Jason Samaha

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

Significance In contrast to canonical, stimulus-driven models of perception, recent proposals argue that perceptual experiences are constructed in an active manner in which top-down influences play a key role. In particular, predictions that the brain makes about the world are incorporated into each perceptual experience. Because forming the appropriate sensory predictions can have a large impact on our visual experiences and visually guided behaviors, a mechanism thought to be disrupted in certain neurological conditions like autism and schizophrenia, an understanding of the neural basis of these predictions is critical. Here, we provide evidence that perceptual expectations about when a stimulus will appear are instantiated in the brain by optimally configuring prestimulus alpha-band oscillations so as to make subsequent processing most efficacious. 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.

The Speed of Alpha-Band Oscillations Predicts the Temporal Resolution of Visual Perception

Evidence suggests that scalp-recorded occipital alpha-band (8-13 Hz) oscillations reflect phasic information transfer in thalamocortical neurons projecting from lateral geniculate nucleus to visual cortex. In animals, the phase of ongoing alpha oscillations has been shown to modulate stimulus discrimination and neuronal spiking. Human research has shown that alpha phase predicts visual perception of near-threshold stimuli and subsequent neural activity and that the frequency of these oscillations predicts reaction times, as well as the maximum temporal interval necessary for perceived simultaneity. These phasic effects have led to the hypothesis that conscious perception occurs in discrete temporal windows, clocked by the frequency of alpha oscillations. Under this hypothesis, variation in the frequency of occipital alpha oscillations should predict variation in the temporal resolution of visual perception. Specifically, when two stimuli fall within the same alpha cycle, they may be perceived as a single stimulus, resulting in perception with lower temporal resolution when alpha frequency is lower. We tested this by assessing the relationship between two-flash fusion thresholds (a measure of the temporal resolution of visual perception) and the frequency of eyes-closed and task-related alpha rhythms. We found, both between and within subjects, that faster alpha frequencies predicted more accurate flash discrimination, providing novel evidence linking alpha frequency to the temporal resolution of perception.

Decoding and reconstructing the focus of spatial attention from the topography of alpha-band oscillations

Many aspects of perception and cognition are supported by activity in neural populations that are tuned to different stimulus features (e.g., orientation, spatial location, color). Goal-directed behavior, such as sustained attention, requires a mechanism for the selective prioritization of contextually appropriate representations. A candidate mechanism of sustained spatial attention is neural activity in the alpha band (8–13 Hz), whose power in the human EEG covaries with the focus of covert attention. Here, we applied an inverted encoding model to assess whether spatially selective neural responses could be recovered from the topography of alpha-band oscillations during spatial attention. Participants were cued to covertly attend to one of six spatial locations arranged concentrically around fixation while EEG was recorded. A linear classifier applied to EEG data during sustained attention demonstrated successful classification of the attended location from the topography of alpha power, although not from other frequency bands. We next sought to reconstruct the focus of spatial attention over time by applying inverted encoding models to the topography of alpha power and phase. Alpha power, but not phase, allowed for robust reconstructions of the specific attended location beginning around 450 msec postcue, an onset earlier than previous reports. These results demonstrate that posterior alpha-band oscillations can be used to track activity in feature-selective neural populations with high temporal precision during the deployment of covert spatial attention.

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.

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.

Prestimulus alpha-band power biases visual discrimination confidence, but not accuracy

The magnitude of power in the alpha-band (8-13Hz) of the electroencephalogram (EEG) prior to the onset of a near threshold visual stimulus predicts performance. Together with other findings, this has been interpreted as evidence that alpha-band dynamics reflect cortical excitability. We reasoned, however, that non-specific changes in excitability would be expected to influence signal and noise in the same way, leaving actual discriminability unchanged. Indeed, using a two-choice orientation discrimination task, we found that discrimination accuracy was unaffected by fluctuations in prestimulus alpha power. Decision confidence, on the other hand, was strongly negatively correlated with prestimulus alpha power. This finding constitutes a clear dissociation between objective and subjective measures of visual perception as a function of prestimulus cortical excitability. This dissociation is predicted by a model where the balance of evidence supporting each choice drives objective performance but only the magnitude of evidence supporting the selected choice drives subjective reports, suggesting that human perceptual confidence can be suboptimal with respect to tracking objective accuracy.

How best to study the function of consciousness

A central project within the scientific study of consciousness is that of uncovering the role that consciousness has in behavior. Under some accounts, the temporary retention of information (short-term or working memory) is accomplished via the maintenance of a conscious representation of that information, and is a candidate function of consciousness (Atkinson and Shiffrin, 1968; Baars and Franklin, 2003). However, recent experiments demonstrating that stimuli rated by observers as invisible can nevertheless be retained over a delay period, suggest that working memory (WM) may, under some conditions, operate unconsciously (Soto et al., 2011; Bergstrom and Eriksson, 2014). Accepting this conclusion would raise important questions about the classical view that WM may be a biological function of consciousness. Complicating this line of research, however, are long-standing concerns in the study of unconscious cognition as to whether one can be certain in establishing complete unawareness. Here, I discuss how recent conceptual and methodological advances in the study of visual awareness might profitably be adapted to study the role of awareness in WM and to study the functional consequences of conscious perception more generally. The strength of the claim that a cognitive process occurs in the absence of awareness rests on the extent to which absolute unawareness was actually achieved. A problematic issue for any study investigating unconscious processing is that of assuring that the reporting methodology employed (1) adequately captures all relevant consciously perceived information, and (2) that observers truly have complete unawareness when they are claiming so (Overgaard et al., 2006). If these conditions are not met, behavior seeming to occur unconsciously may actually be the result of degraded, but conscious perceptual information processing. These issues are particularly salient with regard to recent experiments testing for unconscious working memory (e.g., Soto et al., 2011). In these experiments, the researchers arguments rely on observers being completely unaware of all relevant features of the remembered stimulus (otherwise performance could be attributed to residual conscious processing). As there is currently no consensus regarding the most exhaustive measure of consciousness (Seth et al., 2008), proving complete unawareness of all relevant features of a stimulus may be a suboptimal approach to studying the function of consciousness. An alternative approach, coined “relative blindsight” (Lau and Passingham, 2006), comes from experimental paradigms in which observers are presented with two or more stimulus conditions for which their perceptual discrimination performance (e.g., d-prime) is matched, yet, subjectively, their confidence or reports of having seen the stimulus vary (Lau and Passingham, 2006; Zylberberg et al., 2012). In these paradigms, awareness is not entirely obliterated, but rather a relative difference exists between two otherwise performance-matched conditions. This contrast in the level of awareness effectively isolates the subjective construct of having seen a stimulus while ruling out confounds due to performance factors like attention, arousal, and motivation, which would presumably also affect objective performance. Furthermore, whereas many existing approaches render stimuli unconscious by degrading them until objective performance is at floor, this approach preserves some performance and thereby alleviates uncertainty that a null finding is simply due to weak stimuli. These paradigms can be applied to the study of the function of subjective awareness in the following way: if, under conditions of relative blindsight, one condition has fewer trials during which a stimulus is subjectively seen, any post-perceptual cognitive process hypothesized to rely on subjective awareness should show a corresponding decline in functionality, otherwise the cognitive process cannot be said to depend on subjective awareness. Although reports about visual awareness are not perfect reflections of phenomenology, and may be better characterized as metacognitive, the subjective feeling of knowing that one has perceived a stimulus often accompanies our conscious sensations, and should be considered a central aspect of visual consciousness. Methodologically, relative blindsight has been induced by manipulating the absolute amount and the ratio of target to non-target sensory evidence (Zylberberg et al., 2012), or by contrasting different stimulus onset asynchronies (SOA) during metacontrast masking (Lau and Passingham, 2006) (but see Jannati and Di Lollo, 2012). Using these stimulus conditions as the memoranda in WM tasks provides a means of directly testing whether subjective visual awareness improves visual WM. If subjectively experiencing a visual stimulus enhances the retention of that information, then memory performance should be better for the high-awareness, as contrasted with the low-awareness conditions. Because initial perceptual discrimination has been equated, any performance differences related to awareness can be isolated to post-perceptual WM processes such as memory maintenance. This paradigm can be adapted to address further questions as to whether awareness confers any other type of benefit to WM. By introducing distractors to the delay period of a task, or by having participants hold multiple stimuli in mind, one can test the role that awareness might play in the capacity and distractor resilience of WM processes. Additionally, one could require responses on a continuous scale as a test of the hypothesis that subjective awareness enhances the fidelity of WM. Another intriguing avenue for exploration would be to present multiple items during encoding and employ a retrocue design (Oberauer, 2002) to assess whether the ability to shift attention between items in WM depends on the items being represented consciously. If attention could be allocated to unconscious items in WM (as indexed by enhanced memory of attended information), this would shed light on another important and ongoing debate regarding the dissociation between attention and awareness, but in the WM domain. In this way, relative blindsight paradigms can be adapted to many tasks investigating the role of subjective visual awareness in cognitive processes while circumventing confounds and assumptions associated with creating conditions of complete unawareness. A limitation of the relative blindsight approach is that by virtue of requiring a contrast between two performance-matched stimulus conditions, physical stimulus properties (such as SOAs or signal-to-noise ratios) also vary across conditions. With respect to metacontrast masking, for example, it has been argued that relative blindsight arises from a confound in the physical stimulus attributes that drive responses at short versus long SOAs (Jannati and Di Lollo, 2012). For this reason, a more recent method of inducing relative blindsight, based on manipultating signal-to-noise ratio (Zylberberg et al., 2012), may be preferred. This issue is also problematic for studies investigating the neural correlates of consciousness, especially those focused on brain areas whose activity is known to reflect physical stimulus differences, such as early visual cortex. By the same logic, this issue may be less problematic when investigating regions whose activity can be shown to be insensitive to physical stimulus properties. This concern can also be mitigated analytically by testing whether the cognitive function or neural activity under investigation also varies with awareness within a single stimulus configuration. Another nuance in need of discussion is how awareness is assessed within a relative blindsight paradigm. Researchers can compare conditions in which stimuli are more or less often rated as unconscious (as has been done before using subjective “guessing” rates as an measure of percent “seen”; Lau and Passingham, 2006), or they can induce a relative reduction in visibility ratings using some scale, though the stimuli may always, in some sense, be conscious. Likely both approaches are appropriate and can address different issues. The former procedure may be better suited to detect cognitive functions that fully depend on conscious processing, while the latter procedure may only show that consciousness has some influence on the cognitive process under investigation. The latter procedure may be more sensitive, however, in that it does not require degrading stimuli to the point where they are sometimes rated as unconscious, which could optimize the probability of the “less visible” stimulus engaging other downstream cognitive functions. Lastly, the choice of measurement for both subjective and objective processing deserves careful consideration. The extent to which both measures are maximally sensitive, for example, could alter experimental results. Popular scales of subjective awareness are often pseudo-continuous (e.g., PAS; Overgaard et al., 2006), yet discrimination performance is often binary (e.g., 2AFC). If some parameter of behavioral performance did in fact vary with awareness but was not captured by the objective measure, relative blindsight would not have been truly established. By having participants reproduce the exact angle of a target Gabor patch, for example, one could compare a continuous parameter of perceptual performance (distance from the correct angle) under levels of continuously varying subjective visibility. As work with this novel paradigm continues to develop, the relative blindsight approach is best seen as a flexible tool that can complement existing methods of investigating the role that consciousness has in behavior while ruling out certain performance confounds and insensitivity due to extreme stimulus degradation.

Frequency modulation of neural oscillations according to visual task demands

Significance Neural oscillations are hypothesized to play an important role in modulating perceptual processing in accordance with top-down goals. For instance, the amplitude, phase, and spatial distribution of alpha-band oscillations change with attention. Given recent links between the peak frequency of alpha oscillations and the temporal resolution of perception, we investigated whether frequency modulation occurs when task demands emphasize integration or segregation of visual input over time. We found that alpha frequency in occipital–temporal cortex decreased during, and in anticipation of, stimulus processing when task demands required temporal integration compared with segregation. These results demonstrate a unique top-down mechanism by which the brain controls the temporal resolution of visual processing in accordance with current 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.

Inhibition of Lateral Prefrontal Cortex Produces Emotionally Biased First Impressions: A Transcranial Magnetic Stimulation and Electroencephalography Study

Optimal functioning in everyday life requires the ability to override reflexive emotional responses and prevent affective spillover to situations or people unrelated to the source of emotion. In the current study, we investigated whether the lateral prefrontal cortex (lPFC) causally regulates the influence of emotional information on subsequent judgments. We disrupted left lPFC function using transcranial magnetic stimulation (TMS) and recorded electroencephalography (EEG) before and after. Subjects evaluated the likeability of novel neutral faces after a brief exposure to a happy or fearful face. We found that lPFC inhibition biased evaluations of novel faces according to the previously processed emotional expression. Greater frontal EEG alpha power, reflecting increased inhibition by TMS, predicted increased behavioral bias. TMS-induced affective misattribution was long-lasting: Emotionally biased first impressions formed during lPFC inhibition were still detectable outside of the laboratory 3 days later. These findings indicate that lPFC serves an important emotion-regulation function by preventing incidental emotional encoding from automatically biasing subsequent appraisals.

Dissociating Perceptual Confidence from Discrimination Accuracy Reveals No Influence of Metacognitive Awareness on Working Memory

Visual awareness is hypothesized to be intimately related to visual working memory (WM), such that information present in WM is thought to have necessarily been represented consciously. Recent work has challenged this longstanding view by demonstrating that visual stimuli rated by observers as unseen can nevertheless be maintained over a delay period. These experiments have been criticized, however, on the basis that subjective awareness ratings may contain response bias (e.g., an observer may report no awareness when in fact they had partial awareness). We mitigated this issue by investigating WM for visual stimuli that were matched for perceptual discrimination capacity (d′), yet which varied in subjective confidence ratings (so-called relative blindsight). If the degree of initial subjective awareness of a stimulus facilitates later maintenance of that information, WM performance should improve for stimuli encoded with higher confidence. In contrast, we found that WM performance did not benefit from higher visual discrimination confidence. This relationship was observed regardless of WM load (1 or 3). Insofar as metacognitive ratings (e.g., confidence, visibility) reflect visual awareness, these results challenge a strong relationship between conscious perception and WM using a paradigm that controls for discrimination accuracy and is less subject to response bias (since confidence is manipulated within subjects). Methodologically, we replicate prior efforts to induce relative blindsight using similar stimulus displays, providing a general framework for isolating metacognitive awareness in order to examine the function of consciousness.