Alpha Oscillations Create the Illusion of Time.

Recent neuroscience experiments have brought inconsistent findings to light about the influence of neural activity in the alpha-frequency band (at ≈10 Hz) on the temporal dynamics of visual perception. Whereas strong alpha effects were found when perception was more based on endogenous factors, there were null-effects for alpha when perception relied more on objective physical parameters. In this Perspective, I open up a new view on neural alpha activity that resolves some important aspects of this controversy by interpreting alpha not as temporal processing of sensory inputs per se but above all as the observer's internal processing dynamics, their so-called perception sets. Perception sets reflect internally stored knowledge for how to organize and build up perceptual processes. They result from previous sensory experiences, are under top-down control to support goal-directed behavior, and root in pre-established neural networks that communicate through alpha frequency channels. I present three example cases from the recent neuroscience literature that show an influence of alpha-driven perception sets on the observer's visual-temporal resolution, object processing, and the processing of behaviorally relevant image content. Because alpha-driven perception sets can structure perception from its high-level aspects, like categories, down to its basic building blocks, like objects and time samples, they may have a fundamental impact on our conscious experience of the sensory world, including our perception of time itself.

Brain development: Viewing the world through infants' eyes.

Categories help us make sense of sensory input. A new study has directly compared category-related brain signals between human infants and adults, discovering delayed and temporally highly compressed processing in infants.

Efficient Prestimulus Network Integration of Fusiform Face Area Biases Face Perception during Binocular Rivalry.

Ongoing fluctuations in neural excitability and connectivity influence whether or not a stimulus is seen. Do they also influence which stimulus is seen? We recorded magnetoencephalography data while 21 human participants viewed face or house stimuli, either one at a time or under bistable conditions induced through binocular rivalry. Multivariate pattern analysis revealed common neural substrates for rivalrous versus nonrivalrous stimuli with an additional delay of ∼36 msec for the bistable stimulus, and poststimulus signals were source-localized to the fusiform face area. Before stimulus onset followed by a face versus house report, fusiform face area showed stronger connectivity to primary visual cortex and to the rest of the cortex in the alpha frequency range (8-13 Hz), but there were no differences in local oscillatory alpha power. The prestimulus connectivity metrics predicted the accuracy of poststimulus decoding and the delay associated with rivalry disambiguation suggesting that perceptual content is shaped by ongoing neural network states.

Pre-stimulus alpha-band power and phase fluctuations originate from different neural sources and exert distinct impact on stimulus-evoked responses.

Ongoing oscillatory neural activity before stimulus onset influences subsequent visual perception. Specifically, both the power and the phase of oscillations in the alpha-frequency band (9-13 Hz) have been reported to predict the detection of visual stimuli. Up to now, the functional mechanisms underlying pre-stimulus power and phase effects on upcoming visual percepts are debated. Here, we used magnetoencephalography recordings together with a near-threshold visual detection task to investigate the neural generators of pre-stimulus power and phase and their impact on subsequent visual-evoked responses. Pre-stimulus alpha-band power and phase opposition effects were found consistent with previous reports. Source localization suggested clearly distinct neural generators for these pre-stimulus effects: Power effects were mainly found in occipital-temporal regions, whereas phase effects also involved prefrontal areas. In order to be functionally relevant, the pre-stimulus correlates should influence post-stimulus processing. Using a trial-sorting approach, we observed that only pre-stimulus power modulated the Hits versus Misses difference in the evoked response, a well-established post-stimulus neural correlate of near-threshold perception, such that trials with stronger pre-stimulus power effect showed greater post-stimulus difference. By contrast, no influence of pre-stimulus phase effects were found. In sum, our study shows distinct generators for two pre-stimulus neural patterns predicting visual perception, and that only alpha power impacts the post-stimulus correlate of conscious access. This underlines the functional relevance of prestimulus alpha power on perceptual awareness, while questioning the role of alpha phase.

New methods for oscillation analyses push new theories of discrete cognition.

Classical ways of analyzing neural time series data has led to static views on cognition, in which the cognitive processes are linked to sustained neural activity and interpreted as stationary states. The core analytical focus was on slow power modulations of neural oscillations averaged across many experimental trials. Whereas this custom analytical approach reduces the complexity and increases the signal-to-noise ratio, it may disregard or even remove important aspects of the underlying neural dynamics. Novel analysis methods investigate the instantaneous frequency and phase of neural oscillations and relate them to the precisely controlled timing of brief successive sensory stimuli. This enables to capture how cognitive processes unfold in discrete windows within and across oscillatory cycles. Moreover, several recent studies analyze the oscillatory power modulations on single experimental trials. They suggest that the power modulations are packed into discrete bursts of activity, which occur at different rates and times, and with different durations from trial-to-trial. Here, we review the current work that made use of these methodological advances for neural oscillations. These novel analysis perspectives emphasize that cognitive processes occur in discrete time windows, instead of sustained, stationary states. Evidence for discretization was observed for the entire range of cognitive functions from perception and attention to working memory, goal-directed thought and motor actions, as well as throughout the entire cortical hierarchy and in subcortical regions. These empirical observations create demand for new psychological theories and computational models of cognition in the brain, which integrate its discrete temporal dynamics.

Enumerating the forest before the trees: The time courses of estimation-based and individuation-based numerical processing.

Ensemble perception refers to the ability to report attributes of a group of objects, rather than focusing on only one or a few individuals. An everyday example of ensemble perception is the ability to estimate the numerosity of a large number of items. The time course of ensemble processing, including that of numerical estimation, remains a matter of debate, with some studies arguing for rapid, "preattentive" processing and other studies suggesting that ensemble perception improves with longer presentation durations. We used a forward-simultaneous masking procedure that effectively controls stimulus durations to directly measure the temporal dynamics of ensemble estimation and compared it with more precise enumeration of individual objects. Our main finding was that object individuation within the subitizing range (one to four items) took about 100-150 ms to reach its typical capacity limits, whereas estimation (six or more items) showed a temporal resolution of 50 ms or less. Estimation accuracy did not improve over time. Instead, there was an increasing tendency, with longer effective durations, to underestimate the number of targets for larger set sizes (11-35 items). Overall, the time course of enumeration for one or a few single items was dramatically different from that of estimating numerosity of six or more items. These results are consistent with the idea that the temporal resolution of ensemble processing may be as rapid as, or even faster than, individuation of individual items, and support a basic distinction between the mechanisms underlying exact enumeration of small sets (one to four items) from estimation.

Oscillatory Bursts in Parietal Cortex Reflect Dynamic Attention between Multiple Objects and Ensembles.

The visual system uses two complimentary strategies to process multiple objects simultaneously within a scene and update their spatial positions in real time. It either uses selective attention to individuate a complex, dynamic scene into a few focal objects (i.e., object individuation), or it represents multiple objects as an ensemble by distributing attention more globally across the scene (i.e., ensemble grouping). Neural oscillations may be a key signature for focal object individuation versus distributed ensemble grouping, because they are thought to regulate neural excitability over visual areas through inhibitory control mechanisms. We recorded whole-head MEG data during a multiple-object tracking paradigm, in which human participants (13 female, 11 male) switched between different instructions for object individuation and ensemble grouping on different trials. The stimuli, responses, and the demand to keep track of multiple spatial locations over time were held constant between the two conditions. We observed increased α-band power (9-13 Hz) packed into oscillatory bursts in bilateral inferior parietal cortex during multiple-object processing. Single-trial analysis revealed greater burst occurrences on object individuation versus ensemble grouping trials. By contrast, we found no differences using standard analyses on across-trials averaged α-band power. Moreover, the bursting effects occurred only below/at, but not above, the typical capacity limits for multiple-object processing (at ∼4 objects). Our findings reveal the real-time neural correlates underlying the dynamic processing of multiple-object scenarios, which are modulated by grouping strategies and capacity. They support a rhythmic, α-pulsed organization of dynamic attention to multiple objects and ensembles.SIGNIFICANCE STATEMENT Dynamic multiple-object scenarios are an important problem in real-world and computer vision. They require keeping track of multiple objects as they move through space and time. Such problems can be solved in two ways: One can individuate a scene object by object, or alternatively group objects into ensembles. We observed greater occurrences of α-oscillatory burst events in parietal cortex for processing objects versus ensembles and below/at versus above processing capacity. These results demonstrate a unique top-down mechanism by which the brain dynamically adjusts its computational level between objects and ensembles. They help to explain how the brain copes with its capacity limitations in real-time environments and may lead the way to technological innovations for time-critical video analysis in computer vision.

Brain Mechanisms of Concept Learning.

Concept learning, the ability to extract commonalities and highlight distinctions across a set of related experiences to build organized knowledge, is a critical aspect of cognition. Previous reviews have focused on concept learning research as a means for dissociating multiple brain systems. The current review surveys recent work that uses novel analytical approaches, including the combination of computational modeling with neural measures, focused on testing theories of specific computations and representations that contribute to concept learning. We discuss in detail the roles of the hippocampus, ventromedial prefrontal, lateral prefrontal, and lateral parietal cortices, and how their engagement is modulated by the coherence of experiences and the current learning goals. We conclude that the interaction of multiple brain systems relating to learning, memory, attention, perception, and reward support a flexible concept-learning mechanism that adapts to a range of category structures and incorporates motivational states, making concept learning a fruitful research domain for understanding the neural dynamics underlying complex behaviors.

Prestimulus feedback connectivity biases the content of visual experiences.

Ongoing fluctuations in neural excitability and in networkwide activity patterns before stimulus onset have been proposed to underlie variability in near-threshold stimulus detection paradigms-that is, whether or not an object is perceived. Here, we investigated the impact of prestimulus neural fluctuations on the content of perception-that is, whether one or another object is perceived. We recorded neural activity with magnetoencephalography (MEG) before and while participants briefly viewed an ambiguous image, the Rubin face/vase illusion, and required them to report their perceived interpretation in each trial. Using multivariate pattern analysis, we showed robust decoding of the perceptual report during the poststimulus period. Applying source localization to the classifier weights suggested early recruitment of primary visual cortex (V1) and ∼160-ms recruitment of the category-sensitive fusiform face area (FFA). These poststimulus effects were accompanied by stronger oscillatory power in the gamma frequency band for face vs. vase reports. In prestimulus intervals, we found no differences in oscillatory power between face vs. vase reports in V1 or in FFA, indicating similar levels of neural excitability. Despite this, we found stronger connectivity between V1 and FFA before face reports for low-frequency oscillations. Specifically, the strength of prestimulus feedback connectivity (i.e., Granger causality) from FFA to V1 predicted not only the category of the upcoming percept but also the strength of poststimulus neural activity associated with the percept. Our work shows that prestimulus network states can help shape future processing in category-sensitive brain regions and in this way bias the content of visual experiences.

Different Levels of Category Abstraction by Different Dynamics in Different Prefrontal Areas.

Categories can be grouped by shared sensory attributes (i.e., cats) or a more abstract rule (i.e., animals). We explored the neural basis of abstraction by recording from multi-electrode arrays in prefrontal cortex (PFC) while monkeys performed a dot-pattern categorization task. Category abstraction was varied by the degree of exemplar distortion from the prototype pattern. Different dynamics in different PFC regions processed different levels of category abstraction. Bottom-up dynamics (stimulus-locked gamma power and spiking) in the ventral PFC processed more low-level abstractions, whereas top-down dynamics (beta power and beta spike-LFP coherence) in the dorsal PFC processed more high-level abstractions. Our results suggest a two-stage, rhythm-based model for abstracting categories.

Frequency modulation of neural oscillations according to visual task demands.

Temporal integration in visual perception is thought to occur within cycles of occipital alpha-band (8-12 Hz) oscillations. Successive stimuli may be integrated when they fall within the same alpha cycle and segregated for different alpha cycles. Consequently, the speed of alpha oscillations correlates with the temporal resolution of perception, such that lower alpha frequencies provide longer time windows for perceptual integration and higher alpha frequencies correspond to faster sampling and segregation. Can the brain's rhythmic activity be dynamically controlled to adjust its processing speed according to different visual task demands? We recorded magnetoencephalography (MEG) while participants switched between task instructions for temporal integration and segregation, holding stimuli and task difficulty constant. We found that the peak frequency of alpha oscillations decreased when visual task demands required temporal integration compared with segregation. Alpha frequency was strategically modulated immediately before and during stimulus processing, suggesting a preparatory top-down source of modulation. Its neural generators were located in occipital and inferotemporal cortex. The frequency modulation was specific to alpha oscillations and did not occur in the delta (1-3 Hz), theta (3-7 Hz), beta (15-30 Hz), or gamma (30-50 Hz) frequency range. These results show that alpha frequency is under top-down control to increase or decrease the temporal resolution of visual perception.

Nonretinotopic perception of orientation: Temporal integration of basic features operates in object-based coordinates.

Early, feed-forward visual processing is organized in a retinotopic reference frame. In contrast, visual feature integration on longer time scales can involve object-based or spatiotopic coordinates. For example, in the Ternus-Pikler (T-P) apparent motion display, object identity is mapped across the object motion path. Here, we report evidence from three experiments supporting nonretinotopic feature integration even for the most paradigmatic example of retinotopically-defined features: orientation. We presented observers with a repeated series of T-P displays in which the perceived rotation of Gabor gratings indicates processing in either retinotopic or object-based coordinates. In Experiment 1, the frequency of perceived retinotopic rotations decreased exponentially for longer interstimulus intervals (ISIs) between T-P display frames, with object-based percepts dominating after about 150-250 ms. In a second experiment, we show that motion and rotation judgments depend on the perception of a moving object during the T-P display ISIs rather than only on temporal factors. In Experiment 3, we cued the observers' attentional state either toward a retinotopic or object motion-based reference frame and then tracked both the observers' eye position and the time course of the perceptual bias while viewing identical T-P display sequences. Overall, we report novel evidence for spatiotemporal integration of even basic visual features such as orientation in nonretinotopic coordinates, in order to support perceptual constancy across self- and object motion.

Temporal Integration Windows in Neural Processing and Perception Aligned to Saccadic Eye Movements.

When processing dynamic input, the brain balances the opposing needs of temporal integration and sensitivity to change. We hypothesized that the visual system might resolve this challenge by aligning integration windows to the onset of newly arriving sensory samples. In a series of experiments, human participants observed the same sequence of two displays separated by a brief blank delay when performing either an integration or segregation task. First, using magneto-encephalography (MEG), we found a shift in the stimulus-evoked time courses by a 150-ms time window between task signals. After stimulus onset, multivariate pattern analysis (MVPA) decoding of task in occipital-parietal sources remained above chance for almost 1 s, and the task-decoding pattern interacted with task outcome. In the pre-stimulus period, the oscillatory phase in the theta frequency band was informative about both task processing and behavioral outcome for each task separately, suggesting that the post-stimulus effects were caused by a theta-band phase shift. Second, when aligning stimulus presentation to the onset of eye fixations, there was a similar phase shift in behavioral performance according to task demands. In both MEG and behavioral measures, task processing was optimal first for segregation and then integration, with opposite phase in the theta frequency range (3-5 Hz). The best fit to neurophysiological and behavioral data was given by a dampened 3-Hz oscillation from stimulus or eye fixation onset. The alignment of temporal integration windows to input changes found here may serve to actively organize the temporal processing of continuous sensory input.

Dense sampling reveals behavioral oscillations in rapid visual categorization.

Perceptual systems must create discrete objects and events out of a continuous flow of sensory information. Previous studies have demonstrated oscillatory effects in the behavioral outcome of low-level visual tasks, suggesting a cyclic nature of visual processing as the solution. To investigate whether these effects extend to more complex tasks, a stream of "neutral" photographic images (not containing targets) was rapidly presented (20 ms/image). Embedded were one or two presentations of a randomly selected target image (vehicles and animals). Subjects reported the perceived target category. On dual-presentation trials, the ISI varied systematically from 0 to 600 ms. At randomized timing before first target presentation, the screen was flashed with the intent of creating a phase reset in the visual system. Sorting trials by temporal distance between flash and first target presentation revealed strong oscillations in behavioral performance, peaking at 5 Hz. On dual-target trials, longer ISIs led to reduced performance, implying a temporal integration window for object category discrimination. The "animal" trials exhibited a significant oscillatory component around 5 Hz. Our results indicate that oscillatory effects are not mere fringe effects relevant only with simple stimuli, but are resultant from the core mechanisms of visual processing and may well extend into real-life scenarios.

Expansion and Compression of Time Correlate with Information Processing in an Enumeration Task.

Perception of temporal duration is subjective and is influenced by factors such as attention and context. For example, unexpected or emotional events are often experienced as if time subjectively expands, suggesting that the amount of information processed in a unit of time can be increased. Time dilation effects have been measured with an oddball paradigm in which an infrequent stimulus is perceived to last longer than standard stimuli in the rest of the sequence. Likewise, time compression for the oddball occurs when the duration of the standard items is relatively brief. Here, we investigated whether the amount of information processing changes when time is perceived as distorted. On each trial, an oddball stimulus of varying numerosity (1-14 items) and duration was presented along with standard items that were either short (70 ms) or long (1050 ms). Observers were instructed to count the number of dots within the oddball stimulus and to judge its relative duration with respect to the standards on that trial. Consistent with previous results, oddballs were reliably perceived as temporally distorted: expanded for longer standard stimuli blocks and compressed for shorter standards. The occurrence of these distortions of time perception correlated with perceptual processing; i.e. enumeration accuracy increased when time was perceived as expanded and decreased with temporal compression. These results suggest that subjective time distortions are not epiphenomenal, but reflect real changes in sensory processing. Such short-term plasticity in information processing rate could be evolutionarily advantageous in optimizing perception and action during critical moments.

The temporal window of individuation limits visual capacity.

One of the main tasks of vision is to individuate and recognize specific objects. Unlike the detection of basic features, object individuation is strictly limited in capacity. Previous studies of capacity, in terms of subitizing ranges or visual working memory, have emphasized spatial limits in the number of objects that can be apprehended simultaneously. Here, we present psychophysical and electrophysiological evidence that capacity limits depend instead on time. Contrary to what is commonly assumed, subitizing, the reading-out a small set of individual objects, is not an instantaneous process. Instead, individuation capacity increases in steps within the lifetime of visual persistence of the stimulus, suggesting that visual capacity limitations arise as a result of the narrow window of feedforward processing. We characterize this temporal window as coordinating individuation and integration of sensory information over a brief interval of around 100 ms. Neural signatures of integration windows are revealed in reset alpha oscillations shortly after stimulus onset within generators in parietal areas. Our findings suggest that short-lived alpha phase synchronization (≈1 cycle) is key for individuation and integration of visual transients on rapid time scales (<100 ms). Within this time frame intermediate-level vision provides an equilibrium between the competing needs to individuate invariant objects, integrate information about those objects over time, and remain sensitive to dynamic changes in sensory input. We discuss theoretical and practical implications of temporal windows in visual processing, how they create a fundamental capacity limit, and their role in constraining the real-time dynamics of visual processing.

Temporal windows in visual processing: "prestimulus brain state" and "poststimulus phase reset" segregate visual transients on different temporal scales.

Dynamic vision requires both stability of the current perceptual representation and sensitivity to the accumulation of sensory evidence over time. Here we study the electrophysiological signatures of this intricate balance between temporal segregation and integration in vision. Within a forward masking paradigm with short and long stimulus onset asynchronies (SOA), we manipulated the temporal overlap of the visual persistence of two successive transients. Human observers enumerated the items presented in the second target display as a measure of the informational capacity read-out from this partly temporally integrated visual percept. We observed higher ß-power immediately before mask display onset in incorrect trials, in which enumeration failed due to stronger integration of mask and target visual information. This effect was timescale specific, distinguishing between segregation and integration of visual transients that were distant in time (long SOA). Conversely, for short SOA trials, mask onset evoked a stronger visual response when mask and targets were correctly segregated in time. Examination of the target-related response profile revealed the importance of an evoked α-phase reset for the segregation of those rapid visual transients. Investigating this precise mapping of the temporal relationships of visual signals onto electrophysiological responses highlights how the stream of visual information is carved up into discrete temporal windows that mediate between segregated and integrated percepts. Fragmenting the stream of visual information provides a means to stabilize perceptual events within one instant in time.

Temporal buffering and visual capacity: the time course of object formation underlies capacity limits in visual cognition.

Capacity limits are a hallmark of visual cognition. The upper boundary of our ability to individuate and remember objects is well known but-despite its central role in visual information processing-not well understood. Here, we investigated the role of temporal limits in the perceptual processes of forming "object files." Specifically, we examined the two fundamental mechanisms of object file formation-individuation and identification-by selectively interfering with visual processing by using forward and backward masking with variable stimulus onset asynchronies. While target detection was almost unaffected by these two types of masking, they showed distinct effects on the two different stages of object formation. Forward "integration" masking selectively impaired object individuation, whereas backward "interruption" masking only affected identification and the consolidation of information into visual working memory. We therefore conclude that the inherent temporal dynamics of visual information processing are an essential component in creating the capacity limits in object individuation and visual working memory.

Top-down control in contour grouping.

Human observers tend to group oriented line segments into full contours if they follow the Gestalt rule of 'good continuation'. It is commonly assumed that contour grouping emerges automatically in early visual cortex. In contrast, recent work in animal models suggests that contour grouping requires learning and thus involves top-down control from higher brain structures. Here we explore mechanisms of top-down control in perceptual grouping by investigating synchronicity within EEG oscillations. Human participants saw two micro-Gabor arrays in a random order, with the task to indicate whether the first (S1) or the second stimulus (S2) contained a contour of collinearly aligned elements. Contour compared to non-contour S1 produced a larger posterior post-stimulus beta power (15-21 Hz). Contour S2 was associated with a pre-stimulus decrease in posterior alpha power (11-12 Hz) and in fronto-posterior theta (4-5 Hz) phase couplings, but not with a post-stimulus increase in beta power. The results indicate that subjects used prior knowledge from S1 processing for S2 contour grouping. Expanding previous work on theta oscillations, we propose that long-range theta synchrony shapes neural responses to perceptual groupings regulating lateral inhibition in early visual cortex.