter-trial phase coherency) produced by multisensory stimulation compared to unisensory stimulation. In the somatosensory and anterior cingulate cortices, we observed significant differences in the inter-trial phase coherence of the theta band oscillation 200–400ms post-stimulus, in response to visuotactile (multisensory) and tactile (unisensory) stimulation, while no differences were found in later time windows and other cortical areas. These results suggest that inverse effectiveness is an important aspect of multi-sensory processing in the somato-sensory and frontal cerebral cortices.

Altered frequency distribution in the electroencephalogram is correlated to the analgesic effect of remifentanil.

Opioids alter resting state brain oscillations by multiple and complex factors, which are still to be elucidated. To increase our knowledge, multi-channel electroencephalography (EEG) was subjected to multivariate pattern analysis (MVPA), to identify the most descriptive frequency bands and scalp locations altered by remifentanil in healthy volunteers. Sixty-two channels of resting EEG followed by independent measures of pain scores to heat and bone pain were recorded in 21 healthy males before and during remifentanil infusion in a placebo-controlled, double-blind crossover study. EEG frequency distributions were extracted by a continuous wavelet transform and normalized into delta, theta, alpha, beta and gamma bands. Alterations relative to pre-treatment responses were calculated for all channels and used as input to the MVPA. Compared to placebo, remifentanil increased the delta band and decreased the theta and alpha band oscillations as a mean over all channels (all p ≤ 0.007). The most discriminative channels in these frequency bands were F1 in delta (83.33%, p = 0.0023) and theta bands (95.24%, p < 0.0001), and C6 in the alpha band (80.95%, p = 0.0054). These alterations were correlated to individual changes in heat pain in the delta (p = 0.045), theta (p = 0.038) and alpha (p = 0.039) bands and to bone pain in the alpha band (p = 0.0092). Hence, MVPA of multi-channel EEG was able to identify frequency bands and corresponding channels most sensitive to altered brain activity during remifentanil treatment. As the EEG alterations were correlated to the analgesic effect, the approach may prove to be a novel methodology for monitoring individual efficacy to opioids.

Long range temporal correlations in EEG oscillations of subclinically depressed individuals: their association with brooding and suppression.

Long-range temporal correlations (LRTC) in brain oscillations have been found to be associated with depression severity in clinically depressed patients. Less is known, however, about the relationships between LRTC and proneness to engage in depression-related cognitive emotion regulation (ER) strategies which characterize both clinically and subclinically depressed (SBD) people. In this study we applied detrended fluctuation analysis to the amplitude envelope of broad band, theta band, and alpha band spontaneous EEG oscillations of a group of SBD individuals and a group of non-depressed individuals (both groups from a sample of healthy adults, N=120), to whom brooding and thought suppression questionnaires were administered. Between-groups differences were not found for any band scaling exponents at any brain location, but linear correlations pointed out several associations between exponents at frontal, central, parietal, temporal, and occipital sites and maladaptive ER strategies. These results suggest that alterations in brain dynamics are related with the proneness that depressive individuals show to engage in brooding and thought suppression in order to cognitively regulate their emotions.