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.     

Attentional weighting: a possible account of visual field asymmetries in visual search?

Several previous visual search studies measuring reaction times have demonstrated scanning biases across the visual field (i.e. a tendency to begin a serial search in a particular region of space). In the present study, we measured visual discrimination thresholds for a target presented amongst distractors using displays that were short enough to greatly reduce the potential for serial (i.e. scanning) search. For both a motion and orientation task, subjects' performance was significantly better when the target appeared in the inferior, as compared to the superior, visual field (no differences were observed between left and right visual fields). These findings suggest that subjects may divide attention unevenly across the visual field when searching for a target amongst distractors, a phenomenon we refer to as 'attentional weighting'. To rule out the possibility that these visual field asymmetries were sensory in nature, thresholds were also measured for conditions in which subjects' attention was directed to the location of the target stimulus, either because it was presented alone in the display or because a spatial cue directed subjects' attention to the location of that target presented amongst distractors. Under these conditions, visual field asymmetries were smaller (or non-existent), suggesting that sensory factors (such as crowding) are unlikely to account for our results. In addition, analyses of set-size effects (obtained by comparing thresholds for a single target vs. the target presented amongst distractors) could be accounted for by an unlimited capacity model, suggesting that multiple stimuli can be processed simultaneously without any limitations at an early stage of sensory processing. Taken together, these findings suggest the possible existence of biases in attentional weighting at a late stage of processing. The bias appears to favor the inferior visual field, which may arise from the fact that there is more ecologically-relevant information in this region of space.     

Stay Tuned: What Is Special About Not Shifting Attention?

Background

When studying attentional orienting processes, brain activity elicited by symbolic cue is usually compared to a neutral condition in which no information is provided about the upcoming target location. It is generally assumed that when a neutral cue is provided, participants do not shift their attention. The present study sought to validate this assumption. We further investigated whether anticipated task demands had an impact on brain activity related to processing symbolic cues.

Methodology/Principal Findings

Two experiments were conducted, during which event-related potentials were elicited by symbolic cues that instructed participants to shift their attention to a particular location on a computer screen. In Experiment 1, attention shift-inducing cues were compared to non-informative cues, while in both conditions participants were required to detect target stimuli that were subsequently presented at peripheral locations. In Experiment 2, a non-ambiguous “stay-central” cue that explicitly required participants not to shift their attention was used instead. In the latter case, target stimuli that followed a stay-central cue were also presented at a central location. Both experiments revealed enlarged early latency contralateral ERP components to shift-inducing cues compared to those elicited by either non-informative (exp. 1) or stay-central cues (exp. 2). In addition, cueing effects were modulated by the anticipated difficulty of the upcoming target, particularly so in Experiment 2. A positive difference, predominantly over the posterior contralateral scalp areas, could be observed for stay-central cues, especially for those predicting that the upcoming target would be easy. This effect was not present for non-informative cues.

Conclusions/Significance

We interpret our result in terms of a more rapid engagement of attention occurring in the presence of a more predictive instruction (i.e. stay-central easy target). Our results indicate that the human brain is capable of very rapidly identifying the difference between different types of instructions.     

Alternation of Sound Location Induces Visual Motion Perception of a Static Object

Background

Audition provides important cues with regard to stimulus motion although vision may provide the most salient information. It has been reported that a sound of fixed intensity tends to be judged as decreasing in intensity after adaptation to looming visual stimuli or as increasing in intensity after adaptation to receding visual stimuli. This audiovisual interaction in motion aftereffects indicates that there are multimodal contributions to motion perception at early levels of sensory processing. However, there has been no report that sounds can induce the perception of visual motion.

Methodology/Principal Findings

A visual stimulus blinking at a fixed location was perceived to be moving laterally when the flash onset was synchronized to an alternating left-right sound source. This illusory visual motion was strengthened with an increasing retinal eccentricity (2.5 deg to 20 deg) and occurred more frequently when the onsets of the audio and visual stimuli were synchronized.

Conclusions/Significance

We clearly demonstrated that the alternation of sound location induces illusory visual motion when vision cannot provide accurate spatial information. The present findings strongly suggest that the neural representations of auditory and visual motion processing can bias each other, which yields the best estimates of external events in a complementary manner.     

Mislocalization of visual stimuli: independent effects of static and dynamic attention

Shifts of visual attention cause systematic distortions of the perceived locations of visual objects around the focus of attention. In the attention repulsion effect, the perceived location of a visual target is shifted away from an attention-attracting cue when the cue is presented before the target. Recently it has been found that, if the visual cue is presented after the target, the perceived location of the target shifts toward the location of the following cue. One unanswered question is whether a single mechanism underlies both attentional repulsion and attraction effects. We presented participants with two disks at diagonal locations as visual cues and two vertical lines as targets. Participants were asked to perform a forced-choice task to judge targets' positions. The present study examined whether the magnitude of the repulsion effect and the attraction effect would differ (Experiment 1), whether the two effects would interact (Experiment 2), and whether the location or the dynamic shift of attentional focus would determine the distortions effects (Experiment 3). The results showed that the effect size of the attraction effect was slightly larger than the repulsion effect and the preceding and following cues have independent influences on the perceived positions. The repulsion effect was caused by the location of attnetion and the attraction effect was due to the dynamic shift of attentional focus, suggesting that the underlying mechanisms for the retrospective attraction effect might be different from those for the repulsion effect.     

Vision in Flies: Measuring the Attention Span

A visual stimulus at a particular location of the visual field may elicit a behavior while at the same time equally salient stimuli in other parts do not. This property of visual systems is known as selective visual attention (SVA). The animal is said to have a focus of attention (FoA) which it has shifted to a particular location. Visual attention normally involves an attention span at the location to which the FoA has been shifted. Here the attention span is measured in Drosophila. The fly is tethered and hence has its eyes fixed in space. It can shift its FoA internally. This shift is revealed using two simultaneous test stimuli with characteristic responses at their particular locations. In tethered flight a wild type fly keeps its FoA at a certain location for up to 4s. Flies with a mutation in the radish gene, that has been suggested to be involved in attention-like mechanisms, display a reduced attention span of only 1s.     

Attention increases sensitivity of V4 neurons

When attention is directed to a location in the visual field, sensitivity to stimuli at that location is increased. At the neuronal level, this could arise either through a multiplicative increase in firing rate or through an increase in the effective strength of the stimulus. To test conflicting predictions of these alternative models, we recorded responses of V4 neurons to stimuli across a range of luminance contrasts and measured the change in response when monkeys attended to them in order to discriminate a target stimulus from nontargets. Attention caused greater increases in response at low contrast than at high contrast, consistent with an increase in effective stimulus strength. On average, attention increased the effective contrast of the attended stimulus by a factor of 1.51, an increase of 51% of its physical contrast.     

The multisensory attentional consequences of tool use: a functional magnetic resonance imaging study

Background

Tool use in humans requires that multisensory information is integrated across different locations, from objects seen to be distant from the hand, but felt indirectly at the hand via the tool. We tested the hypothesis that using a simple tool to perceive vibrotactile stimuli results in the enhanced processing of visual stimuli presented at the distal, functional part of the tool. Such a finding would be consistent with a shift of spatial attention to the location where the tool is used.

Methodology/Principal Findings

We tested this hypothesis by scanning healthy human participants'' brains using functional magnetic resonance imaging, while they used a simple tool to discriminate between target vibrations, accompanied by congruent or incongruent visual distractors, on the same or opposite side to the tool. The attentional hypothesis was supported: BOLD response in occipital cortex, particularly in the right hemisphere lingual gyrus, varied significantly as a function of tool position, increasing contralaterally, and decreasing ipsilaterally to the tool. Furthermore, these modulations occurred despite the fact that participants were repeatedly instructed to ignore the visual stimuli, to respond only to the vibrotactile stimuli, and to maintain visual fixation centrally. In addition, the magnitude of multisensory (visual-vibrotactile) interactions in participants'' behavioural responses significantly predicted the BOLD response in occipital cortical areas that were also modulated as a function of both visual stimulus position and tool position.

Conclusions/Significance

These results show that using a simple tool to locate and to perceive vibrotactile stimuli is accompanied by a shift of spatial attention to the location where the functional part of the tool is used, resulting in enhanced processing of visual stimuli at that location, and decreased processing at other locations. This was most clearly observed in the right hemisphere lingual gyrus. Such modulations of visual processing may reflect the functional importance of visuospatial information during human tool use.     

Increased activity in human visual cortex during directed attention in the absence of visual stimulation

When subjects direct attention to a particular location in a visual scene, responses in the visual cortex to stimuli presented at that location are enhanced, and the suppressive influences of nearby distractors are reduced. What is the top-down signal that modulates the response to an attended versus an unattended stimulus? Here, we demonstrate increased activity related to attention in the absence of visual stimulation in extrastriate cortex when subjects covertly directed attention to a peripheral location expecting the onset of visual stimuli. Frontal and parietal areas showed a stronger signal increase during this expectation than did visual areas. The increased activity in visual cortex in the absence of visual stimulation may reflect a top-down bias of neural signals in favor of the attended location, which derives from a fronto-parietal network.     

Is Attention Based on Spatial Contextual Memory Preferentially Guided by Low Spatial Frequency Signals?

A popular model of visual perception states that coarse information (carried by low spatial frequencies) along the dorsal stream is rapidly transmitted to prefrontal and medial temporal areas, activating contextual information from memory, which can in turn constrain detailed input carried by high spatial frequencies arriving at a slower rate along the ventral visual stream, thus facilitating the processing of ambiguous visual stimuli. We were interested in testing whether this model contributes to memory-guided orienting of attention. In particular, we asked whether global, low-spatial frequency (LSF) inputs play a dominant role in triggering contextual memories in order to facilitate the processing of the upcoming target stimulus. We explored this question over four experiments. The first experiment replicated the LSF advantage reported in perceptual discrimination tasks by showing that participants were faster and more accurate at matching a low spatial frequency version of a scene, compared to a high spatial frequency version, to its original counterpart in a forced-choice task. The subsequent three experiments tested the relative contributions of low versus high spatial frequencies during memory-guided covert spatial attention orienting tasks. Replicating the effects of memory-guided attention, pre-exposure to scenes associated with specific spatial memories for target locations (memory cues) led to higher perceptual discrimination and faster response times to identify targets embedded in the scenes. However, either high or low spatial frequency cues were equally effective; LSF signals did not selectively or preferentially contribute to the memory-driven attention benefits to performance. Our results challenge a generalized model that LSFs activate contextual memories, which in turn bias attention and facilitate perception.     

Attention samples stimuli rhythmically

Overt exploration or sampling behaviors, such as whisking, sniffing, and saccadic eye movements, are often characterized by a rhythm. In addition, the electrophysiologically recorded theta or alpha phase predicts global detection performance. These two observations raise the intriguing possibility that covert selective attention samples from multiple stimuli rhythmically. To investigate this possibility, we measured change detection performance on two simultaneously presented stimuli, after resetting attention to one of them. After a reset flash at one stimulus location, detection performance fluctuated rhythmically. When the flash was presented in the right visual field, a 4 Hz rhythm was directly visible in the time courses of behavioral performance at both stimulus locations, and the two rhythms were in antiphase. A left visual field flash exerted only partial reset on performance and induced rhythmic fluctuation at higher frequencies (6-10 Hz). These findings show that selective attention samples multiple stimuli rhythmically, and they position spatial attention within the family of exploration behaviors.     

Functionally independent components of early event-related potentials in a visual spatial attention task.

Spatial visual attention modulates the first negative-going deflection in the human averaged event-related potential (ERP) in response to visual target and non-target stimuli (the N1 complex). Here we demonstrate a decomposition of N1 into functionally independent subcomponents with functionally distinct relations to task and stimulus conditions. ERPs were collected from 20 subjects in response to visual target and non-target stimuli presented at five attended and non-attended screen locations. Independent component analysis, a new method for blind source separation, was trained simultaneously on 500 ms grand average responses from all 25 stimulus-attention conditions and decomposed the non-target N1 complexes into five spatially fixed, temporally independent and physiologically plausible components. Activity of an early, laterally symmetrical component pair (N1aR and N1aL) was evoked by the left and right visual field stimuli, respectively. Component N1aR peaked ca. 9 ms earlier than N1aL. Central stimuli evoked both components with the same peak latency difference, producing a bilateral scalp distribution. The amplitudes of these components were no reliably augmented by spatial attention. Stimuli in the right visual field evoked activity in a spatio-temporally overlapping bilateral component (N1b) that peaked at ca. 180 ms and was strongly enhanced by attention. Stimuli presented at unattended locations evoked a fourth component (P2a) peaking near 240 ms. A fifth component (P3f) was evoked only by targets presented in either visual field. The distinct response patterns of these components across the array of stimulus and attention conditions suggest that they reflect activity in functionally independent brain systems involved in processing attended and unattended visuospatial events.     

The forest or the trees: preference for global over local image processing is reversed by prior experience in honeybees

Traditional models of insect vision have assumed that insects are only capable of low-level analysis of local cues and are incapable of global, holistic perception. However, recent studies on honeybee (Apis mellifera) vision have refuted this view by showing that this insect also processes complex visual information by using spatial configurations or relational rules. In the light of these findings, we asked whether bees prioritize global configurations or local cues by setting these two levels of image analysis in competition. We trained individual free-flying honeybees to discriminate hierarchical visual stimuli within a Y-maze and tested bees with novel stimuli in which local and/or global cues were manipulated. We demonstrate that even when local information is accessible, bees prefer global information, thus relying mainly on the object''s spatial configuration rather than on elemental, local information. This preference can be reversed if bees are pre-trained to discriminate isolated local cues. In this case, bees prefer the hierarchical stimuli with the local elements previously primed even if they build an incorrect global configuration. Pre-training with local cues induces a generic attentional bias towards any local elements as local information is prioritized in the test, even if the local cues used in the test are different from the pre-trained ones. Our results thus underline the plasticity of visual processing in insects and provide new insights for the comparative analysis of visual recognition in humans and animals.     

Preparatory effects of distractor suppression: evidence from visual cortex

Spatial selective attention is the mechanism that facilitates the selection of relevant information over irrelevant information in the visual field. The current study investigated whether foreknowledge of the presence or absence of distractors surrounding an impending target stimulus results in preparatory changes in visual cortex. We cued the location of the target and the presence or absence of distractors surrounding the target while changes in blood oxygen level dependent (BOLD) signals were measured. In line with prior work, we found that top-down spatial attention resulted in an increased contralateral BOLD response, evoked by the cue throughout early visual cortex (areas V1, V2 and V3). In addition, cues indicating distractor presence evoked a substantial increase in the magnitude of the BOLD signal in visual area V3, but not in V2 or V1. This study shows that prior knowledge concerning the presence of a distractor results in enhanced attentional modulation of visual cortex, in visual areas where neuronal receptive fields are large enough to encompass both targets and distractors. We interpret these findings as evidence that top-down attentional control processes include active preparatory suppression mechanisms for irrelevant, distracting information in the visual scene.     

Attention-dependent representation of a size illusion in human V1

One of the most fundamental properties of human primary visual cortex (V1) is its retinotopic organization, which makes it an ideal candidate for encoding spatial properties, such as size, of objects. However, three-dimensional (3D) contextual information can lead to size illusions that are reflected in the spatial pattern of activity in V1 [1]. A critical question is how complex 3D contextual information can influence spatial activity patterns in V1. Here, we assessed whether changes in the spatial distribution of activity in V1 depend on the focus of attention, which would be suggestive of feedback of 3D contextual information from higher visual areas. We presented two 3D rings at close and far apparent depths in a 3D scene. When subjects fixated its center, the far ring appeared to be larger and occupy a more eccentric portion of the visual field, relative to the close ring. Using functional magnetic resonance imaging, we found that the spatial distribution of V1 activity induced by the far ring was also shifted toward a more eccentric representation of the visual field, whereas that induced by the close ring was shifted toward the foveal representation, consistent with their perceptual appearances. This effect was significantly reduced when the focus of spatial attention was narrowed with a demanding central fixation task. We reason that focusing attention on the fixation task resulted in reduced activity in--and therefore reduced feedback from--higher visual areas that process the 3D depth cues.     

Role of chemical and visual cues in food recognition by leatherback posthatchlings (Dermochelys coriacea L)

We raised leatherback posthatchlings in the laboratory for up to 7 weeks to study the role of visual and chemical cues in food recognition and food-seeking behavior. Turtles were reared on a formulated (artificial gelatinous) diet and had no contact with test materials until experiments began. Subjects were presented with visual cues (a plastic jellyfish; white plastic shapes [circle, square, diamond] similar in surface area to the plastic model), chemical cues (homogenates of lion's mane jellyfish, Cyanea capillata; moon jellyfish, Aurelia aurita; and a ctenophore, Ocyropsis sp., introduced through a water filter outflow), and visual and chemical cues presented simultaneously. Visual stimuli evoked an increase in swimming activity, biting, diving, and orientation toward the object. Chemical cues elicited an increase in biting, and orientation into water currents (rheotaxis). When chemical and visual stimuli were combined, turtles ignored currents and oriented toward the visual stimuli. We conclude that both cues are used to search for, and locate, food but that visual cues may be of primary importance. We hypothesize that under natural conditions turtles locate food visually, then, as a consequence of feeding, associate chemical with visual cues. Chemical cues then may function alone as a feeding attractant.     

Shifting attention within memory representations involves early visual areas

Prior studies have shown that spatial attention modulates early visual cortex retinotopically, resulting in enhanced processing of external perceptual representations. However, it is not clear whether the same visual areas are modulated when attention is focused on, and shifted within a working memory representation. In the current fMRI study participants were asked to memorize an array containing four stimuli. After a delay, participants were presented with a verbal cue instructing them to actively maintain the location of one of the stimuli in working memory. Additionally, on a number of trials a second verbal cue instructed participants to switch attention to the location of another stimulus within the memorized representation. Results of the study showed that changes in the BOLD pattern closely followed the locus of attention within the working memory representation. A decrease in BOLD-activity (V1-V3) was observed at ROIs coding a memory location when participants switched away from this location, whereas an increase was observed when participants switched towards this location. Continuous increased activity was obtained at the memorized location when participants did not switch. This study shows that shifting attention within memory representations activates the earliest parts of visual cortex (including V1) in a retinotopic fashion. We conclude that even in the absence of visual stimulation, early visual areas support shifting of attention within memorized representations, similar to when attention is shifted in the outside world. The relationship between visual working memory and visual mental imagery is discussed in light of the current findings.     

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.     

Neurons in area V4 of the macaque translate attended visual features into behaviorally relevant categories

Neural processing at most stages of the primate visual system is modulated by selective attention, such that behaviorally relevant information is emphasized at the expenses of irrelevant, potentially distracting information. The form of attention best understood at the cellular level is when stimuli at a given location in the visual field must be selected (space-based attention). In contrast, fewer single-unit recording studies have so far explored the cellular mechanisms of attention operating on individual stimulus features, specifically when one feature (e.g., color) of an object must guide behavioral responses while a second feature (e.g., shape) of the same object is potentially interfering and therefore must be ignored. Here we show that activity of neurons in macaque area V4 can underlie the selection of elemental object features and their "translation" into a categorical format that can directly contribute to the control of the animal's behavior.