Fast and Slow Rhythms of Naturalistic Reading Revealed by Combined Eye-Tracking and Electroencephalography.

Neural oscillations are thought to support speech and language processing. They may not only inherit acoustic rhythms, but might also impose endogenous rhythms onto processing. In support of this, we here report that human (both male and female) eye movements during naturalistic reading exhibit rhythmic patterns that show frequency-selective coherence with the EEG, in the absence of any stimulation rhythm. Periodicity was observed in two distinct frequency bands: First, word-locked saccades at 4-5 Hz display coherence with whole-head theta-band activity. Second, fixation durations fluctuate rhythmically at ∼1 Hz, in coherence with occipital delta-band activity. This latter effect was additionally phase-locked to sentence endings, suggesting a relationship with the formation of multi-word chunks. Together, eye movements during reading contain rhythmic patterns that occur in synchrony with oscillatory brain activity. This suggests that linguistic processing imposes preferred processing time scales onto reading, largely independent of actual physical rhythms in the stimulus.SIGNIFICANCE STATEMENT The sampling, grouping, and transmission of information are supported by rhythmic brain activity, so-called neural oscillations. In addition to sampling external stimuli, such rhythms may also be endogenous, affecting processing from the inside out. In particular, endogenous rhythms may impose their pace onto language processing. Studying this is challenging because speech contains physical rhythms that mask endogenous activity. To overcome this challenge, we turned to naturalistic reading, where text does not require the reader to sample in a specific rhythm. We observed rhythmic patterns of eye movements that are synchronized to brain activity as recorded with EEG. This rhythmicity is not imposed by the external stimulus, which indicates that rhythmic brain activity may serve as a pacemaker for language processing.

Musical Training Facilitates Exogenous Temporal Attention via Delta Phase Entrainment within a Sensorimotor Network.

Temporal orienting of attention plays an important role in our day-to-day lives and can use timing information from exogenous or endogenous sources. Yet, it is unclear what neural mechanisms give rise to temporal attention, and it is debated whether both exogenous and endogenous forms of temporal attention share a common neural source. Here, older adult nonmusicians (N = 47, 24 female) were randomized to undergo 8 weeks of either rhythm training, which places demands on exogenous temporal attention, or word search training as a control. The goal was to assess (1) the neural basis of exogenous temporal attention and (2) whether training-induced improvements in exogenous temporal attention can transfer to enhanced endogenous temporal attention abilities, thereby providing support for a common neural mechanism of temporal attention. Before and after training, exogenous temporal attention was assessed using a rhythmic synchronization paradigm, whereas endogenous temporal attention was evaluated via a temporally cued visual discrimination task. Results showed that rhythm training improved performance on the exogenous temporal attention task, which was associated with increased intertrial coherence within the δ (1-4 Hz) band as assessed by EEG recordings. Source localization revealed increased δ-band intertrial coherence arose from a sensorimotor network, including premotor cortex, anterior cingulate cortex, postcentral gyrus, and the inferior parietal lobule. Despite these improvements in exogenous temporal attention, such benefits were not transferred to endogenous attentional ability. These results support the notion that exogenous and endogenous temporal attention uses independent neural sources, with exogenous temporal attention relying on the precise timing of δ band oscillations within a sensorimotor network.SIGNIFICANCE STATEMENT Allocating attention to specific points in time is known as temporal attention, and may arise from external (exogenous) or internal (endogenous) sources. Despite its importance to our daily lives, it is unclear how the brain gives rise to temporal attention and whether exogenous- or endogenous-based sources for temporal attention rely on shared brain regions. Here, we demonstrate that musical rhythm training improves exogenous temporal attention, which was associated with more consistent timing of neural activity in sensory and motor processing brain regions. However, these benefits did not extend to endogenous temporal attention, indicating that temporal attention relies on different brain regions depending on the source of timing information.

Intonation Units in Spontaneous Speech Evoke a Neural Response.

Spontaneous speech is produced in chunks called intonation units (IUs). IUs are defined by a set of prosodic cues and presumably occur in all human languages. Recent work has shown that across different grammatical and sociocultural conditions IUs form rhythms of ∼1 unit per second. Linguistic theory suggests that IUs pace the flow of information in the discourse. As a result, IUs provide a promising and hitherto unexplored theoretical framework for studying the neural mechanisms of communication. In this article, we identify a neural response unique to the boundary defined by the IU. We measured the EEG of human participants (of either sex), who listened to different speakers recounting an emotional life event. We analyzed the speech stimuli linguistically and modeled the EEG response at word offset using a GLM approach. We find that the EEG response to IU-final words differs from the response to IU-nonfinal words even when equating acoustic boundary strength. Finally, we relate our findings to the body of research on rhythmic brain mechanisms in speech processing. We study the unique contribution of IUs and acoustic boundary strength in predicting delta-band EEG. This analysis suggests that IU-related neural activity, which is tightly linked to the classic Closure Positive Shift (CPS), could be a time-locked component that captures the previously characterized delta-band neural speech tracking.SIGNIFICANCE STATEMENT Linguistic communication is central to human experience, and its neural underpinnings are a topic of much research in recent years. Neuroscientific research has benefited from studying human behavior in naturalistic settings, an endeavor that requires explicit models of complex behavior. Usage-based linguistic theory suggests that spoken language is prosodically structured in intonation units. We reveal that the neural system is attuned to intonation units by explicitly modeling their impact on the EEG response beyond mere acoustics. To our understanding, this is the first time this is demonstrated in spontaneous speech under naturalistic conditions and under a theoretical framework that connects the prosodic chunking of speech, on the one hand, with the flow of information during communication, on the other.

The neural oscillations in delta- and theta-bands contribute to divided attention in audiovisual integration.

One of key mechanisms implicated in multisensory processing is neural oscillations in distinct frequency band. Many studies explored the modulation of attention by recording the electroencephalography signals when subjects attended one modality, and ignored the other modality input. However, when attention is directed toward one modality, it may be not always possible to shut out completely inputs from a different modality. Since many situations require division of attention between audition and vision, it is imperative to investigate the neural mechanisms underlying processing of concurrent auditory and visual sensory streams. In the present study, we designed a task of audiovisual semantic discrimination, in which the subjects were asked to share attention to both auditory and visual stimuli. We explored the contribution of neural oscillations in lower-frequency to the modulation of divided attention on audiovisual integration. Our results implied that theta-band activity contributes to the early modulation of divided attention, and delta-band activity contributes to the late modulation of divided attention to audiovisual integration. Moreover, the fronto-central delta- and theta-bands activity is likely a marker of divided attention in audiovisual integration, and the neural oscillation on delta- and theta-bands is conducive to allocating attention resources to dual-tasking involving task-coordinating abilities.

Exploring neurophysiological correlates of visually induced motion sickness using electroencephalography (EEG).

Visually induced motion sickness (VIMS) is a common phenomenon when using visual devices such as smartphones and virtual reality applications, with symptoms including nausea, fatigue, and headache. To date, the neuro-cognitive processes underlying VIMS are not fully understood. Previous studies using electroencephalography (EEG) delivered mixed findings, with some reporting an increase in delta and theta power, and others reporting increases in alpha and beta frequencies. The goal of the study was to gain further insight into EEG correlates for VIMS. Participants viewed a VIMS-inducing visual stimulus, composed of moving black-and-white vertical bars presented on an array of three adjacent monitors. The EEG was recorded during visual stimulation and VIMS ratings were recorded after each trial using the Fast Motion Sickness Scale. Time-frequency analyses were conducted comparing neural activity of participants reporting minimal VIMS (n = 21) and mild-moderate VIMS (n = 12). Results suggested a potential increase in delta power in the centro-parietal regions (CP2) and a decrease in alpha power in the central regions (Cz) for participants experiencing mild-moderate VIMS compared to those with minimal VIMS. Event-related spectral perturbations (ERSPs) suggested that group differences in EEG activity developed with increasing duration of a trial. These results support the hypothesis that the EEG might be sensitive to differences in information processing in VIMS and minimal VIMS contexts, and indicate that it may be possible to identify neurophysiological correlate of VIMS. Differences in EEG activity related to VIMS may reflect differential processing of conflicting visual and vestibular sensory information.

Anxiolytic-like Effects and Quantitative EEG Profile of Palmitone Induces Responses Like Buspirone Rather Than Diazepam as Clinical Drugs.

Anxiety is a mental disorder with a growing worldwide incidence due to the SARS-CoV-2 virus pandemic. Pharmacological therapy includes drugs such as benzodiazepines (BDZs) or azapirones like buspirone (BUSP) or analogs, which unfortunately produce severe adverse effects or no immediate response, respectively. Medicinal plants or their bioactive metabolites are a shared global alternative to treat anxiety. Palmitone is one active compound isolated from Annona species due to its tranquilizing activity. However, its influence on neural activity and possible mechanism of action are unknown. In this study, an electroencephalographic (EEG) spectral power analysis was used to corroborate its depressant activity in comparison with the anxiolytic-like effects of reference drugs such as diazepam (DZP, 1 mg/kg) and BUSP (4 mg/kg) or 8-OH-DPAT (1 mg/kg), alone or in the presence of the GABAA (picrotoxin, PTX, 1 mg/kg) or serotonin 5-HT1A receptor antagonists (WAY100634, WAY, 1 mg/kg). The anxiolytic-like activity was assayed using the behavioral response of mice employing open-field, hole-board, and plus-maze tests. EEG activity was registered in both the frontal and parietal cortex, performing a 10 min baseline and 30 min recording after the treatments. As a result, anxiety-like behavior was significantly decreased in mice administered with palmitone, DZP, BUSP, or 8-OH-DPAT. The effect of palmitone was equivalent to that produced by 5-HT1A receptor agonists but 50% less effective than DZP. The presence of PTX and WAY prevented the anxiolytic-like response of DZP and 8-OH-DPAT, respectively. Whereas only the antagonist of the 5-HT1A receptor (WAY) inhibited the palmitone effects. Palmitone and BUSP exhibited similar changes in the relative power bands after the spectral power analysis. This response was different to the changes induced by DZP. In conclusion, brain electrical activity was associated with the anxiolytic-like effects of palmitone implying a serotoninergic rather than a GABAergic mechanism of action.

Event-related delta and theta responses may reflect the valence discrimination in the emotional oddball task.

How emotion and cognition interact is still a matter of debate. Investigation of this interaction in terms of the brain oscillatory dynamics appears to be an essential approach. To investigate this topic, we designed two separate three-stimulus oddball tasks, including emotional stimuli with different valences. Twenty healthy young subjects were included in the study. They completed two tasks, namely: the positive emotional oddball task and the negative emotional oddball task. Each task included the target, non-target, and distractor stimuli. Positive and negative pictures were the target stimuli in the positive and negative emotional oddball task. We asked participants to determine the number of target stimuli in each task. During sessions, EEGs were recorded with 32 electrodes. We found that (negative) target stimuli elicit higher delta (1-3.5 Hz) and theta (4-7 Hz) power responses but not the phase-locking responses compared to (positive) distractor stimuli during the negative oddball task. On the other hand, the same effect was not seen during the positive emotional oddball task. Here, we showed that the valence dimension interacted with the target status. Finally, we summarized our results that the presence of negative distractors attenuated the target effect of the positive stimuli due to the negative bias.

Endogenous Oscillations Time-Constrain Linguistic Segmentation: Cycling the Garden Path.

Speech is transient. To comprehend entire sentences, segments consisting of multiple words need to be memorized for at least a while. However, it has been noted previously that we struggle to memorize segments longer than approximately 2.7 s. We hypothesized that electrophysiological processing cycles within the delta band (<4 Hz) underlie this time constraint. Participants' EEG was recorded while they listened to temporarily ambiguous sentences. By manipulating the speech rate, we aimed at biasing participants' interpretation: At a slow rate, segmentation after 2.7 s would trigger a correct interpretation. In contrast, at a fast rate, segmentation after 2.7 s would trigger a wrong interpretation and thus an error later in the sentence. In line with the suggested time constraint, the phase of the delta-band oscillation at the critical point in the sentence mirrored segmentation on the level of single trials, as indicated by the amplitude of the P600 event-related brain potential (ERP) later in the sentence. The correlation between upstream delta-band phase and downstream P600 amplitude implies that segmentation took place when an underlying neural oscillator had reached a specific angle within its cycle, determining comprehension. We conclude that delta-band oscillations set an endogenous time constraint on segmentation.

Efficient Low-Frequency SSVEP Detection with Wearable EEG Using Normalized Canonical Correlation Analysis.

Recent studies show that the integrity of core perceptual and cognitive functions may be tested in a short time with Steady-State Visual Evoked Potentials (SSVEP) with low stimulation frequencies, between 1 and 10 Hz. Wearable EEG systems provide unique opportunities to test these brain functions on diverse populations in out-of-the-lab conditions. However, they also pose significant challenges as the number of EEG channels is typically limited, and the recording conditions might induce high noise levels, particularly for low frequencies. Here we tested the performance of Normalized Canonical Correlation Analysis (NCCA), a frequency-normalized version of CCA, to quantify SSVEP from wearable EEG data with stimulation frequencies ranging from 1 to 10 Hz. We validated NCCA on data collected with an 8-channel wearable wireless EEG system based on BioWolf, a compact, ultra-light, ultra-low-power recording platform. The results show that NCCA correctly and rapidly detects SSVEP at the stimulation frequency within a few cycles of stimulation, even at the lowest frequency (4 s recordings are sufficient for a stimulation frequency of 1 Hz), outperforming a state-of-the-art normalized power spectral measure. Importantly, no preliminary artifact correction or channel selection was required. Potential applications of these results to research and clinical studies are discussed.

Non-rhythmic temporal prediction involves phase resets of low-frequency delta oscillations.

The phase of neural oscillatory signals aligns to the predicted onset of upcoming stimulation. Whether such phase alignments represent phase resets of underlying neural oscillations or just rhythmically evoked activity, and whether they can be observed in a rhythm-free visual context, however, remains unclear. Here, we recorded the magnetoencephalogram while participants were engaged in a temporal prediction task, judging the visual or tactile reappearance of a uniformly moving stimulus. The prediction conditions were contrasted with a control condition to dissociate phase adjustments of neural oscillations from stimulus-driven activity. We observed stronger delta band inter-trial phase consistency (ITPC) in a network of sensory, parietal and frontal brain areas, but no power increase reflecting stimulus-driven or prediction-related evoked activity. Delta ITPC further correlated with prediction performance in the cerebellum and visual cortex. Our results provide evidence that phase alignments of low-frequency neural oscillations underlie temporal predictions in a non-rhythmic visual and crossmodal context.