Common neural mechanisms supporting time judgements in humans and monkeys.

There has been an increasing interest in identifying the biological underpinnings of human time perception, for which purpose research in non-human primates (NHP) is common. Although previous work, based on behaviour, suggests that similar mechanisms support time perception across species, the neural correlates of time estimation in humans and NHP have not been directly compared. In this study, we assess whether brain evoked responses during a time categorization task are similar across species. Specifically, we assess putative differences in post-interval evoked potentials as a function of perceived duration in human EEG (N = 24) and local field potential (LFP) and spike recordings in pre-supplementary motor area (pre-SMA) of one monkey. Event-related potentials (ERPs) differed significantly after the presentation of the temporal interval between "short" and "long" perceived durations in both species, even when the objective duration of the stimuli was the same. Interestingly, the polarity of the reported ERPs was reversed for incorrect trials (i.e., the ERP of a "long" stimulus looked like the ERP of a "short" stimulus when a time categorization error was made). Hence, our results show that post-interval potentials reflect the perceived (rather than the objective) duration of the presented time interval in both NHP and humans. In addition, firing rates in monkey's pre-SMA also differed significantly between short and long perceived durations and were reversed in incorrect trials. Together, our results show that common neural mechanisms support time categorization in NHP and humans, thereby suggesting that NHP are a good model for investigating human time perception.

Alpha and Beta Oscillations Differentially Support Word Production in a Rule-Switching Task.

Research into the role of brain oscillations in basic perceptual and cognitive functions has suggested that the alpha rhythm reflects functional inhibition while the beta rhythm reflects neural ensemble (re)activation. However, little is known regarding the generalization of these proposed fundamental operations to linguistic processes, such as speech comprehension and production. Here, we recorded magnetoencephalography in participants performing a novel rule-switching paradigm. Specifically, Dutch native speakers had to produce an alternative exemplar from the same category or a feature of a given target word embedded in spoken sentences (e.g., for the word "tuna", an exemplar from the same category-"seafood"-would be "shrimp", and a feature would be "pink"). A cue indicated the task rule-exemplar or feature-either before (pre-cue) or after (retro-cue) listening to the sentence. Alpha power during the working memory delay was lower for retro-cue compared with that for pre-cue in the left hemispheric language-related regions. Critically, alpha power negatively correlated with reaction times, suggestive of alpha facilitating task performance by regulating inhibition in regions linked to lexical retrieval. Furthermore, we observed a different spatiotemporal pattern of beta activity for exemplars versus features in the right temporoparietal regions, in line with the proposed role of beta in recruiting neural networks for the encoding of distinct categories. Overall, our study provides evidence for the generalizability of the role of alpha and beta oscillations from perceptual to more "complex, linguistic processes" and offers a novel task to investigate links between rule-switching, working memory, and word production.

Cardiac activity impacts cortical motor excitability.

Human cognition and action can be influenced by internal bodily processes such as heartbeats. For instance, somatosensory perception is impaired both during the systolic phase of the cardiac cycle and when heartbeats evoke stronger cortical responses. Here, we test whether these cardiac effects originate from overall changes in cortical excitability. Cortical and corticospinal excitability were assessed using electroencephalographic and electromyographic responses to transcranial magnetic stimulation while concurrently monitoring cardiac activity with electrocardiography. Cortical and corticospinal excitability were found to be highest during systole and following stronger neural responses to heartbeats. Furthermore, in a motor task, hand-muscle activity and the associated desynchronization of sensorimotor oscillations were stronger during systole. These results suggest that systolic cardiac signals have a facilitatory effect on motor excitability-in contrast to sensory attenuation that was previously reported for somatosensory perception. Thus, it is possible that distinct time windows exist across the cardiac cycle, optimizing either perception or action.

Alpha oscillations protect working memory against distracters in a modality-specific way.

Alpha oscillations are thought to be involved in suppressing distracting input in working-memory tasks. Yet, the spatial-temporal dynamics of such suppression remain unclear. Key questions are whether such suppression reflects a domain-general inattentiveness mechanism, or occurs in a stimulus- or modality-specific manner within cortical areas most responsive to the distracters; and whether the suppression is proactive (i.e., preparatory) or reactive. Here, we addressed these questions using a working-memory task where participants had to memorize an array of visually presented digits and reproduce one of them upon being probed. We manipulated the presence of distracters and the sensory modality in which distracters were presented during memory maintenance. Our results show that sensory areas most responsive to visual and auditory distracters exhibited stronger alpha power increase after visual and auditory distracter presentation respectively. These results suggest that alpha oscillations underlie distracter suppression in a reactive, modality-specific manner.

Genuine beta bursts in human working memory: controlling for the influence of lower-frequency rhythms.

Human working memory is associated with significant modulations in oscillatory brain activity. However, the functional role of brain rhythms at different frequencies is still debated. Modulations in the beta frequency range (15-40 Hz) are especially difficult to interpret because they could be artifactually produced by (more prominent) oscillations in lower frequencies that show non-sinusoidal properties. In this study, we investigate beta oscillations during working memory while controlling for the possible influence of lower frequency rhythms. We collected electroencephalography (EEG) data in 31 participants who performed a spatial working-memory task with two levels of cognitive load. In order to rule out the possibility that observed beta activity was affected by non-sinusoidalities of lower frequency rhythms, we developed an algorithm that detects transient beta oscillations that do not coincide with more prominent lower frequency rhythms in time and space. Using this algorithm, we show that the amplitude and duration of beta bursts decrease with memory load and during memory manipulation, while their peak frequency and rate increase. In addition, interindividual differences in performance were significantly associated with beta burst rates. Together, our results show that beta rhythms are functionally modulated during working memory and that these changes cannot be attributed to lower frequency rhythms with non-sinusoidal properties.

ß Band Rhythms Influence Reaction Times.

Despite their involvement in many cognitive functions, ß oscillations are among the least understood brain rhythms. Reports on whether the functional role of ß is primarily inhibitory or excitatory have been contradictory. Our framework attempts to reconcile these findings and proposes that several ß rhythms co-exist at different frequencies. ß Frequency shifts and their potential influence on behavior have thus far received little attention. In this human magnetoencephalography (MEG) experiment, we asked whether changes in ß power or frequency in auditory cortex and motor cortex influence behavior (reaction times) during an auditory sweep discrimination task. We found that in motor cortex, increased ß power slowed down responses, while in auditory cortex, increased ß frequency slowed down responses. We further characterized ß as transient burst events with distinct spectro-temporal profiles influencing reaction times. Finally, we found that increased motor-to-auditory ß connectivity also slowed down responses. In sum, ß power, frequency, bursting properties, cortical focus, and connectivity profile all influenced behavioral outcomes. Our results imply that the study of ß oscillations requires caution as ß dynamics are multifaceted phenomena, and that several dynamics must be taken into account to reconcile mixed findings in the literature.

Distinct beta frequencies reflect categorical decisions.

Based on prior findings of content-specific beta synchronization in working memory and decision making, we hypothesized that beta oscillations support the (re-)activation of cortical representations by mediating neural ensemble formation. We found that beta activity in monkey dorsolateral prefrontal cortex (dlPFC) and pre-supplementary motor area (preSMA) reflects the content of a stimulus in relation to the task context, regardless of its objective properties. In duration- and distance-categorization tasks, we changed the boundary between categories from one block of trials to the next. We found that two distinct beta-band frequencies were consistently associated with the two relative categories, with activity in these bands predicting the animals' responses. We characterized beta at these frequencies as transient bursts, and showed that dlPFC and preSMA are connected via these distinct frequency channels. These results support the role of beta in forming neural ensembles, and further show that such ensembles synchronize at different beta frequencies.

Naturalistic Spoken Language Comprehension Is Supported by Alpha and Beta Oscillations.

Brain oscillations are prevalent in all species and are involved in numerous perceptual operations. α oscillations are thought to facilitate processing through the inhibition of task-irrelevant networks, while ß oscillations are linked to the putative reactivation of content representations. Can the proposed functional role of α and ß oscillations be generalized from low-level operations to higher-level cognitive processes? Here we address this question focusing on naturalistic spoken language comprehension. Twenty-two (18 female) Dutch native speakers listened to stories in Dutch and French while MEG was recorded. We used dependency parsing to identify three dependency states at each word: the number of (1) newly opened dependencies, (2) dependencies that remained open, and (3) resolved dependencies. We then constructed forward models to predict α and ß power from the dependency features. Results showed that dependency features predict α and ß power in language-related regions beyond low-level linguistic features. Left temporal, fundamental language regions are involved in language comprehension in α, while frontal and parietal, higher-order language regions, and motor regions are involved in ß. Critically, α- and ß-band dynamics seem to subserve language comprehension tapping into syntactic structure building and semantic composition by providing low-level mechanistic operations for inhibition and reactivation processes. Because of the temporal similarity of the α-ß responses, their potential functional dissociation remains to be elucidated. Overall, this study sheds light on the role of α and ß oscillations during naturalistic spoken language comprehension, providing evidence for the generalizability of these dynamics from perceptual to complex linguistic processes.SIGNIFICANCE STATEMENT It remains unclear whether the proposed functional role of α and ß oscillations in perceptual and motor function is generalizable to higher-level cognitive processes, such as spoken language comprehension. We found that syntactic features predict α and ß power in language-related regions beyond low-level linguistic features when listening to naturalistic speech in a known language. We offer experimental findings that integrate a neuroscientific framework on the role of brain oscillations as "building blocks" with spoken language comprehension. This supports the view of a domain-general role of oscillations across the hierarchy of cognitive functions, from low-level sensory operations to abstract linguistic processes.

Visual working memory recruits two functionally distinct alpha rhythms in posterior cortex.

Oscillatory activity in the human brain is dominated by posterior alpha oscillations (8-14 Hz), which have been shown to be functionally relevant in a wide variety of cognitive tasks. Although posterior alpha oscillations are commonly considered a single oscillator anchored at an individual alpha frequency (IAF; ∼10 Hz), previous work suggests that IAF reflects a spatial mixture of different brain rhythms. In this study, we assess whether Independent Component Analysis (ICA) can disentangle functionally distinct posterior alpha rhythms in the context of visual short-term memory retention. Magnetoencephalography (MEG) was recorded in 33 subjects while performing a visual working memory task. Group analysis at sensor level suggested the existence of a single posterior alpha oscillator that increases in power and decreases in frequency during memory retention. Conversely, single-subject analysis of independent components revealed the existence of two dissociable alpha rhythms: one that increases in power during memory retention (Alpha1) and another one that decreases in power (Alpha2). Alpha1 and Alpha2 rhythms were differentially modulated by the presence of visual distractors (Alpha1 increased in power while Alpha2 decreased) and had an opposite relationship with accuracy (positive for Alpha1 and negative for Alpha2). In addition, Alpha1 rhythms showed a lower peak frequency, a narrower peak width, a greater relative peak amplitude and a more central source than Alpha2 rhythms. Together, our results demonstrate that modulations in posterior alpha oscillations during short-term memory retention reflect the dynamics of at least two distinct brain rhythms with different functions and spatiospectral characteristics.Significance statementAlpha oscillations are the most prominent feature of the human brain's electrical activity, and consist of rhythmic neuronal activity in posterior parts of the cortex. Alpha is usually considered a single brain rhythm that changes in power and frequency to support cognitive operations. We here show that posterior alpha entails at least two dissociable rhythms with distinct functions and characteristics. These findings could solve previous inconsistencies in the literature regarding the direction of task-related alpha power/frequency modulations and their relation to cognitive performance. In addition, the existence of two distinct posterior alpha rhythms could have important consequences for the design of neurostimulation protocols aimed at modulating alpha oscillations and subsequently cognition.

Shaping Information Processing: The Role of Oscillatory Dynamics in a Working Memory Task.

Neural oscillations are thought to reflect low-level operations that can be used for higher-level cognitive functions. Here, we investigated the role of brain rhythms in the 1-30 Hz range by recording MEG in human participants performing a visual delayed match-to-sample paradigm in which orientation or spatial frequency of sample and probe gratings had to be matched. A cue occurring before or after sample presentation indicated the to-be-matched feature. We demonstrate that alpha/beta power decrease tracks the presentation of the informative cue and indexes faster responses. Moreover, these faster responses coincided with an augmented phase alignment of slow oscillations, as well as phase-amplitude coupling between slow and fast oscillations. Importantly, stimulus decodability was boosted by both low alpha power and high beta power. In summary, we provide support for a comprehensive framework in which different rhythms play specific roles: slow rhythms control input sampling, while alpha (and beta) gates the information flow, beta recruits task-relevant circuits, and the timing of faster oscillations is controlled by slower ones.

Breaking Down a Rhythm: Dissecting the Mechanisms Underlying Task-Related Neural Oscillations.

A century worth of research has linked multiple cognitive, perceptual and behavioral states to various brain oscillations. However, the mechanistic roles and circuit underpinnings of these oscillations remain an area of active study. In this review, we argue that the advent of optogenetic and related systems neuroscience techniques has shifted the field from correlational to causal observations regarding the role of oscillations in brain function. As a result, studying brain rhythms associated with behavior can provide insight at different levels, such as decoding task-relevant information, mapping relevant circuits or determining key proteins involved in rhythmicity. We summarize recent advances in this field, highlighting the methods that are being used for this purpose, and discussing their relative strengths and limitations. We conclude with promising future approaches that will help unravel the functional role of brain rhythms in orchestrating the repertoire of complex behavior.

No behavioural evidence for rhythmic facilitation of perceptual discrimination.

It has been hypothesized that internal oscillations can synchronize (i.e., entrain) to external environmental rhythms, thereby facilitating perception and behaviour. To date, evidence for the link between the phase of neural oscillations and behaviour has been scarce and contradictory; moreover, it remains an open question whether the brain can use this tentative mechanism for active temporal prediction. In our present study, we conducted a series of auditory pitch discrimination tasks with 181 healthy participants in an effort to shed light on the proposed behavioural benefits of rhythmic cueing and entrainment. In the three versions of our task, we observed no perceptual benefit of purported entrainment: targets occurring in-phase with a rhythmic cue provided no perceptual benefits in terms of discrimination accuracy or reaction time when compared with targets occurring out-of-phase or targets occurring randomly, nor did we find performance differences for targets preceded by rhythmic versus random cues. However, we found a surprising effect of cueing frequency on reaction time, in which participants showed faster responses to cue rhythms presented at higher frequencies. We therefore provide no evidence of entrainment, but instead a tentative effect of covert active sensing in which a faster external rhythm leads to a faster communication rate between motor and sensory cortices, allowing for sensory inputs to be sampled earlier in time.

Alpha and broadband high-frequency activity track task dynamics and predict performance in controlled decision-making.

Intracranial recordings in human subjects provide a unique, fine-grained temporal and spatial resolution inaccessible to conventional non-invasive methods. A prominent signal in these recordings is broadband high-frequency activity (approx. 70-150 Hz), generally considered to reflect neuronal excitation. Here we explored the use of this broadband signal to track, on a single-trial basis, the temporal and spatial distribution of task-engaged areas involved in decision-making. We additionally focused on the alpha rhythm (8-14 Hz), thought to regulate the (dis)engagement of neuronal populations based on task demands. Using these signals, we characterized activity across cortex using intracranial recordings in patients with intractable epilepsy performing the Multi-Source Interference Task, a Stroop-like decision-making paradigm. We analyzed recordings both from grid electrodes placed over cortical areas including frontotemporal and parietal cortex, and depth electrodes in prefrontal regions, including cingulate cortex. We found a widespread negative relationship between alpha power and broadband activity, substantiating the gating role of alpha in regions beyond sensory/motor cortex. Combined, these signals reflect the spatio-temporal pattern of task-engagement, with alpha decrease signifying task-involved regions and broadband increase temporally locking to specific task aspects, distributed over cortical sites. We report sites that only respond to stimulus presentation or to the decision report and, interestingly, sites that reflect the time-on-task. The latter predict the subject's reaction times on a trial-by-trial basis. A smaller subset of sites showed modulation with task condition. Taken together, alpha and broadband signals allow tracking of neuronal population dynamics across cortex on a fine temporal and spatial scale.

Ongoing neural oscillations influence behavior and sensory representations by suppressing neuronal excitability.

The ability to process and respond to external input is critical for adaptive behavior. Why, then, do neural and behavioral responses vary across repeated presentations of the same sensory input? Ongoing fluctuations of neuronal excitability are currently hypothesized to underlie the trial-by-trial variability in sensory processing. To test this, we capitalized on intracranial electrophysiology in neurosurgical patients performing an auditory discrimination task with visual cues: specifically, we examined the interaction between prestimulus alpha oscillations, excitability, task performance, and decoded neural stimulus representations. We found that strong prestimulus oscillations in the alpha+ band (i.e., alpha and neighboring frequencies), rather than the aperiodic signal, correlated with a low excitability state, indexed by reduced broadband high-frequency activity. This state was related to slower reaction times and reduced neural stimulus encoding strength. We propose that the alpha+ rhythm modulates excitability, thereby resulting in variability in behavior and sensory representations despite identical input.

The Impact of Eye Closure on Anticipatory α Activity in a Tactile Discrimination Task.

One of the very first observations made regarding α oscillations (8-14 Hz), is that they increase in power over posterior areas when awake participants close their eyes. Recent work, especially in the context of (spatial) attention, suggests that α activity reflects a mechanism of functional inhibition. However, it remains unclear how eye closure impacts anticipatory α modulation observed in attention paradigms, and how this affects subsequent behavioral performance. Here, we recorded magnetoencephalography (MEG) in 33 human participants performing a tactile discrimination task with their eyes open versus closed. We replicated the hallmarks of previous somatosensory spatial attention studies: α lateralization across the somatosensory cortices as well as α increase over posterior (visual) regions. Furthermore, we found that eye closure leads to (1) reduced task performance; (2) widespread increase in α power; and (3) reduced anticipatory visual α modulation (4) with no effect on somatosensory α lateralization. Regardless of whether participants had their eyes open or closed, increased visual α power and somatosensory α lateralization improved their performance. Thus, we provide evidence that eye closure does not alter the impact of anticipatory α modulations on behavioral performance. We propose there is an optimal visual α level for somatosensory task performance, which can be achieved through a combination of eye closure and top-down anticipatory attention.

Alpha Oscillations Shape Sensory Representation and Perceptual Sensitivity.

Alpha activity (8-14 Hz) is the dominant rhythm in the awake brain and is thought to play an important role in setting the internal state of the brain. Previous work has associated states of decreased alpha power with enhanced neural excitability. However, evidence is mixed on whether and how such excitability enhancement modulates sensory signals of interest versus noise differently, and what, if any, are the consequences for subsequent perception. Here, human subjects (male and female) performed a visual detection task in which we manipulated their decision criteria in a blockwise manner. Although our manipulation led to substantial criterion shifts, these shifts were not reflected in prestimulus alpha band changes. Rather, lower prestimulus alpha power in occipital-parietal areas improved perceptual sensitivity and enhanced information content decodable from neural activity patterns. Additionally, oscillatory alpha phase immediately before stimulus presentation modulated accuracy. Together, our results suggest that alpha band dynamics modulate sensory signals of interest more strongly than noise.SIGNIFICANCE STATEMENT The internal state of our brain fluctuates, giving rise to variability in perception and action. Neural oscillations, most prominently in the alpha band, have been suggested to play a role in setting this internal state. Here, we show that ongoing alpha band activity in occipital-parietal regions predicts the quality of visual information decodable in neural activity patterns and subsequently the human observer's sensitivity in a visual detection task. Our results provide comprehensive evidence that visual representation is modulated by ongoing alpha band activity and advance our understanding on how, when faced with unchanging external stimuli, internal neural fluctuations influence perception and behavior.

Neural Encoding and Representation of Time for Sensorimotor Control and Learning.

The ability to perceive and produce movements in the real world with precise timing is critical for survival in animals, including humans. However, research on sensorimotor timing has rarely considered the tight interrelation between perception, action, and cognition. In this review, we present new evidence from behavioral, computational, and neural studies in humans and nonhuman primates, suggesting a pivotal link between sensorimotor control and temporal processing, as well as describing new theoretical frameworks regarding timing in perception and action. We first discuss the link between movement coordination and interval-based timing by addressing how motor training develops accurate spatiotemporal patterns in behavior and influences the perception of temporal intervals. We then discuss how motor expertise results from establishing task-relevant neural manifolds in sensorimotor cortical areas and how the geometry and dynamics of these manifolds help reduce timing variability. We also highlight how neural dynamics in sensorimotor areas are involved in beat-based timing. These lines of research aim to extend our understanding of how timing arises from and contributes to perceptual-motor behaviors in complex environments to seamlessly interact with other cognitive processes.

Morning brain: real-world neural evidence that high school class times matter.

Researchers, parents and educators consistently observe a stark mismatch between biologically preferred and socially imposed sleep-wake hours in adolescents, fueling debate about high school start times. We contribute neural evidence to this debate with electroencephalogram data collected from high school students during their regular morning, mid-morning and afternoon classes. Overall, student alpha power was lower when class content was taught via videos than through lectures. Students' resting state alpha brain activity decreased as the day progressed, consistent with adolescents being least attentive early in the morning. During the lessons, students showed consistently worse performance and higher alpha power for early morning classes than for mid-morning classes, while afternoon quiz scores and alpha levels varied. Together, our findings demonstrate that both class activity and class time are reflected in adolescents' brain states in a real-world setting, and corroborate educational research suggesting that mid-morning may be the best time to learn.

Dissociation of broadband high-frequency activity and neuronal firing in the neocortex.

Broadband high-frequency activity (BHA; 70 to 150 Hz), also known as "high gamma," a key analytic signal in human intracranial (electrocorticographic) recordings, is often assumed to reflect local neural firing [multiunit activity (MUA)]. As the precise physiological substrates of BHA are unknown, this assumption remains controversial. Our analysis of laminar multielectrode data from V1 and A1 in monkeys outlines two components of stimulus-evoked BHA distributed across the cortical layers: an "early-deep" and "late-superficial" response. Early-deep BHA has a clear spatial and temporal overlap with MUA. Late-superficial BHA was more prominent and accounted for more of the BHA signal measured near the cortical pial surface. However, its association with local MUA is weak and often undetectable, consistent with the view that it reflects dendritic processes separable from local neuronal firing.

Spontaneous Brain Oscillations and Perceptual Decision-Making.

Making rapid decisions on the basis of sensory information is essential to everyday behaviors. Why, then, are perceptual decisions so variable despite unchanging inputs? Spontaneous neural oscillations have emerged as a key predictor of trial-to-trial perceptual variability. New work casting these effects in the framework of models of perceptual decision-making has driven novel insight into how the amplitude of spontaneous oscillations impact decision-making. This synthesis reveals that the amplitude of ongoing low-frequency oscillations (<30 Hz), particularly in the alpha-band (8-13 Hz), bias sensory responses and change conscious perception but not, surprisingly, the underlying sensitivity of perception. A key model-based insight is that various decision thresholds do not adapt to alpha-related changes in sensory activity, demonstrating a seeming suboptimality of decision mechanisms in tracking endogenous changes in sensory responses.