The scope and limits of top-down attention in unconscious visual processing

Attentional selection plays a critical role in conscious perception. When attention is diverted, even salient stimuli fail to reach visual awareness. Attention can be voluntarily directed to a spatial location or a visual feature for facilitating the processing of information relevant to current goals. In everyday situations, attention and awareness are tightly coupled. This has led some to suggest that attention and awareness might be based on a common neural foundation, whereas others argue that they are mediated by distinct mechanisms. A body of evidence shows that visual stimuli can be processed at multiple stages of the visual-processing streams without evoking visual awareness. To illuminate the relationship between visual attention and conscious perception, we investigated whether top-down attention can target and modulate the neural representations of unconsciously processed visual stimuli. Our experiments show that spatial attention can target only consciously perceived stimuli, whereas feature-based attention can modulate the processing of invisible stimuli. The attentional modulation of unconscious signals implies that attention and awareness can be dissociated, challenging a simplistic view of the boundary between conscious and unconscious visual processing.     

Visual saliency and spike timing in the ventral visual pathway.

Visual saliency is a fundamental yet hard to define property of objects or locations in the visual world. In a context where objects and their representations compete to dominate our perception, saliency can be thought of as the "juice" that makes objects win the race. It is often assumed that saliency is extracted and represented in an explicit saliency map, which serves to determine the location of spatial attention at any given time. It is then by drawing attention to a salient object that it can be recognized or categorized. I argue against this classical view that visual "bottom-up" saliency automatically recruits the attentional system prior to object recognition. A number of visual processing tasks are clearly performed too fast for such a costly strategy to be employed. Rather, visual attention could simply act by biasing a saliency-based object recognition system. Under natural conditions of stimulation, saliency can be represented implicitly throughout the ventral visual pathway, independent of any explicit saliency map. At any given level, the most activated cells of the neural population simply represent the most salient locations. The notion of saliency itself grows increasingly complex throughout the system, mostly based on luminance contrast until information reaches visual cortex, gradually incorporating information about features such as orientation or color in primary visual cortex and early extrastriate areas, and finally the identity and behavioral relevance of objects in temporal cortex and beyond. Under these conditions the object that dominates perception, i.e. the object yielding the strongest (or the first) selective neural response, is by definition the one whose features are most "salient"--without the need for any external saliency map. In addition, I suggest that such an implicit representation of saliency can be best encoded in the relative times of the first spikes fired in a given neuronal population. In accordance with our subjective experience that saliency and attention do not modify the appearance of objects, the feed-forward propagation of this first spike wave could serve to trigger saliency-based object recognition outside the realm of awareness, while conscious perceptions could be mediated by the remaining discharges of longer neuronal spike trains.     

Avoidance of obstacles in the absence of visual awareness

The spatial character of our reaching movements is extremely sensitive to potential obstacles in the workspace. We recently found that this sensitivity was retained by most patients with left visual neglect when reaching between two objects, despite the fact that they tended to ignore the leftward object when asked to bisect the space between them. This raises the possibility that obstacle avoidance does not require a conscious awareness of the obstacle avoided. We have now tested this hypothesis in a patient with visual extinction following right temporoparietal damage. Extinction is an attentional disorder in which patients fail to report stimuli on the side of space opposite a brain lesion under conditions of bilateral stimulation. Our patient avoided obstacles during reaching, to exactly the same degree, regardless of whether he was able to report their presence. This implicit processing of object location, which may depend on spared superior parietal-lobe pathways, demonstrates that conscious awareness is not necessary for normal obstacle avoidance.     

Unconscious Local Motion Alters Global Image Speed

Accurate motion perception of self and object speed is crucial for successful interaction in the world. The context in which we make such speed judgments has a profound effect on their accuracy. Misperceptions of motion speed caused by the context can have drastic consequences in real world situations, but they also reveal much about the underlying mechanisms of motion perception. Here we show that motion signals suppressed from awareness can warp simultaneous conscious speed perception. In Experiment 1, we measured global speed discrimination thresholds using an annulus of 8 local Gabor elements. We show that physically removing local elements from the array attenuated global speed discrimination. However, removing awareness of the local elements only had a small effect on speed discrimination. That is, unconscious local motion elements contributed to global conscious speed perception. In Experiment 2 we measured the global speed of the moving Gabor patterns, when half the elements moved at different speeds. We show that global speed averaging occurred regardless of whether local elements were removed from awareness, such that the speed of invisible elements continued to be averaged together with the visible elements to determine the global speed. These data suggest that contextual motion signals outside of awareness can both boost and affect our experience of motion speed, and suggest that such pooling of motion signals occurs before the conscious extraction of the surround motion speed.     

Spatial attention changes excitability of human visual cortex to direct stimulation

Conscious perception depends not only on sensory input, but also on attention [1, 2]. Recent studies in monkeys [3-6] and humans [7-12] suggest that influences of spatial attention on visual awareness may reflect top-down influences on excitability of visual cortex. Here we tested this specifically, by providing direct input into human visual cortex via cortical transcranial magnetic stimulation (TMS) to produce illusory visual percepts, called phosphenes. We found that a lower TMS intensity was needed to elicit a conscious phosphene when its apparent spatial location was attended, rather than unattended. Our results indicate that spatial attention can enhance visual-cortex excitability, and visual awareness, even when sensory signals from the eye via the thalamic pathway are bypassed.     

Enhanced cortical excitability in grapheme-color synesthesia and its modulation

Synesthesia is an unusual condition characterized by the over-binding of two or more features and the concomitant automatic and conscious experience of atypical, ancillary images or perceptions. Previous research suggests that synesthetes display enhanced modality-specific perceptual processing, but it remains unclear whether enhanced processing contributes to conscious awareness of color photisms. In three experiments, we investigated whether grapheme-color synesthesia is characterized by enhanced cortical excitability in primary visual cortex and the role played by this hyperexcitability in the expression of synesthesia. Using transcranial magnetic stimulation, we show that synesthetes display 3-fold lower phosphene thresholds than controls during stimulation of the primary visual cortex. We next used transcranial direct current stimulation to discriminate between two competing hypotheses of the role of hyperexcitability in the expression of synesthesia. We demonstrate that synesthesia can be selectively augmented with cathodal stimulation and attenuated with anodal stimulation of primary visual cortex. A control task revealed that the effect of the brain stimulation was specific to the experience of synesthesia. These results indicate that hyperexcitability acts as a source of noise in visual cortex that influences the availability of the neuronal signals underlying conscious awareness of synesthetic photisms.     

Crowding by invisible flankers

Background

Human object recognition degrades sharply as the target object moves from central vision into peripheral vision. In particular, one''s ability to recognize a peripheral target is severely impaired by the presence of flanking objects, a phenomenon known as visual crowding. Recent studies on how visual awareness of flanker existence influences crowding had shown mixed results. More importantly, it is not known whether conscious awareness of the existence of both the target and flankers are necessary for crowding to occur.

Methodology/Principal Findings

Here we show that crowding persists even when people are completely unaware of the flankers, which are rendered invisible through the continuous flash suppression technique. Contrast threshold for identifying the orientation of a grating pattern was elevated in the flanked condition, even when the subjects reported that they were unaware of the perceptually suppressed flankers. Moreover, we find that orientation-specific adaptation is attenuated by flankers even when both the target and flankers are invisible.

Conclusions

These findings complement the suggested correlation between crowding and visual awareness. What''s more, our results demonstrate that conscious awareness and attention are not prerequisite for crowding.     

The graded and dichotomous nature of visual awareness

Is our visual experience of the world graded or dichotomous? Opposite pre-theoretical intuitions apply in different cases. For instance, when looking at a scene, one has a distinct sense that our experience has a graded character: one cannot say that there is no experience of contents that fall outside the focus of attention, but one cannot say that there is full awareness of such contents either. By contrast, when performing a visual detection task, our sense of having perceived the stimulus or not exhibits a more dichotomous character. Such issues have recently been the object of intense debate because different theoretical frameworks make different predictions about the graded versus dichotomous character of consciousness. Here, we review both relevant empirical findings as well as the associated theories (i.e. local recurrent processing versus global neural workspace theory). Next, we attempt to reconcile such contradictory theories by suggesting that level of processing is an often-ignored but highly relevant dimension through which we can cast a novel look at existing empirical findings. Thus, using a range of different stimuli, tasks and subjective scales, we show that processing low-level, non-semantic content results in graded visual experience, whereas processing high-level semantic content is experienced in a more dichotomous manner. We close by comparing our perspective with existing proposals, focusing in particular on the partial awareness hypothesis.     

Does consciousness overflow cognitive access? Novel insights from the new phenomenon of attribute amnesia

The moment we open our eyes, we experience a rich and detailed visual world, but the amount of information available to report is rather limited. This dissociation relates to a major debate regarding the nature of visual consciousness. The overflow argument suggests that our conscious experience is quite rich and far beyond what can be reported, standing in sharp contrast to the nooverflow argument that visual consciousness is severely impoverished and limited to what can be reported. In this paper, we systematically reviewed existing evidence in favor of the overflow argument, including studies of several variations of the iconic memory paradigm and the divided attention paradigm, as well as studies of neural correlates of consciousness. Simultaneously,we expounded some critical objections and alternative interpretations to such evidence, as well as some opposing evidence.Finally, we introduced a series of our recent studies based on a striking phenomenon of attribute amnesia, which we believe could provide new insight into the overflow view of visual consciousness.     

The neural fate of consciously perceived and missed events in the attentional blink

Cognitive models of attention propose that visual perception is a product of two stages of visual processing: early operations permit rapid initial categorization of the visual world, while later attention-demanding capacity-limited stages are necessary for the conscious report of the stimuli. Here we used the attentional blink paradigm and fMRI to neurally distinguish these two stages of vision. Subjects detected a face target and a scene target presented rapidly among distractors at fixation. Although the second, scene target frequently went undetected by the subjects, it nonetheless activated regions of the medial temporal cortex involved in high-level scene representations, the parahippocampal place area (PPA). This PPA activation was amplified when the stimulus was consciously perceived. By contrast, the frontal cortex was activated only when scenes were successfully reported. These results suggest that medial temporal cortex permits rapid categorization of the visual input, while the frontal cortex is part of a capacity-limited attentional bottleneck to conscious report.     

Conscious awareness of flicker in humans involves frontal and parietal cortex

Even when confined to the same spatial location, flickering and steady light evoke very different conscious experiences because of their distinct temporal patterns. The neural basis of such differences in subjective experience remains uncertain . Here, we used functional MRI in humans to examine the neural structures involved in awareness of flicker. Participants viewed a single point source of light that flickered at the critical flicker fusion (CFF) threshold, where the same stimulus is sometimes perceived as flickering and sometimes as steady (fused) . We were thus able to compare brain activity for conscious percepts that differed qualitatively (flickering or fused) but were evoked by identical physical stimuli. Greater brain activation was observed on flicker (versus fused) trials in regions of frontal and parietal cortex previously associated with visual awareness in tasks that did not require detection of temporal patterns . In contrast, greater activation was observed on fused (versus flicker) trials in occipital extrastriate cortex. Our findings indicate that activity of higher-level cortical areas is important for awareness of temporally distinct visual events in the context of a nonspatial task, and they thus suggest that frontal and parietal regions may play a general role in visual awareness.     

Colour Terms Affect Detection of Colour and Colour-Associated Objects Suppressed from Visual Awareness

The idea that language can affect how we see the world continues to create controversy. A potentially important study in this field has shown that when an object is suppressed from visual awareness using continuous flash suppression (a form of binocular rivalry), detection of the object is differently affected by a preceding word prime depending on whether the prime matches or does not match the object. This may suggest that language can affect early stages of vision. We replicated this paradigm and further investigated whether colour terms likewise influence the detection of colours or colour-associated object images suppressed from visual awareness by continuous flash suppression. This method presents rapidly changing visual noise to one eye while the target stimulus is presented to the other. It has been shown to delay conscious perception of a target for up to several minutes. In Experiment 1 we presented greyscale photos of objects. They were either preceded by a congruent object label, an incongruent label, or white noise. Detection sensitivity (d’) and hit rates were significantly poorer for suppressed objects preceded by an incongruent label compared to a congruent label or noise. In Experiment 2, targets were coloured discs preceded by a colour term. Detection sensitivity was significantly worse for suppressed colour patches preceded by an incongruent colour term as compared to a congruent term or white noise. In Experiment 3 targets were suppressed greyscale object images preceded by an auditory presentation of a colour term. On congruent trials the colour term matched the object’s stereotypical colour and on incongruent trials the colour term mismatched. Detection sensitivity was significantly poorer on incongruent trials than congruent trials. Overall, these findings suggest that colour terms affect awareness of coloured stimuli and colour- associated objects, and provide new evidence for language-perception interaction in the brain.     

Attention without awareness in blindsight.

The act of attending has frequently been equated with visual awareness. We examined this relationship in 'blindsight'--a condition in which the latter is absent or diminished as a result of damage to the primary visual cortex. Spatially selective visual attention is demonstrated when information that stimuli are likely to appear at a specific location enhances the speed or accuracy of detection of stimuli subsequently presented at that location. In a blindsight subject, we showed that attention can confer an advantage in processing stimuli presented at an attended location, without those stimuli entering consciousness. Attention could be directed both by symbolic cues in the subject's spared field of vision or cues presented in his blind field. Cues in his blind field were even effective in directing his attention to a second location remote from that at which the cue was presented. These indirect cues were effective whether or not they themselves elicited non-visual awareness. We concluded that the spatial selection of information by an attentional mechanism and its entry into conscious experience cannot be one and the same process.     

Attentional load modulates responses of human primary visual cortex to invisible stimuli

Visual neuroscience has long sought to determine the extent to which stimulus-evoked activity in visual cortex depends on attention and awareness. Some influential theories of consciousness maintain that the allocation of attention is restricted to conscious representations [1, 2]. However, in the load theory of attention [3], competition between task-relevant and task-irrelevant stimuli for limited-capacity attention does not depend on conscious perception of the irrelevant stimuli. The critical test is whether the level of attentional load in a relevant task would determine unconscious neural processing of invisible stimuli. Human participants were scanned with high-field fMRI while they performed a foveal task of low or high attentional load. Irrelevant, invisible monocular stimuli were simultaneously presented peripherally and were continuously suppressed by a flashing mask in the other eye [4]. Attentional load in the foveal task strongly modulated retinotopic activity evoked in primary visual cortex (V1) by the invisible stimuli. Contrary to traditional views [1, 2, 5, 6], we found that availability of attentional capacity determines neural representations related to unconscious processing of continuously suppressed stimuli in human primary visual cortex. Spillover of attention to cortical representations of invisible stimuli (under low load) cannot be a sufficient condition for their awareness.     

Neuroimaging of visual awareness in patients and normal subjects

The immediacy and directness of our visual experience belies the complexity of the underlying neural mechanisms, which remain incompletely understood. Recent neuroimaging studies suggest that activity in ventral visual cortex is necessary but not sufficient for visual awareness. Experiments in both patients and normal subjects indicate that parietal and frontal areas make an important contribution to visual awareness, suggesting that reciprocal interactions between dorsal frontoparietal areas and ventral visual cortex may provide a fundamental neural substrate for conscious visual experience.     

Primary visual cortex and visual awareness

The primary visual cortex (V1) is probably the best characterized area of primate cortex, but whether this region contributes directly to conscious visual experience is controversial. Early neurophysiological and neuroimaging studies found that visual awareness was best correlated with neural activity in extrastriate visual areas, but recent studies have found similarly powerful effects in V1. Lesion and inactivation studies have provided further evidence that V1 might be necessary for conscious perception. Whereas hierarchical models propose that damage to V1 simply disrupts the flow of information to extrastriate areas that are crucial for awareness, interactive models propose that recurrent connections between V1 and higher areas form functional circuits that support awareness. Further investigation into V1 and its interactions with higher areas might uncover fundamental aspects of the neural basis of visual awareness.     

The Temporal Dynamics of Early Visual Cortex Involvement in Behavioral Priming

Transcranial magnetic stimulation (TMS) allows for non-invasive interference with ongoing neural processing. Applied in a chronometric design over early visual cortex (EVC), TMS has proved valuable in indicating at which particular time point EVC must remain unperturbed for (conscious) vision to be established. In the current study, we set out to examine the effect of EVC TMS across a broad range of time points, both before (pre-stimulus) and after (post-stimulus) the onset of symbolic visual stimuli. Behavioral priming studies have shown that the behavioral impact of a visual stimulus can be independent from its conscious perception, suggesting two independent neural signatures. To assess whether TMS-induced suppression of visual awareness can be dissociated from behavioral priming in the temporal domain, we thus implemented three different measures of visual processing, namely performance on a standard visual discrimination task, a subjective rating of stimulus visibility, and a visual priming task. To control for non-neural TMS effects, we performed electrooculographical recordings, placebo TMS (sham), and control site TMS (vertex). Our results suggest that, when considering the appropriate control data, the temporal pattern of EVC TMS disruption on visual discrimination, subjective awareness and behavioral priming are not dissociable. Instead, TMS to EVC disrupts visual perception holistically, both when applied before and after the onset of a visual stimulus. The current findings are discussed in light of their implications on models of visual awareness and (subliminal) priming.     

The neural correlate of consciousness

I propose that we are only aware of changes in our underlying cognition. This hypothesis is based on four lines of evidence. (1) Without changes in visual input (including fixational eye movements), static images fade from awareness. (2) Consciousness appears to be continuous, but is actually broken up into discrete cycles of cognition. Without continuity, conscious awareness disintegrates into a series of isolated cycles. The simplest mechanism for creating continuity is to track the changes between the cycles. (3) While these conscious vectors are putative, they have a clear source: the dorsolateral prefrontal cortex (DLPFC). The DLPFC is active during awareness of changes, and this awareness is disrupted by repetitive transcranial magnetic stimulation. (4) When the DLPFC and the orbital and inferior parietal cortices are deactivated during dreaming, conscious awareness is absent even though the rest of the brain is active. Moreover, Lau and Passingham showed that activation of the DLPFC, but no other brain region, correlates with awareness. In summary, if the DLPFC and conscious vectors are the neural correlate of consciousness, then we are only aware of changes in our underlying cognition. The glue that holds conscious awareness together is conscious awareness.     

Exposure Is Not Enough: Suppressing Stimuli from Awareness Can Abolish the Mere Exposure Effect

Passive exposure to neutral stimuli increases subsequent liking of those stimuli – the mere exposure effect. Because of the broad implications for understanding and controlling human preferences, the role of conscious awareness in mere exposure has received much attention. Previous studies have claimed that the mere exposure effect can occur without conscious awareness of the stimuli. In two experiments, we applied a technique new to the mere exposure literature, called continuous flash suppression, to expose stimuli for a controlled duration with and without awareness. To ensure the reliability of the awareness manipulation, awareness was monitored on a trial-by-trial basis. Our results show that under these conditions the mere exposure effect does not occur without conscious awareness. In contrast, only when participants were aware of the stimuli did exposure increase liking and recognition. Together these data are consistent with the idea that the mere exposure effect requires conscious awareness and has important implications for theories of memory and affect.     

Dissociable modulation of overt visual attention in valence and arousal revealed by topology of scan path

Emotional stimuli have evolutionary significance for the survival of organisms; therefore, they are attention-grabbing and are processed preferentially. The neural underpinnings of two principle emotional dimensions in affective space, valence (degree of pleasantness) and arousal (intensity of evoked emotion), have been shown to be dissociable in the olfactory, gustatory and memory systems. However, the separable roles of valence and arousal in scene perception are poorly understood. In this study, we asked how these two emotional dimensions modulate overt visual attention. Twenty-two healthy volunteers freely viewed images from the International Affective Picture System (IAPS) that were graded for affective levels of valence and arousal (high, medium, and low). Subjects' heads were immobilized and eye movements were recorded by camera to track overt shifts of visual attention. Algebraic graph-based approaches were introduced to model scan paths as weighted undirected path graphs, generating global topology metrics that characterize the algebraic connectivity of scan paths. Our data suggest that human subjects show different scanning patterns to stimuli with different affective ratings. Valence salient stimuli (with neutral arousal) elicited faster and larger shifts of attention, while arousal salient stimuli (with neutral valence) elicited local scanning, dense attention allocation and deep processing. Furthermore, our model revealed that the modulatory effect of valence was linearly related to the valence level, whereas the relation between the modulatory effect and the level of arousal was nonlinear. Hence, visual attention seems to be modulated by mechanisms that are separate for valence and arousal.