Double Dissociation of Spontaneous Alpha-Band Activity and Pupil-Linked Arousal on Additive and Multiplicative Perceptual Gain.

Perception is a probabilistic process dependent on external stimulus properties and one's internal state. However, which internal states influence perception and via what mechanisms remain debated. We studied how spontaneous alpha-band activity (8-13 Hz) and pupil fluctuations impact visual detection and confidence across stimulus contrast levels (i.e., the contrast response function, CRF). In human subjects of both sexes, we found that low prestimulus alpha power induced an "additive" shift in the CRF, whereby stimuli were reported present more frequently at all contrast levels, including contrast of zero (i.e., false alarms). Conversely, prestimulus pupil size had a "multiplicative" effect on detection such that stimuli occurring during large pupil states (putatively corresponding to higher arousal) were perceived more frequently as contrast increased. Signal detection modeling reveals that alpha power changes detection criteria equally across the CRF but not detection sensitivity (d'), whereas pupil-linked arousal modulated sensitivity, particularly for higher contrasts. Interestingly, pupil size and alpha power were positively correlated, meaning that some of the effect of alpha on detection may be mediated by pupil fluctuations. However, pupil-independent alpha still induced an additive shift in the CRF corresponding to a criterion effect. Our data imply that low alpha boosts detection and confidence by an additive factor, rather than by a multiplicative scaling of contrast responses, a profile which captures the effect of pupil-linked arousal. We suggest that alpha power and arousal fluctuations have dissociable effects on behavior. Alpha reflects the baseline level of visual excitability, which can vary independent of arousal.

Alpha-Band Frequency and Temporal Windows in Perception: A Review and Living Meta-analysis of 27 Experiments (and Counting).

Temporal windows in perception refer to windows of time within which distinct stimuli interact to influence perception. A simple example is two temporally proximal stimuli fusing into a single percept. It has long been hypothesized that the human alpha rhythm (an 8- to 13-Hz neural oscillation maximal over posterior cortex) is linked to temporal windows, with higher frequencies corresponding to shorter windows and finer-grained temporal resolution. This hypothesis has garnered support from studies demonstrating a correlation between individual differences in alpha-band frequency (IAF) and behavioral measures of temporal processing. However, nonsignificant effects have also been reported. Here, we review and meta-analyze 27 experiments correlating IAF with measures of visual and audiovisual temporal processing. Our results estimate the true correlation in the population to be between .39 and .53, a medium-to-large effect. The effect held when considering visual or audiovisual experiments separately, when examining different IAF estimation protocols (i.e., eyes open and eyes closed), and when using analysis choices that favor a null result. Our review shows that (1) effects have been internally and independently replicated, (2) several positive effects are based on larger sample sizes than the null effects, and (3) many reported null effects are actually in the direction predicted by the hypothesis. A free interactive web app was developed to allow users to replicate our meta-analysis and change or update the study selection at will, making this a "living" meta-analysis (randfxmeta.streamlit.app). We discuss possible factors underlying null reports, design recommendations, and open questions for future research.

Alpha-band Brain Dynamics and Temporal Processing: An Introduction to the Special Focus.

For decades, the intriguing connection between the human alpha rhythm (an 8- to 13-Hz oscillation maximal over posterior cortex) and temporal processes in perception has furnished a rich landscape of proposals. The past decade, however, has seen a surge in interest in the topic, bringing new theoretical, analytic, and methodological developments alongside fresh controversies. This Special Focus on alpha-band dynamics and temporal processing provides an up-to-date snapshot of the playing field, with contributions from leading researchers in the field spanning original perspectives, new evidence, comprehensive reviews and meta-analyses, as well as discussion of ongoing controversies and paths forward. We hope that the perspectives captured here will help catalyze future research and shape the pathways toward a theoretically grounded and mechanistic account of the link between alpha dynamics and temporal properties of perception.

Neural Signatures of Evidence Accumulation Encode Subjective Perceptual Confidence Independent of Performance.

Confidence is an adaptive computation when environmental feedback is absent, yet there is little consensus regarding how perceptual confidence is computed in the brain. Difficulty arises because confidence correlates with other factors, such as accuracy, response time (RT), or evidence quality. We investigated whether neural signatures of evidence accumulation during a perceptual choice predict subjective confidence independently of these factors. Using motion stimuli, a central-parietal positive-going electroencephalogram component (CPP) behaves as an accumulating decision variable that predicts evidence quality, RT, accuracy, and confidence (Experiment 1, N = 25 adults). When we psychophysically varied confidence while holding accuracy constant (Experiment 2, N = 25 adults), the CPP still predicted confidence. Statistically controlling for RT, accuracy, and evidence quality (Experiment 3, N = 24 adults), the CPP still explained unique variance in confidence. The results indicate that a predecision neural signature of evidence accumulation, the CPP, encodes subjective perceptual confidence in decision-making independent of task performance.

Spectral Distribution Dynamics across Different Attentional Priority States.

Anticipatory covert spatial attention improves performance on tests of visual detection and discrimination, and shifts are accompanied by decreases and increases of α band power at electroencephalography (EEG) electrodes corresponding to the attended and unattended location, respectively. Although the increase at the unattended location is often interpreted as an active mechanism (e.g., inhibiting processing at the unattended location), most experiments cannot rule out the alternative possibility that it is a secondary consequence of selection elsewhere. To adjudicate between these accounts, we designed a Posner-style visual cueing task in which male and female human participants made orientation judgments of targets appearing at one of four locations: up, down, right, or left. Critically, trials were blocked such that within a block the locations along one meridian alternated in status between attended and unattended, and targets never appeared at the other two, making them irrelevant. Analyses of the concurrently measured EEG signal were conducted on "traditional" narrowband α (8-14 Hz), as well as on two components resulting from the decomposition of this signal: "periodic" α; and the slope of the aperiodic 1/f-like component. Although data from right-left blocks replicated the familiar pattern of lateralized asymmetry in narrowband α power, with neither α signal could we find evidence for any difference in the time course at unattended versus irrelevant locations, an outcome consistent with the secondary-consequence interpretation of attention-related dynamics in the α band. Additionally, 1/f slope was shallower at attended and unattended locations, relative to irrelevant, suggesting a tonic adjustment of physiological state.SIGNIFICANCE STATEMENT Visual spatial attention, the prioritization of one location in the visual field, is critical for guiding behavior in cluttered environments. Although influential theories posit an important role for α band oscillations in the inhibition of processing at unattended locations, we used a novel procedure to find evidence for an alternative interpretation: selection of one location may simply result in a return to physiological baseline at all others. In addition to determining one way that attention does not work (important for future progress in this field), we also discovered novel evidence for one way that it does work: by modifying the tonic physiological state (indexed by an aperiodic component of the electroencephalography (EEG)] at locations where spatial selection is likely to occur.

Evaluating the Evidence for the Functional Inhibition Account of Alpha-band Oscillations during Preparatory Attention.

The functional inhibition account states that alpha-band (8-14 Hz) power implements attentional control by selectively inhibiting task-irrelevant neural representations. This account has been well supported by decades of correlational research showing attention-related changes in the topography of alpha power in anticipation of task-relevant stimuli and is a viable theory of how attention impacts sensory processing, namely, via alpha power changes in sensory areas before stimulus onset. In addition, attention is known to modulate neural responses to stimuli themselves. Thus, a critical prediction of the functional inhibition account is that preparatory alpha modulations should explain variance in the degree of attention-related modulation of neural responses to stimuli. The present article sought evidence for or against this prediction by scouring the literature on attention and alpha oscillations to review papers that explicitly correlated attention-related changes in prestimulus alpha with attention-related changes in stimulus-evoked neural activity. Surprisingly, out of over 100 papers that were examined, we found only nine that explicitly computed such relationships. The results of these nine papers were mixed, with some in support and some arguing against the functional inhibition account of alpha. Our synthesis draws out common design features that may help explain when effects are observed or not. Even among studies that do find correlations, there is inconsistency as to whether preparatory alpha modulations are predictive of sensory or postsensory components of stimulus responses, highlighting avenues for future research. A clear outcome of this review is that future studies on the role of alpha in attentional processing should analyze correlations between attention effects on alpha and attention effects on stimulus-evoked activity, as more data pertinent to this hypothesized relationship are needed.

Effects of satisfying and violating expectations on serial dependence.

Serial dependence refers to the phenomenon that observers tend to report stimuli as being more similar to previous stimuli than they really are (attractive dependence) or, in some cases, as more different than they really are (repulsive dependence). Numerous experiments have demonstrated serial dependence for a range of modalities and stimulus features, highlighting the role of bottom-up sensory interactions. However, comparatively less research has focused on how higher-level cognitive factors, such as expectations, might influence serial dependence. Here, we manipulated expectations by having observers respond to target luminance gratings that occurred at the end of a sequence of non-target gratings. The sequence either rotated predictably (inducing an expectation), varied randomly (inducing no expectation), or rotated predictably but had a random target orientation (violating expectations). We found that observers produced less errors and indicated less uncertainty in their estimations of expected stimuli but their responses were biased away from the penultimate stimulus in the sequence (repulsive dependence). In contrast, following random sequences, responses showed an attractive bias to the penultimate stimulus in the sequence. Unexpected targets showed a mixture of both biases, such that when targets happened (by chance) to appear as expected, responses were repulsed, but responses to target orientations that more clearly violated expectations were attracted. These results indicate that, whereas attraction to previous stimuli may be a default strategy employed in response to random and unexpected events, certain expectations can reverse the default bias into a repulsive one.

Task feedback suggests a post-perceptual component to serial dependence.

Decisions across a range of perceptual tasks are biased toward past stimuli. Such serial dependence is thought to be an adaptive low-level mechanism that promotes perceptual stability across time. However, recent studies suggest post-perceptual mechanisms may also contribute to serially biased responses, calling into question a single locus of serial dependence and the nature of integration of past and present sensory inputs. We measured serial dependence in the context of a three-dimensional (3D) motion perception task where uncertainty in the sensory information varied substantially from trial to trial. We found that serial dependence varied with stimulus properties that impact sensory uncertainty on the current trial. Reduced stimulus contrast was associated with an increased bias toward the stimulus direction of the previous trial. Critically, performance feedback, which reduced sensory uncertainty, abolished serial dependence. These results provide clear evidence for a post-perceptual locus of serial dependence in 3D motion perception and support the role of serial dependence as a response strategy in the face of substantial sensory uncertainty.

Power spectrum slope confounds estimation of instantaneous oscillatory frequency.

Oscillatory neural dynamics are highly non-stationary and require methods capable of quantifying time-resolved changes in oscillatory activity in order to understand neural function. Recently, a method termed 'frequency sliding' was introduced to estimate the instantaneous frequency of oscillatory activity, providing a means of tracking temporal changes in the dominant frequency within a sub-band of field potential recordings. Here, the ability of frequency sliding to recover ground-truth oscillatory frequency in simulated data is tested while the exponent (slope) of the 1/fx component of the signal power spectrum is systematically varied, mimicking real electrophysiological data. The results show that 1) in the presence of 1/f activity, frequency sliding systematically underestimates the true frequency of the signal, 2) the magnitude of underestimation is correlated with the steepness of the slope, suggesting that, if unaccounted for, slope changes could be misinterpreted as frequency changes, 3) the impact of slope on frequency estimates interacts with oscillation amplitude, indicating that changes in oscillation amplitude alone may also influence instantaneous frequency estimates in the presence of strong 1/f activity; and 4) analysis parameters such as filter bandwidth and location also mediate the influence of slope on estimated frequency, indicating that these settings should be considered when interpreting estimates obtained via frequency sliding. The origin of these biases resides in the output of the filtering step of frequency sliding, whose energy is biased towards lower frequencies precisely because of the 1/f structure of the data. We discuss several strategies to mitigate these biases and provide a proof-of-principle for a 1/f normalization strategy.

Pre-stimulus alpha-band phase gates early visual cortex responses.

Alpha-band (8-13 Hz) oscillations have been shown to phasically inhibit perceptual reports in human observers, yet the underlying physiological mechanism of this effect is debated. According to contrasting models, based primarily on animal experiments, alpha activity is thought to either originate from specialized cells in the visual thalamus and periodically inhibit the relay of visual information to the primary visual cortex (V1) in a feedforward manner, or to propagate from higher visual areas back to V1 in a feedback manner. Human neurophysiological evidence in favor of either hypothesis, both, or neither, has been limited. To help address this issue, we explored the link between pre-stimulus alpha phase and visual electroencephalography (EEG) responses thought to arise from afferent input onto human V1. Specially-designed visual stimuli were used to elicit large amplitude C1 event-related potentials (ERP), with polarity, topography, and timing indicative of striate genesis. Single-trial circular-linear associations between pre-stimulus phase and post-stimulus global field power (GFP) during the C1 time window revealed significant effects peaking in the alpha frequency band. Control analyses ruling out the potential confound of post-stimulus data bleeding into the pre-stimulus window demonstrated that GFP amplitude decreases as pre-stimulus alpha phase deviates from an individual's preferred phase. These findings demonstrate an early locus - suggesting that the phase of pre-stimulus alpha oscillations could modulate visual processing by gating the feedforward flow of sensory input between the thalamus and V1, although other models are potentially compatible.

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.

No evidence for a single oscillator underlying discrete visual percepts.

Theories of perception based on discrete sampling posit that visual consciousness is reconstructed based on snapshot-like perceptual moments, as opposed to being updated continuously. According to a model proposed by Schneider (2018), discrete sampling can explain both the flash-lag and the Fröhlich illusion, whereby a lag in the conscious updating of a moving stimulus alters its perceived spatial location in comparison to stationary stimulus. The alpha-band frequency, which is associated with phasic modulation of stimulus detection and the temporal resolution of perception, has been proposed to reflect the duration of perceptual moments. The goal of this study was to determine whether a single oscillator (e.g., alpha) is underlying the duration of perceptual moments, which would predict that the point of subjective equality (PSE) in the flash-lag and Fröhlich illusions are positively correlated across individuals. Although our displays induced robust flash-lag and Fröhlich effects, virtually zero correlation was seen between the PSE in the two illusions, indicating that the illusion magnitudes are unrelated across observers. These findings suggest that, if discrete sampling theory is true, these illusory percepts either rely on different oscillatory frequencies or not on oscillations at all. Alternatively, discrete sampling may not be the mechanism underlying these two motion illusions or our methods were ill-suited to test the theory.

Spontaneous alpha-band amplitude predicts subjective visibility but not discrimination accuracy during high-level perception.

Near-threshold perception is a paradigm case of awareness diverging from reality - the perception of an unchanging stimulus can vacillate from undetected to clearly perceived. The amplitude of low-frequency brain oscillations - particularly in the alpha-band (8-13 Hz) - has emerged as a reliable predictor of trial-to-trial variability in perceptual decisions based on simple, low-level stimuli. Here, we addressed the question of how spontaneous oscillatory amplitude impacts subjective and objective aspects of perception using high-level visual stimuli. Human observers completed a near-threshold face/house discrimination task with subjective visibility ratings while electroencephalograms (EEG) were recorded. Using single-trial multiple regression analysis, we found that spontaneous fluctuations in prestimulus alpha-band amplitude were negatively related to visibility judgments but did not predict trial-by-trial accuracy. These results extend previous findings that indicate that strong prestimulus alpha diminishes subjective perception without affecting the accuracy or sensitivity (d') of perceptual decisions into the domain of high-level perception.

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.

Confidence boosts serial dependence in orientation estimation.

In the absence of external feedback, a decision maker must rely on a subjective estimate of their decision accuracy in order to appropriately guide behavior. Normative models of perceptual decision-making relate subjective estimates of internal signal quality (e.g., confidence) directly to the internal signal quality itself, thereby making it unknowable whether the subjective estimate or the underlying signal is what drives behavior. We constructed stimuli that dissociated the human observer's performance on a visual estimation task from their subjective estimates of confidence in their performance, thus violating normative principles. To understand whether confidence influences future decision-making, we examined serial dependence in observer's responses, a phenomenon whereby the estimate of a stimulus on the current trial can be biased toward the stimulus from the previous trial. We found that when decisions were made with high confidence, they conferred stronger biases upon the following trial, suggesting that confidence may enhance serial dependence. Critically, this finding was true also when confidence was experimentally dissociated from task performance, indicating that subjective confidence, independent of signal quality, can amplify serial dependence. These findings demonstrate an effect of confidence on future behavior, independent of task performance, and suggest that perceptual decisions incorporate recent history in an uncertainty-weighted manner, but where the uncertainty carried forward is a subjectively estimated and possibly suboptimal readout of objective sensory uncertainty.

Distinct Oscillatory Frequencies Underlie Excitability of Human Occipital and Parietal Cortex.

Transcranial magnetic stimulation (TMS) of human occipital and posterior parietal cortex can give rise to visual sensations called phosphenes. We used near-threshold TMS with concurrent EEG recordings to measure how oscillatory brain dynamics covary, on single trials, with the perception of phosphenes after occipital and parietal TMS. Prestimulus power and phase, predominantly in the alpha band (8-13 Hz), predicted occipital TMS phosphenes, whereas higher-frequency beta-band (13-20 Hz) power (but not phase) predicted parietal TMS phosphenes. TMS-evoked responses related to phosphene perception were similar across stimulation sites and were characterized by an early (200 ms) posterior negativity and a later (>300 ms) parietal positivity in the time domain and an increase in low-frequency (∼5-7 Hz) power followed by a broadband decrease in alpha/beta power in the time-frequency domain. These correlates of phosphene perception closely resemble known electrophysiological correlates of conscious perception of near-threshold visual stimuli. The regionally differential pattern of prestimulus predictors of phosphene perception suggests that distinct frequencies may reflect cortical excitability in occipital versus posterior parietal cortex, calling into question the broader assumption that the alpha rhythm may serve as a general index of cortical excitability.SIGNIFICANCE STATEMENT Alpha-band oscillations are thought to reflect cortical excitability and are therefore ascribed an important role in gating information transmission across cortex. We probed cortical excitability directly in human occipital and parietal cortex and observed that, whereas alpha-band dynamics indeed reflect excitability of occipital areas, beta-band activity was most predictive of parietal cortex excitability. Differences in the state of cortical excitability predicted perceptual outcomes (phosphenes), which were manifest in both early and late patterns of evoked activity, revealing the time course of phosphene perception. Our findings prompt revision of the notion that alpha activity reflects excitability across all of cortex and suggest instead that excitability in different regions is reflected in distinct frequency bands.

Three-Dimensional Digital Template Atlas of the Macaque Brain.

We present a new 3D template atlas of the anatomical subdivisions of the macaque brain, which is based on and aligned to the magnetic resonance imaging (MRI) data set and histological sections of the Saleem and Logothetis atlas. We describe the creation and validation of the atlas that, when registered with macaque structural or functional MRI scans, provides a straightforward means to estimate the boundaries between architectonic areas, either in a 3D volume with different planes of sections, or on an inflated brain surface (cortical flat map). As such, this new template atlas is intended for use as a reference standard for macaque brain research. Atlases and templates are available as both volumes and surfaces in standard NIFTI and GIFTI formats.

Top-down control of the phase of alpha-band oscillations as a mechanism for temporal prediction.

The physiological state of the brain before an incoming stimulus has substantial consequences for subsequent behavior and neural processing. For example, the phase of ongoing posterior alpha-band oscillations (8-14 Hz) immediately before visual stimulation has been shown to predict perceptual outcomes and downstream neural activity. Although this phenomenon suggests that these oscillations may phasically route information through functional networks, many accounts treat these periodic effects as a consequence of ongoing activity that is independent of behavioral strategy. Here, we investigated whether alpha-band phase can be guided by top-down control in a temporal cueing task. When participants were provided with cues predictive of the moment of visual target onset, discrimination accuracy improved and targets were more frequently reported as consciously seen, relative to unpredictive cues. This effect was accompanied by a significant shift in the phase of alpha-band oscillations, before target onset, toward each participant's optimal phase for stimulus discrimination. These findings provide direct evidence that forming predictions about when a stimulus will appear can bias the phase of ongoing alpha-band oscillations toward an optimal phase for visual processing, and may thus serve as a mechanism for the top-down control of visual processing guided by temporal predictions.

Preparatory Encoding of the Fine Scale of Human Spatial Attention.

Our attentional focus is constantly shifting: In one moment, our attention may be intently concentrated on a specific spot, whereas in another moment we might spread our attention more broadly. Although much is known about the mechanisms by which we shift our visual attention from place to place, relatively little is known about how we shift the aperture of attention from more narrowly to more broadly focused. Here we introduce a novel attentional distribution task to examine the neural mechanisms underlying this process. In this task, participants are presented with an informative cue that indicates the location of an upcoming target. This cue can be perfectly predictive of the exact target location, or it can indicate-with varying degrees of certainty-approximately where the target might appear. This cue is followed by a preparatory period in which there is nothing on the screen except a central fixation cross. Using scalp EEG, we examined neural activity during this preparatory period. We find that, with decreasing certainty regarding the precise location of the impending target, participant RTs increased whereas target identification accuracy decreased. Additionally, the multivariate pattern of preparatory period visual cortical alpha (8-12 Hz) activity encoded attentional distribution. This alpha encoding was predictive of behavioral accuracy and RT nearly 1 sec later. These results offer insight into the neural mechanisms underlying how we use information to guide our attentional distribution and how that influences behavior.

Correlated individual differences suggest a common mechanism underlying metacognition in visual perception and visual short-term memory.

Adaptive behaviour depends on the ability to introspect accurately about one's own performance. Whether this metacognitive ability is supported by the same mechanisms across different tasks is unclear. We investigated the relationship between metacognition of visual perception and metacognition of visual short-term memory (VSTM). Experiments 1 and 2 required subjects to estimate the perceived or remembered orientation of a grating stimulus and rate their confidence. We observed strong positive correlations between individual differences in metacognitive accuracy between the two tasks. This relationship was not accounted for by individual differences in task performance or average confidence, and was present across two different metrics of metacognition and in both experiments. A model-based analysis of data from a third experiment showed that a cross-domain correlation only emerged when both tasks shared the same task-relevant stimulus feature. That is, metacognition for perception and VSTM were correlated when both tasks required orientation judgements, but not when the perceptual task was switched to require contrast judgements. In contrast with previous results comparing perception and long-term memory, which have largely provided evidence for domain-specific metacognitive processes, the current findings suggest that metacognition of visual perception and VSTM is supported by a domain-general metacognitive architecture, but only when both domains share the same task-relevant stimulus feature.