Object-based attention to one of two superimposed surfaces alters responses in human early visual cortex

Faced with an overwhelming amount of sensory information, we are able to prioritize the processing of select spatial locations and visual features. The neuronal mechanisms underlying such spatial and feature-based selection have been studied in considerable detail. More recent work shows that attention can also be allocated to objects, even spatially superimposed objects composed of dynamically changing features that must be integrated to create a coherent object representation. Much less is known about the mechanisms underlying such object-based selection. Our goal was to investigate behavioral and neuronal responses when attention was directed to one of two objects, specifically one of two superimposed transparent surfaces, in a task designed to preclude space-based and feature-based selection. We used functional magnetic resonance imaging (fMRI) to measure changes in blood oxygen level-dependent (BOLD) signals when attention was deployed to one or the other surface. We found that visual areas V1, V2, V3, V3A, and MT+ showed enhanced BOLD responses to translations of an attended relative to an unattended surface. These results reveal that visual areas as early as V1 can be modulated by attending to objects, even objects defined by dynamically changing elements. This provides definitive evidence in humans that early visual areas are involved in a seemingly high-order process. Furthermore, our results suggest that these early visual areas may participate in object-specific feature "binding," a process that seemingly must occur for an object or a surface to be the unit of attentional selection.     

Effects of attention and emotion on repetition priming and their modulation by cholinergic enhancement

We examined whether behavioral and neural effects of repeating faces are modulated by independent factors of selective attention, emotion, and cholinergic enhancement, during functional MRI. Face repetition occurred either between task-relevant (spatially attended) or task-irrelevant (unattended) stimuli; faces could be fearful or neutral; subjects received either placebo or physostigmine. Under placebo, a reaction time advantage occurred with repetition (i.e., priming) that did not differ between levels of attention, but was attenuated with emotion. Inferior temporo-occipital cortex demonstrated repetition decreases to both attended and unattended faces, and showed either equivalent or greater repetition decreases with emotional compared with neutral faces. By contrast, repetition decreases were attenuated for emotional relative to neutral faces in lateral orbitofrontal cortex. These results distinguish automatic repetition effects in sensory cortical regions from repetition effects modulated by emotion in orbitofrontal cortex, which parallel behavioral effects. Under physostigmine, unlike placebo, behavioral repetition effects were seen selectively for attended faces only, whereas emotional faces no longer impaired priming. Physostigmine enhanced repetition decreases in inferior occipital cortex selectively for attended faces, and reversed the emotional interaction with repetition in lateral orbitofrontal cortex. Thus we show that cholinergic enhancement both augments a neural signature of priming and modulates the effects of attention and emotion on behavioral and neural consequences of repetition.     

Parallel attentional facilitation of features and objects in early visual cortex

Selective attention can enhance the processing of attended features across the entire visual field. Attention also spreads within objects, enhancing all internal locations and task-irrelevant features of selected objects. Here, we examine the extent to which attentional enhancement of a feature spreads across attended and unattended objects. Two fully overlapping counter-rotating bicolored surfaces of light and dark random dots were presented on a gray background of intermediate luminance. This stimulus creates a percept of two separate semitransparent surfaces and allows the measurement of feature- and object-based selections while controlling spatial attention. On each trial, human participants attended to a subset of dots defined by feature (luminance polarity) and object (surface) in order to detect brief episodes of radial motion while ignoring any events in the unattended groups of dots. Attentional selection was assessed by means of steady-state visual evoked potentials (SSVEPs) and behavioral measures. SSVEP amplitudes recorded at medial occipital electrode sites were modulated both by surface-based and luminance polarity-based selection in a manner consistent with independent multiplicative enhancement of attentional effects in different dimensions in early visual cortex. This finding supports the view that feature-based attention spreads across object boundaries, at least at an early stage of processing. However, SSVEPs elicited at more lateral electrode sites showed a hierarchical pattern of selection, potentially reflecting the binding of surface-defining features with luminance features to enable surface-based attention.     

A deficit in contralesional object representation associated with attentional limitations after parietal damage

Stankiewicz, Hummel, and Cooper (1998) proposed that detailed coding of part-whole relations for objects is contingent on objects being attended. We report a neuropsychological test of this assertion. We examined the effects of left-right reflection on object matching in a group of patients with parietal damage and impaired attention to the contralesional side of space (Experiment 1). The patients were poor at matching objects subject to left-right reflection, relative to identical stimuli (Experiment 2). This was not due to a lack of sensitivity to information on the contralesional side. In a subsequent study, the patients were better at matching identical whole objects at fixation than when they just received half the object in their ipsilesional field (Experiment 3). However, unlike both nonlesioned controls and control patients with frontal lesions, the parietal patients were unaffected by altering the relative spatial locations of object features in their contralesional field (Experiment 4). The basic result, of poor performance with left-right-reflected items, was also replicated using a priming rather than an explicit matching procedure (Experiment 5). These results provide confirmation that visual attention, mediated by the posterior parietal cortex, is important for generating part-whole codes that facilitate the matching of mirror-reflected objects.     

Spatial and cross-modal attention alter responses to unattended sensory information in early visual and auditory human cortex

Attending to a visual or auditory stimulus often requires irrelevant information to be filtered out, both within the modality attended and in other modalities. For example, attentively listening to a phone conversation can diminish our ability to detect visual events. We used functional magnetic resonance imaging (fMRI) to examine brain responses to visual and auditory stimuli while subjects attended visual or auditory information. Although early cortical areas are traditionally considered unimodal, we found that brain responses to the same ignored information depended on the modality attended. In early visual area V1, responses to ignored visual stimuli were weaker when attending to another visual stimulus, compared with attending to an auditory stimulus. The opposite was true in more central visual area MT+, where responses to ignored visual stimuli were weaker when attending to an auditory stimulus. Furthermore, fMRI responses to the same ignored visual information depended on the location of the auditory stimulus, with stronger responses when the attended auditory stimulus shared the same side of space as the ignored visual stimulus. In early auditory cortex, responses to ignored auditory stimuli were weaker when attending a visual stimulus. A simple parameterization of our data can describe the effects of redirecting attention across space within the same modality (spatial attention) or across modalities (cross-modal attention), and the influence of spatial attention across modalities (cross-modal spatial attention). Our results suggest that the representation of unattended information depends on whether attention is directed to another stimulus in the same modality or the same region of space.     

Selective attention modulates visual and haptic repetition priming: effects in aging and Alzheimer's disease

In two experiments, we examined the effect of selective attention at encoding on repetition priming in normal aging and Alzheimer's disease (AD) patients for objects presented visually (experiment 1) or haptically (experiment 2). We used a repetition priming paradigm combined with a selective attention procedure at encoding. Reliable priming was found for both young adults and healthy older participants for visually presented pictures (experiment 1) as well as for haptically presented objects (experiment 2). However, this was only found for attended and not for unattended stimuli. The results suggest that independently of the perceptual modality, repetition priming requires attention at encoding and that perceptual facilitation is maintained in normal aging. However, AD patients did not show priming for attended stimuli, or for unattended visual or haptic objects. These findings suggest an early deficit of selective attention in AD. Results are discussed from a cognitive neuroscience approach.     

A deficit in contralesional object representation associated with attentional limitations after parietal damage

Stankiewicz, Hummel, and Cooper (1998) proposed that detailed coding of part–whole relations for objects is contingent on objects being attended. We report a neuropsychological test of this assertion. We examined the effects of left–right reflection on object matching in a group of patients with parietal damage and impaired attention to the contralesional side of space (Experiment 1). The patients were poor at matching objects subject to left–right reflection, relative to identical stimuli (Experiment 2). This was not due to a lack of sensitivity to information on the contralesional side. In a subsequent study, the patients were better at matching identical whole objects at fixation than when they just received half the object in their ipsilesional field (Experiment 3). However, unlike both nonlesioned controls and control patients with frontal lesions, the parietal patients were unaffected by altering the relative spatial locations of object features in their contralesional field (Experiment 4). The basic result, of poor performance with left–right-reflected items, was also replicated using a priming rather than an explicit matching procedure (Experiment 5). These results provide confirmation that visual attention, mediated by the posterior parietal cortex, is important for generating part–whole codes that facilitate the matching of mirror-reflected objects.     

Effect of mental fatigue caused by mobile 3D viewing on selective attention: An ERP study

This study investigated behavioral responses to and auditory event-related potential (ERP) correlates of mental fatigue caused by mobile three-dimensional (3D) viewing. Twenty-six participants (14 women) performed a selective attention task in which they were asked to respond to the sounds presented at the attended side while ignoring sounds at the ignored side before and after mobile 3D viewing. Considering different individual susceptibilities to 3D, participants' subjective fatigue data were used to categorize them into two groups: fatigued and unfatigued. The amplitudes of d-ERP components were defined as differences in amplitudes between time-locked brain oscillations of the attended and ignored sounds, and these values were used to calculate the degree to which spatial selective attention was impaired by 3D mental fatigue. The fatigued group showed significantly longer response times after mobile 3D viewing compared to before the viewing. However, response accuracy did not significantly change between the two conditions, implying that the participants used a behavioral strategy to cope with their performance accuracy decrement by increasing their response times. No significant differences were observed for the unfatigued group. Analysis of covariance revealed group differences with significant and trends toward significant decreases in the d-P200 and d-late positive potential (LPP) amplitudes at the occipital electrodes of the fatigued and unfatigued groups. Our findings indicate that mentally fatigued participants did not effectively block out distractors in their information processing mechanism, providing support for the hypothesis that 3D mental fatigue impairs spatial selective attention and is characterized by changes in d-P200 and d-LPP amplitudes.     

Modulation of event-related potentials by word repetition: The role of visual selective attention

Event-related potentials (ERPs) were recorded while subjects viewed visually presented words, some of which occurred twice. Each trial consisted of two colored letter strings, the requirement being to attend to and make a word/non word discrimination for one of the strings. Attention was manipulated by color in Experiment 1, and color and a precue were used in Experiment 2. As in previous ERP studies of word repetition, a positive offset to repeated words developed when both first and second presentations were the focus of attention. In Experiment 2, ERPs showed evidence of positive-going repetition effects in all conditions in which at least one of the two presentations of the repeated word was attended. In the visual modality, the positive-going ERP repetition effect occurs only when at least one of the two presentations of a repeated item is the object of attention, which suggests that one or more of the processes reflected by the effect is capacity limited.     

Object-selective cortex exhibits performance-independent repetition suppression

Object-selective cortical regions exhibit a decreased response when an object stimulus is repeated [repetition suppression (RS)]. RS is often associated with priming: reduced response times and increased accuracy for repeated stimuli. It is unknown whether RS reflects stimulus-specific repetition, the associated changes in response time, or the combination of the two. To address this question, we performed a rapid event-related functional MRI (fMRI) study in which we measured BOLD signal in object-selective cortex, as well as object recognition performance, while we manipulated stimulus repetition. Our design allowed us to examine separately the roles of response time and repetition in explaining RS. We found that repetition played a robust role in explaining RS: repeated trials produced weaker BOLD responses than nonrepeated trials, even when comparing trials with matched response times. In contrast, response time played a weak role in explaining RS when repetition was controlled for: it explained BOLD responses only for one region of interest (ROI) and one experimental condition. Thus repetition suppression seems to be mostly driven by repetition rather than performance changes. We further examined whether RS reflects processes occurring at the same time as recognition or after recognition by manipulating stimulus presentation duration. In one experiment, durations were longer than required for recognition (2 s), whereas in a second experiment, durations were close to the minimum time required for recognition (85-101 ms). We found significant RS for brief presentations (albeit with a reduced magnitude), which again persisted when controlling for performance. This suggests a substantial amount of RS occurs during recognition.     

Attentional capacity for processing concurrent stimuli is larger across sensory modalities than within a modality

One finding in attention research is that visual and auditory attention mechanisms are linked together. Such a link would predict a central, amodal capacity limit in processing visual and auditory stimuli. Here we show that this is not the case. Letter streams were accompanied by asynchronously presented streams of auditory, visual, and audiovisual objects. Either the letter streams or the visual, auditory, or audiovisual parts of the object streams were attended. Attending to various aspects of the objects resulted in modulations of the letter-stream-elicited steady-state evoked potentials (SSVEPs). SSVEPs were larger when auditory objects were attended than when either visual objects alone or when auditory and visual object stimuli were attended together. SSVEP amplitudes were the same in the latter conditions, indicating that attentional capacity between modalities is larger than attentional capacity within one and the same modality.     

Spatially specific FMRI repetition effects in human visual cortex

The functional MRI (fMRI) response to a pair of identical, successively presented stimuli can result in a smaller signal than the presentation of two nonidentical stimuli. This "repetition effect" has become a frequently used tool to make inferences about neural selectivity in specific cortical areas. However, little is known about the mechanism(s) underlying the effect. In particular, despite many successful applications of the technique in higher visual areas, repetition effects in lower visual areas [e.g., primary visual cortex (V1)] have been more difficult to characterize. One property that is well understood in early visual areas is the mapping of visual field locations to specific areas of the cortex (i.e., retinotopy). We used the retinotopic organization of V1 to activate progressively different populations of neurons in a rapid fMRI experimental design. We observed a repetition effect (reduced signal) when localized stimulus elements were repeated in identical locations. We show that this effect is spatially tuned and largely independent of both interstimulus interval (100-800 ms) and the focus of attention. Using the same timing parameters for which we observed a large effect of spatial position, we also examined the response to orientation changes and observed no effect of an orientation change on the response to repeated stimuli in V1 but significant effects in other retinotopic areas. Given these results, we discuss the possible causes of these repetition effects as well as the implications for interpreting other experiments that use this potentially powerful imaging technique.     

Independence of anticipatory signals for spatial attention from number of nontarget stimuli in the visual field

Covertly attending to a location modulates the activity of visual areas even in the absence of visual stimulation. These effects are widespread, being found in the cortical representations of both attended and unattended portions of the visual field. It is not clear, however, whether preparatory modulations depend on subjects' expectation regarding the presence of additional nontarget stimuli in the visual field. Here, we asked subjects to endogenously direct attention to a peripheral location in the upper visual field, to identify the orientation of a low-contrast target stimulus, and we manipulated the number and behavioral relevance of other low-contrast nontarget stimuli in the visual field. Anticipatory (i.e., prestimulus) blood oxygenation level-dependent (BOLD) signal increments in visual cortex were strongest at the contralateral attended location, whereas signal decrements were strongest at the unattended mirror-opposite ipsilateral location/region of visual cortex. Importantly, these strong anticipatory decrements were not related to the presence/absence of nontarget low-contrast stimuli and did not correlate with either weaker target-evoked responses or worse performance. Second, the presence of other low-contrast stimuli in the visual field, even when potential targets, did not modify the anticipatory signal modulation either at target or nontarget locations. We conclude that the topography of spatial attention-related anticipatory BOLD signal modulation across visual cortex, specifically decrements at unattended locations, is mainly determined by processes at the cued location and not by the number or behavioral relevance of distant low-contrast nontarget stimuli elsewhere in the visual field.     

Effects of task difficulty and target likelihood in area V4 of macaque monkeys

Spatial attention improves performance at attended locations and correspondingly modulates firing rates of cortical neurons. The size of these behavioral and neuronal effects depends on the difficulty of the task performed at the attended location. Psychological theorists have attributed this to a tighter focus of a fixed amount of processing resource at the attended location, but the effects of task difficulty on the distribution of neuronal effects of attention across the visual field have not been fully explored. We trained rhesus monkeys to do a detection task in which difficulty and spatial attention were manipulated independently. Probe stimuli were used to measure behavioral performance in different conditions of attention and difficulty. Animals performed better at attended locations and this advantage increased with difficulty, consistent with data from human psychophysics. Neuronal modulation by spatial attention was larger with greater difficulty. In two animals, increasing difficulty caused a modest increase in neuronal responses to visual stimuli regardless of the locus of spatial attention. In a third animal, which was previously trained to ignore multiple distracting stimuli, increasing task difficulty increased responses at the focus of attention and suppressed responses away from the focus of attention. The results show that difficulty can modulate effects of spatial attention in V4; it can alter the distribution of sensory responses across the visual scene in ways that may depend on the subject's behavioral strategy.     

Impaired distractor inhibition on a selective attention task in unmedicated, depressed subjects

BACKGROUND: Impaired distractor inhibition may contribute to the selective attention deficits observed in depressed patients, but studies to date have not tested the distractor inhibition theory against the possibility that processes such as transient memory review processes may account for the observed deficits. A negative priming paradigm can dissociate inhibition from such a potentially confounding process called object review. The negative priming task also isolates features of the distractor such as colour and location for independent examination. METHOD: A computerized negative priming task was used in which colour, identification and location features of a stimulus and distractor were systematically manipulated across successive prime and probe trials. Thirty-two unmedicated subjects with DSM-IV diagnoses of non-psychotic unipolar depression were compared with 32 age, sex and IQ matched controls. RESULTS: Depressed subjects had reduced levels of negative priming for conditions where the colour feature of the stimulus was repeated across prime and probe trials but not when identity or location was the repeated feature. When both the colour and location feature were the repeated feature across trials, facilitation in response was apparent. CONCLUSIONS: The pattern of results supports studies that found reduced distractor inhibition in depressed subjects, and suggests that object review is intact in these subjects. Greater impairment in negative priming for colour versus location suggests that subjects may have greater impairment in the visual stream associated with processing colour features.     

Automatic spread of attentional response modulation along Gestalt criteria in primary visual cortex

Visual attention can select spatial locations, features and objects. Theories of object-based attention claim that attention enhances the representation of all parts of an object, even parts that are not task relevant. We recorded neuronal activity in area V1 of macaque monkeys and observed an automatic spread of attention to image elements outside of the attentional focus when they were bound to an attended stimulus by Gestalt criteria.     

Preparatory activity in visual cortex indexes distractor suppression during covert spatial orienting

The deployment of spatial attention induces retinotopically specific increases in neural activity that occur even before a target stimulus is presented. Although this preparatory activity is thought to prime the attended regions, thereby improving perception and recognition, it is not yet clear whether this activity is a manifestation of signal enhancement at the attended locations or suppression of interference from distracting stimuli (or both). We investigated the functional role of these preparatory shifts by isolating a distractor suppression component of selection. Behavioral data have shown that manipulating the probability that visual distractors will appear modulates distractor suppression without concurrent changes in signal enhancement. In 2 experiments, functional magnetic resonance imaging revealed increased cue-evoked activity in retinotopically specific regions of visual cortex when increased distractor suppression was elicited by a high probability of distractors. This finding directly links cue-evoked preparatory activity in visual cortex with a distractor suppression component of visual selective attention.     

Visual attention in the occipitotemporal processing stream of the macaque

Abstract

The occipitotemporal cortical areas of the macaque monkey are known to be important for normal object recognition processes, but comparatively little effort has gone into investigations of the role of these areas in selective attention to objects. In this paper we review the behavioural and electrophysiological evidence, which suggests that the occipitotemporal areas are also important for selective attention to recognisable objects. Areas V4 and IT are seen to be involved in aspects of selective attention driven by the spatial location of the attended object, features of objects, the relevance of a stimulus to a particular task, and the amount of sustained attention required to perform a task. The superior temporal polysensory area (STPa) is an area usually thought of as a component of the temporal processing stream. However, the evidence reviewed here shows that one role of area STPa is to decode the direction of others' attention, a function which requires that the region accesses information from both of the major corticocortical processing streams.     

Are visual stimuli sufficient to evoke motor information?: Studies with hand primes

In two experiments we assessed whether seeing objects automatically activates information regarding how to manipulate them. In Experiment 1 participants categorized photographs of objects that could be manipulated either with a power or a precision grip into artefacts or natural kinds. Target-objects were preceded by primes consisting of photographs of hands in grasping postures (precision or power grip). Experiment 2 involved a preliminary motor training phase in which each visual prime was associated with the actual motor action. In both experiments, natural kinds graspable with a power grip produced the fastest responses. In Experiment 2 we also found a congruency effect between the prime and the kind of grip required by the object (precision, power). Results suggest that visual stimuli automatically activate motor information. Specific motor programs are, however, activated only if motor training is performed before the categorization task. Implications of the results for the understanding of the organization of conceptual and motor information in the brain are discussed.     

Cross-modal links in endogenous spatial attention are mediated by common external locations: evidence from event-related brain potentials

Recent behavioural and event-related potential (ERP) studies reported cross-modal links in spatial attention between vision, audition and touch. Such links could reflect differences in hemispheric-activation levels associated with spatial attention to one side, or more abstract spatial reference-frames mediating selectivity across modalities. To distinguish these hypotheses, ERPs were recorded to lateral tactile stimuli, plus visual (experiment 1) or auditory stimuli (experiment 2), while participants attended to the left or right hand to detect infrequent tactile targets, and ignored other modalities. In separate blocks, hands were either in a crossed or uncrossed posture. With uncrossed hands, visual stimuli on the tactually attended side elicited enhanced N1 and P2 components at occipital sites, and an enhanced negativity at midline electrodes, reflecting cross-modal links in spatial attention from touch to vision. Auditory stimuli at tactually attended locations elicited an enhanced negativity overlapping with the N1 component, reflecting cross-modal links from touch to audition. An analogous pattern of results arose for crossed hands, with tactile attention enhancing auditory or visual responses on the side where the attended hand now lay (i.e. in the opposite visual or auditory hemifield to that enhanced by attending the same hand when uncrossed). This suggests that cross-modal attentional links are not determined by hemispheric projections, but by common external locations. Unexpectedly, somatosensory ERPs were strongly affected by hand posture in both experiments, with attentional effects delayed and smaller for crossed hands. This may reflect the combined influence of anatomical and external spatial codes within the tactile modality, while cross-modal links depend only on the latter codes. Electronic Publication