Cross-frequency Dynamics Research Articles

Imagined speech can be decoded from low- and cross-frequency intracranial EEG features

Reconstructing intended speech from neural activity using brain-computer interfaces holds great promises for people with severe speech production deficits. While decoding overt speech has progressed, decoding imagined speech has met limited success, mainly because the associated neural signals are weak and variable compared to overt speech, hence difficult to decode by learning algorithms. We obtained three electrocorticography datasets from 13 patients, with electrodes implanted for epilepsy evaluation, who performed overt and imagined speech production tasks. Based on recent theories of speech neural processing, we extracted consistent and specific neural features usable for future brain computer interfaces, and assessed their performance to discriminate speech items in articulatory, phonetic, and vocalic representation spaces. While high-frequency activity provided the best signal for overt speech, both low- and higher-frequency power and local cross-frequency contributed to imagined speech decoding, in particular in phonetic and vocalic, i.e. perceptual, spaces. These findings show that low-frequency power and cross-frequency dynamics contain key information for imagined speech decoding.

Tracking transient changes in the intrinsic neural frequency architecture: Oxytocin facilitates non-harmonic relationships between alpha and theta rhythms in the resting brain

Shifts in the peak frequencies of oscillatory neural rhythms have been put forward as a principal mechanism by which cross-frequency coupling and decoupling is implemented in the brain. This notion is based on the mathematical reality that neural oscillations can only fully synchronize when their peak frequencies form harmonic 2:1 relationships (e.g., f2=f1/2). Non-harmonic cross-frequency relationships, on the other hand (based on the irrational golden mean 1.618.:1), provide the highest physiologically possible desynchronized state (reducing the occurrence of spurious, noisy, background coupling), and are therefore anticipated to characterize the resting state of the brain, in which no selective information processing takes place. The present study sought to assess whether the transient occurrence of 1.6:1 non-harmonic and 2:1 harmonic relationships between peak frequencies in the alpha (8–14 Hz) and theta (4–8 Hz) bands – respectively facilitating states of decoupling or coupling between oscillatory rhythms – are impacted by the intranasal administration of a single-dose of oxytocin (OT) or placebo. To do so, continuous resting-state electroencephalography (5 min eyes open, 19 electrodes) was obtained from 96 healthy adult men before and after nasal spray administration. The transient formation of non-harmonic cross-frequency configurations between alpha and theta peak frequencies was significantly increased after OT nasal spray administration, indicating an effect of OT on reducing the intrinsic occurrence of spurious (noisy) background phase synchronizations during resting-state. As a group, the OT group also showed a significant parallel increase in high-frequency and decrease in low-frequency heart rate variability, confirming a homeostatic role of OT in balancing parasympathetic drive. Overall, non-harmonic cross-frequency configurations have been put forward to lay the ground for a healthy neural network allowing the opportunity for an efficient transition from resting state to activity. The observed effects of OT on cross-frequency dynamics are therefore interpreted to reflect a homeostatic role of OT in increasing the signal-to-noise properties of the intrinsic EEG neural frequency architecture, i.e., by precluding the occurrence of ‘noisy’, unwanted, spurious couplings among neural rhythms in the resting brain.

Mindfulness Training is Associated with Changes in Alpha-Theta Cross-Frequency Dynamics During Meditation

ObjectivesPrevious literature suggests that cross-frequency phase synchronization is a mechanism by which information is transmitted and coordinated in the brain. Since cross-frequency phase synchronization is only strictly possible when two oscillators form a harmonic frequency ratio (e.g., 2:1, 3:1), a recent theory posited that interactions between brain oscillations at different frequencies are facilitated/hindered by the transient occurrence of harmonic/non-harmonic cross-frequency arrangements. In this line, recent evidence has shown that 2:1 harmonic relationships between alpha (8–14 Hz) and theta (4–8 Hz) rhythms are reduced during meditative states in experienced practitioners. In the present study, we investigated whether mindfulness training in novices is associated with longitudinal changes in alpha-theta cross-frequency dynamics during meditation practice.MethodsThirty-six participants (mean age = 30.3; 2 men) underwent an 8-week mindfulness training program based on the mindfulness-based stress reduction (MBSR) syllabus and electroencephalography (EEG) recordings (64 electrodes) were performed during a guided meditation before and after the training.ResultsMindfulness training compliance (quantified by minutes of attendance and practice at home) was significantly correlated to decreased 3:1 harmonicity and cross-frequency phase synchrony between alpha and theta rhythms during meditation.ConclusionsMindfulness training in novices was shown to be associated with a reduction in alpha-theta cross-frequency coupling during meditation. EEG parameters based on alpha-theta cross-frequency dynamics may be adequate for quantifying and/or facilitating mindfulness meditation training.

Spectral-power associations reflect amplitude modulation and within-frequency interactions on the sub-second timescale and cross-frequency interactions on the seconds timescale.

We investigated the global structure of intrinsic cross-frequency dynamics by systematically examining power-based temporal associations among a broad range of oscillation frequencies both within and across EEG-based current sources (sites). We focused on power-based associations that could reveal unique timescale dependence independently of interacting frequencies. Large spectral-power fluctuations across all sites occurred at two characteristic timescales, sub-second and seconds, yielding distinct patterns of cross-frequency associations. On the fast sub-second timescale, within-site (local) associations were consistently between pairs of β-γ frequencies differing by a constant Δf (particularly Δf ~ 10 Hz at posterior sites and Δf ~ 16 Hz at lateral sites) suggesting that higher-frequency oscillations are organized into Δf amplitude-modulated packets, whereas cross-site (long-distance) associations were all within-frequency (particularly in the >30 Hz and 6-12 Hz ranges, suggestive of feedforward and feedback interactions). On the slower seconds timescale, within-site (local) associations were characterized by a broad range of frequencies selectively associated with ~10 Hz at posterior sites and associations among higher (>20 Hz) frequencies at lateral sites, whereas cross-site (long-distance) associations were characterized by a broad range of frequencies at posterior sites selectively associated with ~10 Hz at other sites, associations among higher (>20 Hz) frequencies among lateral and anterior sites, and prevalent associations at ~10 Hz. Regardless of timescale, within-site (local) cross-frequency associations were weak at anterior sites indicative of frequency-specific operations. Overall, these results suggest that the fast sub-second-timescale coordination of spectral power is limited to local amplitude modulation and insulated within-frequency long-distance interactions (likely feedforward and feedback interactions), while characteristic patterns of cross-frequency interactions emerge on the slower seconds timescale. The results also suggest that the occipital α oscillations play a role in organizing higher-frequency oscillations into ~10 Hz amplitude-modulated packets to communicate with other regions. Functional implications of these timescale-dependent cross-frequency associations await future investigations.

From thoughtless awareness to effortful cognition: alpha - theta cross-frequency dynamics in experienced meditators during meditation, rest and arithmetic

Neural activity is known to oscillate within discrete frequency bands and the synchronization between these rhythms is hypothesized to underlie information integration in the brain. Since strict synchronization is only possible for harmonic frequencies, a recent theory proposes that the interaction between different brain rhythms is facilitated by transient harmonic frequency arrangements. In this line, it has been recently shown that the transient occurrence of 2:1 harmonic cross-frequency relationships between alpha and theta rhythms (i.e. falpha ≈ 12 Hz; ftheta ≈ 6 Hz) is enhanced during effortful cognition. In this study, we tested whether achieving a state of ‘mental emptiness’ during meditation is accompanied by a relative decrease in the occurrence of 2:1 harmonic cross-frequency relationships between alpha and theta rhythms. Continuous EEG recordings (19 electrodes) were obtained from 43 highly experienced meditators during meditation practice, rest and an arithmetic task. We show that the occurrence of transient alpha:theta 2:1 harmonic relationships increased linearly from a meditative to an active cognitive processing state (i.e. meditation < rest < arithmetic task). It is argued that transient EEG cross-frequency arrangements that prevent alpha:theta cross-frequency coupling could facilitate the experience of ‘mental emptiness’ by avoiding the interaction between the memory and executive components of cognition.

Midfrontal theta phase coordinates behaviorally relevant brain computations during cognitive control

Neural oscillations are thought to provide a cyclic time frame for orchestrating brain computations. Following this assumption, midfrontal theta oscillations have recently been proposed to temporally organize brain computations during conflict processing. Using a multivariate analysis approach, we show that brain-behavior relationships during conflict tasks are modulated according to the phase of ongoing endogenous midfrontal theta oscillations recorded by scalp EEG. We found reproducible results in two independent datasets, using two different conflict tasks: brain-behavior relationships (correlation between reaction time and theta power) were theta phase-dependent in a subject-specific manner, and these “behaviorally optimal” theta phases were also associated with fronto-parietal cross-frequency dynamics emerging as theta phase-locked beta power bursts. These effects were present regardless of the strength of conflict. Thus, these results provide empirical evidence that midfrontal theta oscillations are involved in cyclically orchestrating brain computations likely related to response execution during the tasks rather than purely related to conflict processing. More generally, this study supports the hypothesis that phase-based computation is an important mechanism giving rise to cognitive processing.

Tracking Transient Changes in the Neural Frequency Architecture: Harmonic Relationships between Theta and Alpha Peaks Facilitate Cognitive Performance.

The synchronization between neural oscillations at different frequencies has been proposed as a core mechanism for the coordination and integration of neural systems at different spatiotemporal scales. Because neural oscillations of different frequencies can only fully synchronize when their "peak" frequencies form harmonic relationships (e.g., f2 = f1/2), the present study explored whether the transient occurrence of harmonic cross-frequency relationship between task-relevant rhythms underlies efficient cognitive processing. Continuous EEG recordings (51 human participants; 14 males) were obtained during an arithmetic task, rest and breath focus. In two separate experiments, we consistently show that the proportion of epochs displaying a 2:1 harmonic relationship between alpha (8-14 Hz) and theta (4-8 Hz) peak frequencies (i.e., alphapeak ≈ 10.6 Hz; thetapeak ≈ 5.3 Hz), was significantly higher when cognitive demands increased. In addition, a higher incidence of 2:1 harmonic cross-frequency relationships was significantly associated with increased alpha-theta phase synchrony and improved arithmetic task performance, thereby underlining the functional relevance of this cross-frequency configuration. Notably, opposite dynamics were identified for a specific range of "nonharmonic" alpha-theta cross-frequency relationships (i.e., alphapeak/thetapeak = 1.1-1.6), which showed a higher incidence during rest compared with the arithmetic task. The observation that alpha and theta rhythms shifted into harmonic versus nonharmonic cross-frequency relationships depending on (cognitive) task demands is in line with the notion that the neural frequency architecture entails optimal frequency arrangements to facilitate cross-frequency "coupling" and "decoupling".SIGNIFICANCE STATEMENT Neural activity is known to oscillate within discrete frequency bands and the interplay between these brain rhythms is hypothesized to underlie cognitive functions. A recent theory posits that shifts in the peak frequencies of oscillatory rhythms form the principal mechanism by which cross-frequency coupling and decoupling is implemented in the brain. In line with this notion, we show that the occurrence of a cross-frequency arrangement that mathematically enables coupling between alpha and theta rhythms is more prominent during active cognitive processing (compared with rest and non-cognitively demanding tasks) and is associated with improved cognitive performance. Together, our results open new vistas for future research on cross-frequency dynamics in the brain and their functional role in cognitive processing.

Theta modulation of inter-regional gamma synchronization during auditory attention control

Synchronization of gamma oscillations among brain regions is relevant for dynamically organizing communication among neurons to support cognitive and perceptual processing, including attention orienting. Recent research has demonstrated that inter-regional synchronization in the gamma-band is modulated by theta rhythms during cortical processing. It has been proposed that such cross-frequency dynamics underlie the integration of local processes into large-scale functional networks. To investigate the potential role of theta-gamma mechanisms during auditory attention control, we localized activated regions using EEG beamformer analysis, and calculated inter-regional gamma-band synchronization between activated regions as well as modulation of inter-regional gamma-band synchronization by the phase of cortical theta rhythms. Abundant synchronization of gamma-band oscillations among regions comprising the auditory attention control network was observed. This inter-regional gamma synchronization was modulated by theta phase. These results provide further evidence implicating inter-regional gamma-band synchronization, and theta-gamma interactions, in task-dependent communication among cortical regions, and provide the first evidence that such mechanisms are relevant for auditory attention control.