The Influence of Prestimulus 1/f-Like versus Alpha-Band Activity on Subjective Awareness of Auditory and Visual Stimuli.

Alpha rhythmic activity is often suggested to exert an inhibitory influence on information processing. However, relatively little is known about how reported alpha-related effects are influenced by a potential confounding element of the neural signal, power-law scaling. In the current study, we systematically examine the effect of accounting for 1/f activity on the relation between prestimulus alpha power and human behavior during both auditory and visual detection (N = 27; 19 female, 6 male, 2 nonbinary). The results suggest that, at least in the scalp-recorded EEG signal, the difference in alpha power often reported before visual hits versus misses is probably best thought of as a combination of narrowband alpha and broadband shifts. That is, changes in broadband parameters (exponent and offset of 1/f-like activity) also appear to be strong predictors of the subsequent awareness of visual stimuli. Neither changes in posterior alpha power nor changes in 1/f-like activity reliably predicted detection of auditory stimuli. These results appear consistent with suggestions that broadband changes in the scalp-recorded EEG signal may account for a portion of prior results linking alpha band dynamics to visuospatial attention and behavior, and suggest that systematic re-examination of existing data may be warranted.Significance Statement Fluctuations in alpha band (∼8-12 Hz) activity systematically follow the allocation of attention across space and sensory modality. Increases in alpha amplitude, which often precede failures to report awareness of threshold visual stimuli, are suggested to exert an inhibitory influence on information processing. However, fluctuations in alpha activity are often confounded with changes in the broadband 1/f-like pattern of the neural signal. When both factors are considered, we find that changes in broadband activity are as effective as narrowband alpha activity as predictors of subsequent visual detection. These results are consistent with emerging understanding of the potential functional importance of broadband changes in the neural signal and may have significant consequences for our understanding of alpha rhythmic activity.

The Brain's Sensitivity to Real-world Statistical Regularity Does Not Require Full Attention.

Predictive coding accounts of perception state that the brain generates perceptual predictions in the service of processing incoming sensory data. These predictions are hypothesized to be afforded by the brain's ability to internalize useful patterns, that is, statistical regularities, from the environment. We have previously argued that the N300 ERP component serves as an index of the brain's use of representations of (real-world) statistical regularities. However, we do not yet know whether overt attention is necessary in order for this process to engage. We addressed this question by presenting stimuli of either high or low real-world statistical regularity in terms of their representativeness (good/bad exemplars of natural scene categories) to participants who either fully attended the stimuli or were distracted by another task (attended/distracted conditions). Replicating past work, N300 responses were larger to bad than to good scene exemplars, and furthermore, we demonstrate minimal impacts of distraction on N300 effects. Thus, it seems that overtly focused attention is not required to maintain the brain's sensitivity to real-world statistical regularity. Furthermore, in an exploratory analysis, we showed that providing additional, artificial regularities, formed by altering the proportions of good and bad exemplars within blocks, further enhanced the N300 effect in both attended and distracted conditions, shedding light on the relationship between statistical regularities learned in the real world and those learned within the context of an experiment.

Is attention necessary for the representational advantage of good exemplars over bad exemplars?

Real-world (rw-) statistical regularities, or expectations about the visual world learned over a lifetime, have been found to be associated with scene perception efficiency. For example, good (i.e., highly representative) exemplars of basic scene categories, one example of an rw-statistical regularity, are detected more readily than bad exemplars of the category. Similarly, good exemplars achieve higher multivariate pattern analysis (MVPA) classification accuracy than bad exemplars in scene-responsive regions of interest, particularly in the parahippocampal place area (PPA). However, it is unclear whether the good exemplar advantages observed depend on or are even confounded by selective attention. Here, we ask whether the observed neural advantage of the good scene exemplars requires full attention. We used a dual-task paradigm to manipulate attention and exemplar representativeness while recording neural responses with functional magnetic resonance imaging (fMRI). Both univariate analysis and MVPA were adopted to examine the effect of representativeness. In the attend-to-scenes condition, our results replicated an earlier study showing that good exemplars evoke less activity but a clearer category representation than bad exemplars. Importantly, similar advantages of the good exemplars were also observed when participants were distracted by a serial visual search task demanding a high attention load. In addition, cross-decoding between attended and distracted representations revealed that attention resulted in a quantitative (increased activation) rather than qualitative (altered activity patterns) improvement of the category representation, particularly for good exemplars. We, therefore, conclude that the effect of category representativeness on neural representations does not require full attention.

Effects of task type on spontaneous alternations of attentional states.

Mind wandering is a common occurrence that can have serious consequences, but estimating when mind wandering occurs is a challenging research question. Previous research has shown that during meditation, people may spontaneously alternate between task-oriented and mind-wandering states without awareness (Zukosky & Wang, 2021, Cognition, 212, Article 104689). However, under what conditions such alternations occur is not clear. The present study examined the effects of task type on spontaneous alternations between task focus and mind wandering. In addition to a meditation task, participants performed either a scene-categorization-based CPT or a visual detection task while attentional orientation was assessed via self-monitoring and intermittent probes. The three tasks differ in the extent of their reliance on continuous monitoring (less required in the detection than meditation and CPT tasks) and attentional orientation (oriented internally in meditation task and externally in CPT and detection tasks). To overcome prior methodological challenges, we applied a technique designed to detect spontaneous alternations between focused and mind-wandering states without awareness, based on how the proportion of "focused" responses/ratings to intermittent probes changes during a focus-to-mind-wandering interval (i.e., the period from one self-report of mind wandering to the subsequent self-report). Our results showed that the proportion of "focused" responses to intermittent probes remained constant with increasing interprobe interval during meditation (consistent with previous work), but declined significantly in the CPT and detection tasks. These findings support the hypothesis that spontaneous alternations of attentional states without self-awareness occur during tasks emphasizing internally but not externally oriented attention.

Dynamics of alpha suppression index both modality specific and general attention processes.

EEG alpha power varies under many circumstances requiring visual attention. However, mounting evidence indicates that alpha may not only serve visual processing, but also the processing of stimuli presented in other sensory modalities, including hearing. We previously showed that alpha dynamics during an auditory task vary as a function of competition from the visual modality (Clements et al., 2022) suggesting that alpha may be engaged in multimodal processing. Here we assessed the impact of allocating attention to the visual or auditory modality on alpha dynamics at parietal and occipital electrodes, during the preparatory period of a cued-conflict task. In this task, bimodal precues indicated the modality (vision, hearing) relevant to a subsequent reaction stimulus, allowing us to assess alpha during modality-specific preparation and while switching between modalities. Alpha suppression following the precue occurred in all conditions, indicating that it may reflect general preparatory mechanisms. However, we observed a switch effect when preparing to attend to the auditory modality, in which greater alpha suppression was elicited when switching to the auditory modality compared to repeating. No switch effect was evident when preparing to attend to visual information (although robust suppression did occur in both conditions). In addition, waning alpha suppression preceded error trials, irrespective of sensory modality. These findings indicate that alpha can be used to monitor the level of preparatory attention to process both visual and auditory information, and support the emerging view that alpha band activity may index a general attention control mechanism used across modalities.

Dynamics of alpha suppression and enhancement may be related to resource competition in cross-modal cortical regions.

In the face of multiple sensory streams, there may be competition for processing resources in multimodal cortical areas devoted to establishing representations. In such cases, alpha oscillations may serve to maintain the relevant representations and protect them from interference, whereas theta band activity may facilitate their updating when needed. It can be hypothesized that these oscillations would differ in response to an auditory stimulus when the eyes are open or closed, as intermodal resource competition may be more prominent in the former than in the latter case. Across two studies we investigated the role of alpha and theta power in multimodal competition using an auditory task with the eyes open and closed, respectively enabling and disabling visual processing in parallel with the incoming auditory stream. In a passive listening task (Study 1a), we found alpha suppression following a pip tone with both eyes open and closed, but subsequent alpha enhancement only with closed eyes. We replicated this eyes-closed alpha enhancement in an independent sample (Study 1b). In an active auditory oddball task (Study 2), we again observed the eyes open/eyes closed alpha pattern found in Study 1 and also demonstrated that the more attentionally demanding oddball trials elicited the largest oscillatory effects. Theta power did not interact with eye status in either study. We propose a hypothesis to account for the findings in which alpha may be endemic to multimodal cortical areas in addition to visual ones.

Typical viewpoints of objects are better detected than atypical ones.

Previous work has claimed that canonical viewpoints of objects are more readily perceived than noncanonical viewpoints. However, all of these studies required participants to identify the object, a late perceptual process at best and arguably a cognitive process (Pylyshyn, 1999). Here, we extend this work to early vision by removing the explicit need to identify the objects. In particular, we asked participants to make an intact/scrambled discrimination of briefly presented objects that were viewed from either typical or atypical viewpoints. Notably, participants did not have to identify the object; only discriminate it from noise (scrambled). Participants were more sensitive in discriminating objects presented in typically encountered orientations than when objects were presented in atypical depth rotations (Experiment 1). However, the same effect for objects presented in atypical picture plane rotations (as opposed to typical ones) did not reach statistical significance (Experiments 2 and 3), suggesting that particular informative views may play a critical role in this effect. We interpret this enhanced perceptibility, for both these items and good exemplars and probable scenes, as deriving from their high real-world statistical regularity.

Separation of item and context in item-method directed forgetting.

Contextual information plays a critical role in directed forgetting (DF) of lists of items, whereas DF of individual items has been primarily associated with item-level processing. This study was designed to investigate whether context processing also contributes to the forgetting of individual items. Participants first viewed a series of words, with task-irrelevant scene images (used as "context tags") interspersed between them. Later, these words reappeared without the scenes and were followed by an instruction to remember or forget that word. Multivariate pattern analyses of fMRI data revealed that the reactivation of context information associated with the studied words (i.e., scene-related activity) was greater whereas the item-related information diminished after a forget instruction compared to a remember instruction. Critically, we found the magnitude of the separation between item information and context information predicted successful forgetting. These results suggest that the unbinding of an item from its context may support the intention to forget, and more generally they establish that contextual processing indeed contributes to item-method DF.

Examining the role of feedback in TMS-induced visual suppression: A cautionary tale.

Visual suppression by single-pulse transcranial magnetic stimulation (sTMS) has been attributed to interruptions of either feedforward or feedback activity in the visual stream. The relative timing of the C1 event related potential (ERP) and of the TMS suppression, taken from separate studies, supports an interruption of feedback. Here we probe the validity of such cross-study comparisons, both by conducting a literature survey and by measuring each time window within participants for the same stimuli. Cortical transmission time was estimated using the C1. We then suppressed the same stimuli that elicited the C1 using sTMS of variable post-stimulus lags. Results do not conclusively discriminate between interruption of feedback or feedforward mechanisms as the source of the visual suppression. We suggest that more evidence is needed to distinguish between feedback and feedforward interference in TMS suppression effects and we advise caution in making inferences derived from separate literatures, using different stimuli.

Human-Object Interactions Are More than the Sum of Their Parts.

Understanding human-object interactions is critical for extracting meaning from everyday visual scenes and requires integrating complex relationships between human pose and object identity into a new percept. To understand how the brain builds these representations, we conducted 2 fMRI experiments in which subjects viewed humans interacting with objects, noninteracting human-object pairs, and isolated humans and objects. A number of visual regions process features of human-object interactions, including object identity information in the lateral occipital complex (LOC) and parahippocampal place area (PPA), and human pose information in the extrastriate body area (EBA) and posterior superior temporal sulcus (pSTS). Representations of human-object interactions in some regions, such as the posterior PPA (retinotopic maps PHC1 and PHC2) are well predicted by a simple linear combination of the response to object and pose information. Other regions, however, especially pSTS, exhibit representations for human-object interaction categories that are not predicted by their individual components, indicating that they encode human-object interactions as more than the sum of their parts. These results reveal the distributed networks underlying the emergent representation of human-object interactions necessary for social perception.

Regulating the Access to Awareness: Brain Activity Related to Probe-related and Spontaneous Reversals in Binocular Rivalry.

Research on the neural correlates of consciousness (NCC) has implicated an assortment of brain regions, ERP components, and network properties associated with visual awareness. Recently, the P3b ERP component has emerged as a leading NCC candidate. However, typical P3b paradigms depend on the detection of some stimulus change, making it difficult to separate brain processes elicited by the stimulus itself from those associated with updates or changes in visual awareness. Here we used binocular rivalry to ask whether the P3b is associated with changes in awareness even in the absence of changes in the object of awareness. We recorded ERPs during a probe-mediated binocular rivalry paradigm in which brief probes were presented over the image in either the suppressed or dominant eye to determine whether the elicited P3b activity is probe or reversal related. We found that the timing of P3b (but not its amplitude) was closely related to the timing of the report of a perceptual change rather than to the onset of the probe. This is consistent with the proposal that P3b indexes updates in conscious awareness, rather than being related to stimulus processing per se. Conversely, the probe-related P1 amplitude (but not its latency) was associated with reversal latency, suggesting that the degree to which the probe is processed increases the likelihood of a fast perceptual reversal. Finally, the response-locked P3b amplitude (but not its latency) was associated with the duration of an intermediate stage between reversals in which parts of both percepts coexist (piecemeal period). Together, the data suggest that the P3b reflects an update in consciousness and that the intensity of that process (as indexed by P3b amplitude) predicts how immediate that update is.

Evidence for similar patterns of neural activity elicited by picture- and word-based representations of natural scenes.

A long-standing core question in cognitive science is whether different modalities and representation types (pictures, words, sounds, etc.) access a common store of semantic information. Although different input types have been shown to activate a shared network of brain regions, this does not necessitate that there is a common representation, as the neurons in these regions could still differentially process the different modalities. However, multi-voxel pattern analysis can be used to assess whether, e.g., pictures and words evoke a similar pattern of activity, such that the patterns that separate categories in one modality transfer to the other. Prior work using this method has found support for a common code, but has two limitations: they have either only examined disparate categories (e.g. animals vs. tools) that are known to activate different brain regions, raising the possibility that the pattern separation and inferred similarity reflects only large scale differences between the categories or they have been limited to individual object representations. By using natural scene categories, we not only extend the current literature on cross-modal representations beyond objects, but also, because natural scene categories activate a common set of brain regions, we identify a more fine-grained (i.e. higher spatial resolution) common representation. Specifically, we studied picture- and word-based representations of natural scene stimuli from four different categories: beaches, cities, highways, and mountains. Participants passively viewed blocks of either phrases (e.g. "sandy beach") describing scenes or photographs from those same scene categories. To determine whether the phrases and pictures evoke a common code, we asked whether a classifier trained on one stimulus type (e.g. phrase stimuli) would transfer (i.e. cross-decode) to the other stimulus type (e.g. picture stimuli). The analysis revealed cross-decoding in the occipitotemporal, posterior parietal and frontal cortices. This similarity of neural activity patterns across the two input types, for categories that co-activate local brain regions, provides strong evidence of a common semantic code for pictures and words in the brain.

Categorization influences detection: A perceptual advantage for representative exemplars of natural scene categories.

Traditional models of recognition and categorization proceed from registering low-level features, perceptually organizing that input, and linking it with stored representations. Recent evidence, however, suggests that this serial model may not be accurate, with object and category knowledge affecting rather than following early visual processing. Here, we show that the degree to which an image exemplifies its category influences how easily it is detected. Participants performed a two-alternative forced-choice task in which they indicated whether a briefly presented image was an intact or phase-scrambled scene photograph. Critically, the category of the scene is irrelevant to the detection task. We nonetheless found that participants "see" good images better, more accurately discriminating them from phase-scrambled images than bad scenes, and this advantage is apparent regardless of whether participants are asked to consider category during the experiment or not. We then demonstrate that good exemplars are more similar to same-category images than bad exemplars, influencing behavior in two ways: First, prototypical images are easier to detect, and second, intact good scenes are more likely than bad to have been primed by a previous trial.

Typicality sharpens category representations in object-selective cortex.

The purpose of categorization is to identify generalizable classes of objects whose members can be treated equivalently. Within a category, however, some exemplars are more representative of that concept than others. Despite long-standing behavioral effects, little is known about how typicality influences the neural representation of real-world objects from the same category. Using fMRI, we showed participants 64 subordinate object categories (exemplars) grouped into 8 basic categories. Typicality for each exemplar was assessed behaviorally and we used several multi-voxel pattern analyses to characterize how typicality affects the pattern of responses elicited in early visual and object-selective areas: V1, V2, V3v, hV4, LOC. We found that in LOC, but not in early areas, typical exemplars elicited activity more similar to the central category tendency and created sharper category boundaries than less typical exemplars, suggesting that typicality enhances within-category similarity and between-category dissimilarity. Additionally, we uncovered a brain region (cIPL) where category boundaries favor less typical categories. Our results suggest that typicality may constitute a previously unexplored principle of organization for intra-category neural structure and, furthermore, that this representation is not directly reflected in image features describing natural input, but rather built by the visual system at an intermediate processing stage.

Pinpointing the peripheral bias in neural scene-processing networks during natural viewing.

Peripherally presented stimuli evoke stronger activity in scene-processing regions than foveally presented stimuli, suggesting that scene understanding is driven largely by peripheral information. We used functional MRI to investigate whether functional connectivity evoked during natural perception of audiovisual movies reflects this peripheral bias. For each scene-sensitive region--the parahippocampal place area (PPA), retrosplenial cortex, and occipital place area--we computed two measures: the extent to which its activity could be predicted by V1 activity (connectivity strength) and the eccentricities within V1 to which it was most closely related (connectivity profile). Scene regions were most related to peripheral voxels in V1, but the detailed nature of this connectivity varied within and between these regions. The retrosplenial cortex showed the most consistent peripheral bias but was less predictable from V1 activity, while the occipital place area was related to a wider range of eccentricities and was strongly coupled to V1. We divided the PPA along its posterior-anterior axis into retinotopic maps PHC1, PHC2, and anterior PPA, and found that a peripheral bias was detectable throughout all subregions, though the anterior PPA showed a less consistent relationship to eccentricity and a substantially weaker overall relationship to V1. We also observed an opposite foveal bias in object-perception regions including the lateral occipital complex and fusiform face area. These results show a fine-scale relationship between eccentricity biases and functional correlation during natural perception, giving new insight into the structure of the scene-perception network.

The folly of boxology.

Although the authors do a valuable service by elucidating the pitfalls of inferring top-down effects, they overreach by claiming that vision is cognitively impenetrable. Their argument, and the entire question of cognitive penetrability, seems rooted in a discrete, stage-like model of the mind that is unsupported by neural data.

Basic level category structure emerges gradually across human ventral visual cortex.

Objects can be simultaneously categorized at multiple levels of specificity ranging from very broad ("natural object") to very distinct ("Mr. Woof"), with a mid-level of generality (basic level: "dog") often providing the most cognitively useful distinction between categories. It is unknown, however, how this hierarchical representation is achieved in the brain. Using multivoxel pattern analyses, we examined how well each taxonomic level (superordinate, basic, and subordinate) of real-world object categories is represented across occipitotemporal cortex. We found that, although in early visual cortex objects are best represented at the subordinate level (an effect mostly driven by low-level feature overlap between objects in the same category), this advantage diminishes compared to the basic level as we move up the visual hierarchy, disappearing in object-selective regions of occipitotemporal cortex. This pattern stems from a combined increase in within-category similarity (category cohesion) and between-category dissimilarity (category distinctiveness) of neural activity patterns at the basic level, relative to both subordinate and superordinate levels, suggesting that successive visual areas may be optimizing basic level representations.

Trial history effects in the ventral attentional network.

The ventral attentional network (VAN) is thought to drive "stimulus driven attention" [e.g., Asplund, C. L., Todd, J. J., Snyder, A. P., & Marois, R. A central role for the lateral prefrontal cortex in goal-directed and stimulus-driven attention. Nature Neuroscience, 13, 507-512, 2010; Shulman, G. L., McAvoy, M. P., Cowan, M. C., Astafiev, S. V., Tansy, A. P., D' Avossa, G., et al. Quantitative analysis of attention and detection signals during visual search. Journal of Neurophysiology, 90, 3384-3397, 2003]; in other words, it instantiates within the current stimulus environment the top-down attentional biases maintained by the dorsal attention network [e.g., Kincade, J. M., Abrams, R. A., Astafiev, S. V., Shulman, G. L., & Corbetta, M. An event-related functional magnetic resonance imaging study of voluntary and stimulus-driven orienting of attention. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 25, 4593-4604, 2005]. Previous work has shown that the dorsal attentional network is sensitive to trial history, such that it is challenged by changes in task goals and facilitated by repetition thereof [e.g., Kristjánsson, A., Vuilleumier, P., Schwartz, S., Macaluso, E., & Driver, J. Neural basis for priming of pop-out during visual search revealed with fMRI. Cerebral Cortex, 17, 1612-1624, 2007]. Here, we investigate whether the VAN also preserves information across trials such that it is challenged when previously rejected stimuli become task relevant. We used fMRI to investigate the sensitivity of the ventral attentional system to prior history effects as measured by the distractor preview effect. This behavioral phenomenon reflects a bias against stimuli that have historically not supported task performance. We found regions traditionally considered to be part of the VAN (right middle frontal gyrus, inferior frontal gyrus and right supramarginal gyrus) [Shulman, G. L., McAvoy, M. P., Cowan, M. C., Astafiev, S. V., Tansy, A. P., D' Avossa, G., et al. Quantitative analysis of attention and detection signals during visual search. Journal of Neurophysiology, 90, 3384-3397, 2003] to be more active when task-relevant stimuli had not supported task performance in a previous trial than when they had. Investigations of the ventral visual system suggest that this effect is more reliably driven by trial history preserved within the VAN than that preserved within the visual system per se. We conclude that VAN maintains its interactions with top-down stimulus biases and bottom-up stimulation across time, allowing previous experience with the stimulus environment to influence attentional biases under current circumstances.

Dynamics of alpha control: preparatory suppression of posterior alpha oscillations by frontal modulators revealed with combined EEG and event-related optical signal.

We investigated the dynamics of brain processes facilitating conscious experience of external stimuli. Previously, we proposed that alpha (8-12 Hz) oscillations, which fluctuate with both sustained and directed attention, represent a pulsed inhibition of ongoing sensory brain activity. Here we tested the prediction that inhibitory alpha oscillations in visual cortex are modulated by top-down signals from frontoparietal attention networks. We measured modulations in phase-coherent alpha oscillations from superficial frontal, parietal, and occipital cortices using the event-related optical signal (EROS), a measure of neuronal activity affording high spatiotemporal resolution, along with concurrently recorded EEG, while participants performed a visual target detection task. The pretarget alpha oscillations measured with EEG and EROS from posterior areas were larger for subsequently undetected targets, supporting alpha's inhibitory role. Using EROS, we localized brain correlates of these awareness-related alpha oscillations measured at the scalp to the cuneus and precuneus. Crucially, EROS alpha suppression correlated with posterior EEG alpha power across participants. Sorting the EROS data based on EEG alpha power quartiles to investigate alpha modulators revealed that suppression of posterior alpha was preceded by increased activity in regions of the dorsal attention network and decreased activity in regions of the cingulo-opercular network. Cross-correlations revealed the temporal dynamics of activity within these preparatory networks before posterior alpha modulation. The novel combination of EEG and EROS afforded localization of the sources and correlates of alpha oscillations and their temporal relationships, supporting our proposal that top-down control from attention networks modulates both posterior alpha and awareness of visual stimuli.

Phosphene-guided transcranial magnetic stimulation of occipital but not parietal cortex suppresses stimulus visibility.

Transcranial magnetic stimulation (TMS) applied over the occipital lobe approximately 100 ms after the onset of a stimulus decreases its visibility if it appears in the location of the phosphene. Because phosphenes can also be elicited by stimulation of the parietal regions, we asked if the same procedure that is used to reduce visibility of stimuli with occipital TMS will lead to decreased stimulus visibility when TMS is applied to parietal regions. TMS was randomly applied at 0-130 ms after the onset of the stimulus in steps of 10 ms in occipital and parietal regions. Participants responded to the orientation of the line stimulus and rated its visibility. We replicate previous reports of phosphenes from both occipital and parietal TMS. As previously reported, we also observed visual suppression around the classical 100 ms window both in the objective line orientation and subjective visibility responses with occipital TMS. Parietal stimulation, on the other hand, did not consistently reduce stimulus visibility in any time window.