Random Tactile Noise Stimulation Reveals Beta-Rhythmic Impulse Response Function of the Somatosensory System.

Both passive tactile stimulation and motor actions result in dynamic changes in beta band (15-30 Hz Hz) oscillations over somatosensory cortex. Similar to alpha band (8-12 Hz) power decrease in the visual system, beta band power also decreases following stimulation of the somatosensory system. This relative suppression of α and ß oscillations is generally interpreted as an increase in cortical excitability. Here, next to traditional single-pulse stimuli, we used a random intensity continuous right index finger tactile stimulation (white noise), which enabled us to uncover an impulse response function of the somatosensory system. Contrary to previous findings, we demonstrate a burst-like initial increase rather than decrease of beta activity following white noise stimulation (human participants, N = 18, 8 female). These ß bursts, on average, lasted for 3 cycles, and their frequency was correlated with resonant frequency of somatosensory cortex, as measured by a multifrequency steady-state somatosensory evoked potential paradigm. Furthermore, beta band bursts shared spectro-temporal characteristics with evoked and resting-state ß oscillations. Together, our findings not only reveal a novel oscillatory signature of somatosensory processing that mimics the previously reported visual impulse response functions, but also point to a common oscillatory generator underlying spontaneous ß bursts in the absence of tactile stimulation and phase-locked ß bursts following stimulation, the frequency of which is determined by the resonance properties of the somatosensory system.SIGNIFICANCE STATEMENT The investigation of the transient nature of oscillations has gained great popularity in recent years. The findings of bursting activity, rather than sustained oscillations in the beta band, have provided important insights into its role in movement planning, working memory, inhibition, and reactivation of neural ensembles. In this study, we show that also in response to tactile stimulation the somatosensory system responds with ∼3 cycle oscillatory beta band bursts, whose spectro-temporal characteristics are shared with evoked and resting-state beta band oscillatory signatures of the somatosensory system. As similar bursts have been observed in the visual domain, these oscillatory signatures might reflect an important supramodal mechanism in sensory processing.

A multidimensional evaluation of the benefits of an ecologically realistic training based on pretend play for preschoolers' cognitive control and self-regulation: From behavior to the underlying theta neuro-oscillatory activity.

To what extent can cognitive control, self-regulation, and the underlying midfrontal theta oscillatory activity of preschool children be modified by an ecologically realistic training based on pretend play? To answer this question, 70 children aged 4-6 years (37 boys) were assigned to a training group or a control group using a pairing randomization procedure. Children were administered 20 play sessions over 10 weeks. Benefits were evaluated with a pre-post design. The intervention helped children to engage more in self-regulation within the training activities. However, the intervention did not promote self-regulation outside of the training context, nor did it influence cognitive control and theta activity. These results provide a better understanding of the limitations of an ecologically realistic approach to cognitive control training.

The role of midfrontal theta oscillations across the development of cognitive control in preschoolers and school-age children.

The development of cognitive control enables children to better resist acting based on distracting information that interferes with the current action. Cognitive control improvement serves different functions that differ in part by the type of interference to resolve. Indeed, resisting to interference at the task-set level or at the response-preparation level is, respectively, associated with cognitive flexibility and inhibition. It is, however, unknown whether the same neural mechanism underlies these two functions across development. Studies in adults have revealed the contribution of midfrontal theta (MFT) oscillations in interference resolution. This study investigated whether MFT is involved in the resolution of different types of interference in two age groups identified as corresponding to different latent structures of executive functions. Preschool (4-6 years) and school children (6-8 years) were tested with a task involving interference at the response level and/or the task-set level while (electroencephalogram) EEG was recorded. Behaviorally, response time and accuracy were affected by task-set. Both age groups were less accurate when the interference occurred at the task-set level and only the younger group showed decreased accuracy when interference was presented at the response-preparation level. Furthermore, MFT power was increased, relative to the baseline, during the resolution of both types of interference and in both age groups. These findings suggest that MFT is involved in immature cognitive control (i.e., preschool and school-ages), by orchestrating its different cognitive processes, irrespective of the interference to resolve and of the level of cognitive control development (i.e., the degree of differentiation of executive functions).

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.

Attention differentially modulates the amplitude of resonance frequencies in the visual cortex.

Rhythmic visual stimuli (flicker) elicit rhythmic brain responses at the frequency of the stimulus, and attention generally enhances these oscillatory brain responses (steady state visual evoked potentials, SSVEPs). Although SSVEP responses have been tested for flicker frequencies up to 100 Hz [Herrmann, 2001], effects of attention on SSVEP amplitude have only been reported for lower frequencies (up to ~30 Hz), with no systematic comparison across a wide, finely sampled frequency range. Does attention modulate SSVEP amplitude at higher flicker frequencies (gamma band, 30-80 Hz), and is attentional modulation constant across frequencies? By isolating SSVEP responses from the broadband EEG signal using a multivariate spatiotemporal source separation method, we demonstrate that flicker in the alpha and gamma bands elicit strongest and maximally phase stable brain responses (resonance), on which the effect of attention is opposite: positive for gamma and negative for alpha. Finding subject-specific gamma resonance frequency and a positive attentional modulation of gamma-band SSVEPs points to the untapped potential of flicker as a non-invasive tool for studying the causal effects of interactions between visual gamma-band rhythmic stimuli and endogenous gamma oscillations on perception and attention.

Individual Alpha Peak Frequency Predicts 10 Hz Flicker Effects on Selective Attention.

Rhythmic visual stimulation ("flicker") is primarily used to "tag" processing of low-level visual and high-level cognitive phenomena. However, preliminary evidence suggests that flicker may also entrain endogenous brain oscillations, thereby modulating cognitive processes supported by those brain rhythms. Here we tested the interaction between 10 Hz flicker and endogenous alpha-band (∼10 Hz) oscillations during a selective visuospatial attention task. We recorded EEG from human participants (both genders) while they performed a modified Eriksen flanker task in which distractors and targets flickered within (10 Hz) or outside (7.5 or 15 Hz) the alpha band. By using a combination of EEG source separation, time-frequency, and single-trial linear mixed-effects modeling, we demonstrate that 10 Hz flicker interfered with stimulus processing more on incongruent than congruent trials (high vs low selective attention demands). Crucially, the effect of 10 Hz flicker on task performance was predicted by the distance between 10 Hz and individual alpha peak frequency (estimated during the task). Finally, the flicker effect on task performance was more strongly predicted by EEG flicker responses during stimulus processing than during preparation for the upcoming stimulus, suggesting that 10 Hz flicker interfered more with reactive than proactive selective attention. These findings are consistent with our hypothesis that visual flicker entrained endogenous alpha-band networks, which in turn impaired task performance. Our findings also provide novel evidence for frequency-dependent exogenous modulation of cognition that is determined by the correspondence between the exogenous flicker frequency and the endogenous brain rhythms.SIGNIFICANCE STATEMENT Here we provide novel evidence that the interaction between exogenous rhythmic visual stimulation and endogenous brain rhythms can have frequency-specific behavioral effects. We show that alpha-band (10 Hz) flicker impairs stimulus processing in a selective attention task when the stimulus flicker rate matches individual alpha peak frequency. The effect of sensory flicker on task performance was stronger when selective attention demands were high, and was stronger during stimulus processing and response selection compared with the prestimulus anticipatory period. These findings provide novel evidence that frequency-specific sensory flicker affects online attentional processing, and also demonstrate that the correspondence between exogenous and endogenous rhythms is an overlooked prerequisite when testing for frequency-specific cognitive effects of flicker.

The Triple-Flash Illusion Reveals a Driving Role of Alpha-Band Reverberations in Visual Perception.

The modulatory role of spontaneous brain oscillations on perception of threshold-level stimuli is well established. Here, we provide evidence that alpha-band (∼10 Hz) oscillations not only modulate perception of threshold-level sensory inputs but also can drive perception and generate percepts without a physical stimulus being present. We used the "triple-flash" illusion: Occasional perception of three flashes when only two spatially coincident veridical ones, separated by ∼100 ms, are presented. The illusion was proposed to result from superposition of two hypothetical oscillatory impulse response functions generated in response to each flash: When the delay between flashes matches the period of the oscillation, the superposition enhances a later part of the oscillation that is normally damped; when this enhancement crosses perceptual threshold, a third flash is erroneously perceived (Bowen, 1989). In Experiment 1, we varied stimulus onset asynchrony and validated Bowen's theory: The optimal stimulus onset asynchrony for illusion to occur was correlated, across human subjects (both genders), with the subject-specific impulse response function period determined from a separate EEG experiment. Experiment 2 revealed that prestimulus parietal, but no occipital, alpha EEG phase and power, as well as poststimulus alpha phase-locking, together determine the occurrence of the illusion on a trial-by-trial basis. Thus, oscillatory reverberations create something out of nothing: A third flash where there are only two.SIGNIFICANCE STATEMENT We highlight a novel property of alpha-band (∼10 Hz) oscillations based on three experiments (two EEG and one psychophysics) by demonstrating that alpha-band oscillations do not merely modulate perception, but can also drive perception. We show that human participants report seeing a third flash when only two are presented (the "triple-flash" illusion) most often when the interflash delay matches the period of participant's oscillatory impulse response function reverberating in alpha. Within-subject, the phase and power of ongoing parietal, but not occipital, alpha-band oscillations at the time of the first flash determine illusory percept on a trial-by-trial basis. We revealed a physiologically plausible mechanism that validates and extends the original theoretical account of the triple-flash illusion proposed by Bowen in 1989.

Protecting visual short-term memory during maintenance: Attentional modulation of target and distractor representations.

In the presence of distraction, attentional filtering is a key predictor of efficient information storage in visual short-term memory (VSTM). Yet, the role of attention in distractor filtering, and the extent to which attentional filtering continues to protect information during post-perceptual stages of VSTM, remains largely unknown. In the current study, we investigated the role of spatial attention in distractor filtering during VSTM encoding and maintenance. Participants performed a change detection task with varying distractor load. Attentional deployment to target and distractor locations was tracked continuously by means of Steady-State Visual Evoked Potentials (SSVEPs). Analyses revealed that attention strongly modulated the amplitude of the second harmonic SSVEP response, with larger amplitudes at target compared to distractor locations. These attentional modulations commenced during encoding, and remained present during maintenance. Furthermore, the amount of attention paid to distractor locations was directly related to behavioral distractor costs: Individuals who paid more attention to target compared to distractor locations during VSTM maintenance generally suffered less from the presence of distractors. Together, these findings support an important role of spatial attention in distractor filtering at multiple stages of VSTM, and highlight the usefulness of SSVEPs in continuously tracking attention to multiple locations during VSTM.

Rhythmic entrainment source separation: Optimizing analyses of neural responses to rhythmic sensory stimulation.

Steady-state evoked potentials (SSEPs) are rhythmic brain responses to rhythmic sensory stimulation, and are often used to study perceptual and attentional processes. We present a data analysis method for maximizing the signal-to-noise ratio of the narrow-band steady-state response in the frequency and time-frequency domains. The method, termed rhythmic entrainment source separation (RESS), is based on denoising source separation approaches that take advantage of the simultaneous but differential projection of neural activity to multiple electrodes or sensors. Our approach is a combination and extension of existing multivariate source separation methods. We demonstrate that RESS performs well on both simulated and empirical data, and outperforms conventional SSEP analysis methods based on selecting electrodes with the strongest SSEP response, as well as several other linear spatial filters. We also discuss the potential confound of overfitting, whereby the filter captures noise in absence of a signal. Matlab scripts are available to replicate and extend our simulations and methods. We conclude with some practical advice for optimizing SSEP data analyses and interpreting the results.

Fronto-parietal network oscillations reveal relationship between working memory capacity and cognitive control.

Executive-attention theory proposes a close relationship between working memory capacity (WMC) and cognitive control abilities. However, conflicting results are documented in the literature, with some studies reporting that individual variations in WMC predict differences in cognitive control and trial-to-trial control adjustments (operationalized as the size of the congruency effect and congruency sequence effects, respectively), while others report no WMC-related differences. We hypothesized that brain network dynamics might be a more sensitive measure of WMC-related differences in cognitive control abilities. Thus, in the present study, we measured human EEG during the Simon task to characterize WMC-related differences in the neural dynamics of conflict processing and adaptation to conflict. Although high- and low-WMC individuals did not differ behaviorally, there were substantial WMC-related differences in theta (4-8 Hz) and delta (1-3 Hz) connectivity in fronto-parietal networks. Group differences in local theta and delta power were relatively less pronounced. These results suggest that the relationship between WMC and cognitive control abilities is more strongly reflected in large-scale oscillatory network dynamics than in spatially localized activity or in behavioral task performance.

Dissociable mechanisms underlying individual differences in visual working memory capacity.

Individuals scoring relatively high on measures of working memory tend to be more proficient at controlling attention to minimize the effect of distracting information. It is currently unknown whether such superior attention control abilities are mediated by stronger suppression of irrelevant information, enhancement of relevant information, or both. Here we used steady-state visual evoked potentials (SSVEPs) with the Eriksen flanker task to track simultaneously the attention to relevant and irrelevant information by tagging target and distractors with different frequencies. This design allowed us to dissociate attentional biasing of perceptual processing (via SSVEPs) and stimulus processing in the frontal cognitive control network (via time-frequency analyses of EEG data). We show that while preparing for the upcoming stimulus, high- and low-WMC individuals use different strategies: High-WMC individuals show attentional suppression of the irrelevant stimuli, whereas low-WMC individuals demonstrate attentional enhancement of the relevant stimuli. Moreover, behavioral performance was predicted by trial-to-trial fluctuations in strength of distractor-suppression for high-WMC participants. We found no evidence for WMC-related differences in cognitive control network functioning, as measured by midfrontal theta-band power. Taken together, these findings suggest that early suppression of irrelevant information is a key underlying neural mechanism by which superior attention control abilities are implemented.

Five methodological challenges in cognitive electrophysiology.

Here we discuss five methodological challenges facing the current cognitive electrophysiology literature that address the roles of brain oscillations in cognition. The challenges focus on (1) unambiguous and consistent terminology, (2) neurophysiologically meaningful interpretations of results, (3) evaluation and comparison of different spatial filters often used in M/EEG research, (4) the role of multiscale interactions in brain and cognitive function, and (5) development of biophysically plausible cognitive models. We also suggest research directions that will help address these challenges. We hope that this paper will help foster discussions and debates about important themes in the study of how the brain's rhythmic patterns of spatiotemporal electrophysiological activity support cognition.

Working memory capacity predicts conflict-task performance.

The relationship between the ability to maintain task goals and working memory capacity (WMC) is firmly established, but evidence for WMC-related differences in conflict processing is mixed. We investigated whether WMC (measured using two complex-span tasks) mediates differences in adjustments of cognitive control in response to conflict. Participants performed a Simon task in which congruent and incongruent trials were equiprobable, but in which the proportion of congruency repetitions (congruent trials followed by congruent trials or incongruent trials followed by incongruent trials) and thus the need for trial-by-trial adjustments in cognitive control varied by block. The overall Simon effect did not depend on WMC capacity. However, for the low-WMC participants the Simon effect decreased as the proportion of congruency repetitions decreased, whereas for the high- and average-WMC participants it was relatively constant across conditions. Distribution analysis of the Simon effect showed more evidence for the inhibition of stimulus location in the low- than in the high-WMC participants, especially when the proportion of congruency repetitions was low. We hypothesize that low-WMC individuals exhibit more interference from task-irrelevant information due to weaker preparatory control prior to stimulus presentation and, thus, stronger reliance on reactive recruitment of cognitive control.