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.     

Advantage of hole stimulus in rivalry competition

Mounting psychophysical evidence suggests that early visual computations are sensitive to the topological properties of stimuli, such as the determination of whether the object has a hole or not. Previous studies have demonstrated that the hole feature took some advantages during conscious perception. In this study, we investigate whether there exists a privileged processing for hole stimuli during unconscious perception. By applying a continuous flash suppression paradigm, the target was gradually introduced to one eye to compete against a flashed full contrast Mondrian pattern which was presented to the other eye. This method ensured that the target image was suppressed during the initial perceptual period. We compared the initial suppressed duration between the stimuli with and without the hole feature and found that hole stimuli required less time than no-hole stimuli to gain dominance against the identical suppression noise. These results suggest the hole feature could be processed in the absence of awareness, and there exists a privileged detection of hole stimuli during suppressed phase in the interocular rivalry.     

Visuospatial Sequence Learning without Seeing

Background

The ability to detect and integrate associations between unrelated items that are close in space and time is a key feature of human learning and memory. Learning sequential associations between non-adjacent visual stimuli (higher-order visuospatial dependencies) can occur either with or without awareness (explicit vs. implicit learning) of the products of learning. Existing behavioural and neurocognitive studies of explicit and implicit sequence learning, however, are based on conscious access to the sequence of target locations and, typically, on conditions where the locations for orienting, or motor, responses coincide with the locations of the target sequence.

Methodology/Principal Findings

Dichoptic stimuli were presented on a novel sequence learning task using a mirror stereoscope to mask the eye-of-origin of visual input from conscious awareness. We demonstrate that conscious access to the sequence of target locations and responses that coincide with structure of the target sequence are dispensable features when learning higher-order visuospatial associations. Sequence knowledge was expressed in the ability of participants to identify the trained higher-order visuospatial sequence on a recognition test, even though the trained and untrained recognition sequences were identical when viewed at a conscious binocular level, and differed only at the level of the masked sequential associations.

Conclusions/Significance

These results demonstrate that unconscious processing can support perceptual learning of higher-order sequential associations through interocular integration of retinotopic-based codes stemming from monocular eye-of-origin information. Furthermore, unlike other forms of perceptual associative learning, visuospatial attention did not need to be directed to the locations of the target sequence. More generally, the results pose a challenge to neural models of learning to account for a previously unknown capacity of the human visual system to support the detection, learning and recognition of higher-order sequential associations under conditions where observers are unable to see the target sequence or perform responses that coincide with structure of the target sequence.     

Individual differences in trait anxiety predict the response of the basolateral amygdala to unconsciously processed fearful faces

Responses to threat-related stimuli are influenced by conscious and unconscious processes, but the neural systems underlying these processes and their relationship to anxiety have not been clearly delineated. Using fMRI, we investigated the neural responses associated with the conscious and unconscious (backwardly masked) perception of fearful faces in healthy volunteers who varied in threat sensitivity (Spielberger trait anxiety scale). Unconscious processing modulated activity only in the basolateral subregion of the amygdala, while conscious processing modulated activity only in the dorsal amygdala (containing the central nucleus). Whereas activation of the dorsal amygdala by conscious stimuli was consistent across subjects and independent of trait anxiety, activity in the basolateral amygdala to unconscious stimuli, and subjects' reaction times, were predicted by individual differences in trait anxiety. These findings provide a biological basis for the unconscious emotional vigilance characteristic of anxiety and a means for investigating the mechanisms and efficacy of treatments for anxiety.     

综述: 人脑视觉意识的神经机制

意识的存在决定了人类生命的意义.意识问题被认为是21世纪科学要回答的一个最重要问题.意识科学正在成为认知和心理科学的皇冠,成为基础科学的顶峰.近20年来,随着认知科学、心理科学、神经科学和脑成像技术的发展,人们开始通过实验科学地研究意识问题,特别是与视觉意识相关的研究工作取得了很多重要进展.在这篇综述中,我们对以往的视觉意识研究工作进行了总结,并对未来的研究方向进行了展望.     

The flexible nature of unconscious cognition

The cognitive signature of unconscious processes is hotly debated recently. Generally, consciousness is thought to mediate flexible, adaptive and goal-directed behavior, but in the last decade unconscious processing has rapidly gained ground on traditional conscious territory. In this study we demonstrate that the scope and impact of unconscious information on behavior and brain activity can be modulated dynamically on a trial-by-trial basis. Participants performed a Go/No-Go experiment in which an unconscious (masked) stimulus preceding a conscious target could be associated with either a Go or No-Go response. Importantly, the mapping of stimuli onto these actions varied on a trial-by-trial basis, preventing the formation of stable associations and hence the possibility that unconscious stimuli automatically activate these control actions. By eliminating stimulus-response associations established through practice we demonstrate that unconscious information can be processed in a flexible and adaptive manner. In this experiment we show that the same unconscious stimulus can have a substantially different effect on behavior and (prefrontal) brain activity depending on the rapidly changing task context in which it is presented. This work suggests that unconscious information processing shares many sophisticated characteristics (including flexibility and context-specificity) with its conscious counterpart.     

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.     

Your unconscious knows your name

One''s own name constitutes a unique part of conscious awareness – but does this also hold true for unconscious processing? The present study shows that the own name has the power to bias a person''s actions unconsciously even in conditions that render any other name ineffective. Participants judged whether a letter string on the screen was a name or a non-word while this target stimulus was preceded by a masked prime stimulus. Crucially, the participant''s own name was among these prime stimuli and facilitated reactions to following name targets whereas the name of another, yoked participant did not. Signal detection results confirmed that participants were not aware of any of the prime stimuli, including their own name. These results extend traditional findings on “breakthrough” phenomena of personally relevant stimuli to the domain of unconscious processing. Thus, the brain seems to possess adroit mechanisms to identify and process such stimuli even in the absence of conscious awareness.     

Perceptual grouping of biological motion promotes binocular rivalry

Investigation of perceptual rivalry between conflicting stimuli presented one to each eye can further understanding of the neural underpinnings of conscious visual perception. During rivalry, visual awareness fluctuates between perceptions of the two stimuli. Here, we demonstrate that high-level perceptual grouping can promote rivalry between stimulus pairs that would otherwise be perceived as nonrivalrous. Perceptual grouping was generated with point-light walker stimuli that simulate human motion, visible only as lights placed on the joints. Although such walking figures are unrecognizable when stationary, recognition judgments as complex as gender and identity can accurately be made from animated displays, demonstrating the efficiency with which our visual system can group dynamic local signals into a globally coherent walking figure. We find that point-light walker stimuli presented one to each eye and in different colors and configurations results in strong rivalry. However, rivalry is minimal when the two walkers are split between the eyes or both presented to one eye. This pattern of results suggests that processing animated walker figures promotes rivalry between signals from the two eyes rather than between higher-level representations of the walkers. This leads us to hypothesize that awareness during binocular rivalry involves the integrated activity of high-level perceptual mechanisms in conjunction with lower-level ocular suppression modulated via cortical feedback.     

Robust Single Trial Identification of Conscious Percepts Triggered by Sensory Events of Variable Saliency

The neural correlates of visual awareness are elusive because of its fleeting nature. Here we have addressed this issue by using single trial statistical “brain reading” of neurophysiological event related (ERP) signatures of conscious perception of visual attributes with different levels of saliency. Behavioral reports were taken at every trial in 4 experiments addressing conscious access to color, luminance, and local phase offset cues. We found that single trial neurophysiological signatures of target presence can be observed around 300 ms at central parietal sites. Such signatures are significantly related with conscious perception, and their probability is related to sensory saliency levels. These findings identify a general neural correlate of conscious perception at the single trial level, since conscious perception can be decoded as such independently of stimulus salience and fluctuations of threshold levels. This approach can be generalized to successfully detect target presence in other individuals.     

To what extent are emotional visual stimuli processed without attention and awareness?

In the past few years, important contributions have been made to the study of emotional visual perception. Researchers have reported responses to emotional stimuli in the human amygdala under some unattended conditions (i.e. conditions in which the focus of attention was diverted away from the stimuli due to task instructions), during visual masking and during binocular suppression. Taken together, these results reveal the relative degree of autonomy of emotional processing. At the same time, however, important limitations to the notion of complete automaticity have been revealed. Effects of task context and attention have been shown, as well as large inter-subject differences in sensitivity to the detection of masked fearful faces (whereby briefly presented, target fearful faces are immediately followed by a neutral face that 'masks' the initial face). A better understanding of the neural basis of emotional perception and how it relates to visual attention and awareness is likely to require further refinement of the concepts of automaticity and awareness.     

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.     

Seeing without Seeing? Degraded Conscious Vision in a Blindsight Patient

Blindsight patients, whose primary visual cortex is lesioned, exhibit preserved ability to discriminate visual stimuli presented in their "blind" field, yet report no visual awareness hereof. Blindsight is generally studied in experimental investigations of single patients, as very few patients have been given this "diagnosis". In our single case study of patient GR, we ask whether blindsight is best described as unconscious vision, or rather as conscious, yet severely degraded vision. In experiment 1 and 2, we successfully replicate the typical findings of previous studies on blindsight. The third experiment, however, suggests that GR's ability to discriminate amongst visual stimuli does not reflect unconscious vision, but rather degraded, yet conscious vision. As our finding results from using a method for obtaining subjective reports that has not previously used in blindsight studies (but validated in studies of healthy subjects and other patients with brain injury), our results call for a reconsideration of blindsight, and, arguably also of many previous studies of unconscious perception in healthy subjects.     

Single units and conscious vision.

Figures that can be seen in more than one way are invaluable tools for the study of the neural basis of visual awareness, because such stimuli permit the dissociation of the neural responses that underlie what we perceive at any given time from those forming the sensory representation of a visual pattern. To study the former type of responses, monkeys were subjected to binocular rivalry, and the response of neurons in a number of different visual areas was studied while the animals reported their alternating percepts by pulling levers. Perception-related modulations of neural activity were found to occur to different extents in different cortical visual areas. The cells that were affected by suppression were almost exclusively binocular, and their proportion was found to increase in the higher processing stages of the visual system. The strongest correlations between neural activity and perception were observed in the visual areas of the temporal lobe. A strikingly large number of neurons in the early visual areas remained active during the perceptual suppression of the stimulus, a finding suggesting that conscious visual perception might be mediated by only a subset of the cells exhibiting stimulus selective responses. These physiological findings, together with a number of recent psychophysical studies, offer a new explanation of the phenomenon of binocular rivalry. Indeed, rivalry has long been considered to be closely linked with binocular fusion and stereopsis, and the sequences of dominance and suppression have been viewed as the result of competition between the two monocular channels. The physiological data presented here are incompatible with this interpretation. Rather than reflecting interocular competition, the rivalry is most probably between the two different central neural representations generated by the dichoptically presented stimuli. The mechanisms of rivalry are probably the same as, or very similar to, those underlying multistable perception in general, and further physiological studies might reveal much about the neural mechanisms of our perceptual organization.     

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.     

连续闪现抑制下对洞的无意识知觉

大量收敛一致的实验证据表明,图形的大范围性质可以由拓扑性质来描述,并且其检测发生在视觉过程的最早期,这些证据几乎全部来自对意识上知觉的研究,而拓扑性质的意识下加工机制尚有待发掘.意识下知觉是人的感官系统客观上接受刺激呈现但主观上没有察觉的知觉,其机制和应用长期以来一直是知觉研究的热点.本文采用了一种双眼竞争的变式——连续闪现抑制,将待检测的刺激图形掩蔽,使之处于意识下状态,考察意识下知觉中拓扑性质的加工."洞的个数"作为一种拓扑性质是本文的研究对象.通过量度被抑制图形从发生变化到被知觉的被抑制时间,或者被试对被抑制的变化图形的正确检测率,我们发现,相比于不变或者各种非拓扑性质变化,意识下知觉中的拓扑性质(洞的个数)的变化会使图形更快、更容易被检测到.本研究揭示了拓扑性质(洞的个数)在意识下知觉中的优先性,将拓扑知觉理论从意识上知觉领域拓展到了意识下知觉领域,为拓扑性质加工的早期性提供了有力的证据;另一方面,本研究也提示了拓扑性质经由皮层下视通路加工处理的可能性.     

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.     

Attention Increases the Temporal Precision of Conscious Perception: Verifying the Neural-ST2 Model

What role does attention play in ensuring the temporal precision of visual perception? Behavioural studies have investigated feature selection and binding in time using fleeting sequences of stimuli in the Rapid Serial Visual Presentation (RSVP) paradigm, and found that temporal accuracy is reduced when attentional control is diminished. To reduce the efficacy of attentional deployment, these studies have employed the Attentional Blink (AB) phenomenon. In this article, we use electroencephalography (EEG) to directly investigate the temporal dynamics of conscious perception. Specifically, employing a combination of experimental analysis and neural network modelling, we test the hypothesis that the availability of attention reduces temporal jitter in the latency between a target''s visual onset and its consolidation into working memory. We perform time-frequency analysis on data from an AB study to compare the EEG trials underlying the P3 ERPs (Event-related Potential) evoked by targets seen outside vs. inside the AB time window. We find visual differences in phase-sorted ERPimages and statistical differences in the variance of the P3 phase distributions. These results argue for increased variation in the latency of conscious perception during the AB. This experimental analysis is complemented by a theoretical exploration of temporal attention and target processing. Using activation traces from the Neural-ST² model, we generate virtual ERPs and virtual ERPimages. These are compared to their human counterparts to propose an explanation of how target consolidation in the context of the AB influences the temporal variability of selective attention. The AB provides us with a suitable phenomenon with which to investigate the interplay between attention and perception. The combination of experimental and theoretical elucidation in this article contributes to converging evidence for the notion that the AB reflects a reduction in the temporal acuity of selective attention and the timeliness of perception.     

Modulation of semantic processing by spatial selective attention

The effects of spatial selective attention upon ERPs associated with the processing of word stimuli were investigated. While subjects maintained central eye fixation, ERPs were recorded to words presented to the left and right visual fields. In each of 6 runs, subjects focussed attention to alternate fields to perform a category-detection task. Pairs of semantically related and repeated words were embedded in the word lists presented to the attended and unattended visual fields. Consistent with prior studies, the P1-N1 visual ERP was larger when elicited by words in attended spatial locations. A large negative slow wave identified as N400 was elicited by attended, but not unattended, words. For attended words, N400 was smaller for semantically primed or repeated words. We concluded that spatial selective attention can modulate the degree to which words are processed, and that the cognitive processes associated with N400 are not automatic.     

Overt visual attention as a causal factor of perceptual awareness

Our everyday conscious experience of the visual world is fundamentally shaped by the interaction of overt visual attention and object awareness. Although the principal impact of both components is undisputed, it is still unclear how they interact. Here we recorded eye-movements preceding and following conscious object recognition, collected during the free inspection of ambiguous and corresponding unambiguous stimuli. Using this paradigm, we demonstrate that fixations recorded prior to object awareness predict the later recognized object identity, and that subjects accumulate more evidence that is consistent with their later percept than for the alternative. The timing of reached awareness was verified by a reaction-time based correction method and also based on changes in pupil dilation. Control experiments, in which we manipulated the initial locus of visual attention, confirm a causal influence of overt attention on the subsequent result of object perception. The current study thus demonstrates that distinct patterns of overt attentional selection precede object awareness and thereby directly builds on recent electrophysiological findings suggesting two distinct neuronal mechanisms underlying the two phenomena. Our results emphasize the crucial importance of overt visual attention in the formation of our conscious experience of the visual world.