Distractor-target interactions during directed visual attention

The spatial extent of directed visual attention (DVA) was examined in a series of experiments using precuing in a suprathreshold luminance detection (reaction time) paradigm. Previous findings (Hughes, H. C. and Zimba, L. D. J. Exp. Psychol.; Human Percept Perf., 1985, 11, 409-430) indicated that, in an empty visual field, the effects of DVA were primarily manifest as a uniform elevation of response times to all probe targets in the hemifield contralateral to the observer's expectancy. The present experiments were designed to determine whether increased spatial selectivity could be found when luminous markers indicated the exact location of the expected visual target. To maintain equivalent states of adaptation in both hemifields, luminous markers were also present at the same location in the contralateral hemifield. In general, hemifield effects were again obtained, but with two notable exceptions. First, marking locations in the unattended hemifield produced a local increase (enhanced interference) in RTs above the level characteristic of other locations within that hemifield. Second, when multiple locations were indicated with identical luminous markers, graded costs were obtained in both hemifields. However, scaling the markers according to estimates of cortical magnification factor (M) substantially reduced the slope of these inhibitory gradients, and the results once again approached those characteristic of an unstructured visual field. The findings suggest that when attention is directed to a marked location along the horizontal meridian, a transition in performance typically occurs at the vertical meridian. In addition, irrelevant stimuli some distance from the attentional focus interfere with detection times to unexpected targets that appear in the same vicinity. This interference may relate to an enhanced susceptibility to spatial interactions between the distractors and target away from the attentional focus. The interference appears to extend over a constant area of visual cortex, since it is reduced when the markers are M-scaled.     

Dynamic spatial coding within the dorsal frontoparietal network during a visual search task

To what extent are the left and right visual hemifields spatially coded in the dorsal frontoparietal attention network? In many experiments with neglect patients, the left hemisphere shows a contralateral hemifield preference, whereas the right hemisphere represents both hemifields. This pattern of spatial coding is often used to explain the right-hemispheric dominance of lesions causing hemispatial neglect. However, pathophysiological mechanisms of hemispatial neglect are controversial because recent experiments on healthy subjects produced conflicting results regarding the spatial coding of visual hemifields. We used an fMRI paradigm that allowed us to distinguish two attentional subprocesses during a visual search task. Either within the left or right hemifield subjects first attended to stationary locations (spatial orienting) and then shifted their attentional focus to search for a target line. Dynamic changes in spatial coding of the left and right hemifields were observed within subregions of the dorsal front-parietal network: During stationary spatial orienting, we found the well-known spatial pattern described above, with a bilateral hemifield representation in the right hemisphere and a contralateral preference in the left hemisphere. However, during search, the right hemisphere had a contralateral preference and the left hemisphere equally represented both hemifields. This finding leads to novel perspectives regarding models of visuospatial attention and hemispatial neglect.     

Electrical Neuroimaging Reveals Timing of Attentional Control Activity in Human Brain

Voluntarily shifting attention to a location of the visual field improves the perception of events that occur there. Regions of frontal cortex are thought to provide the top-down control signal that initiates a shift of attention, but because of the temporal limitations of functional brain imaging, the timing and sequence of attentional-control operations remain unknown. We used a new analytical technique (beamformer spatial filtering) to reconstruct the anatomical sources of low-frequency brain waves in humans associated with attentional control across time. Following a signal to shift attention, control activity was seen in parietal cortex 100–200 ms before activity was seen in frontal cortex. Parietal cortex was then reactivated prior to anticipatory biasing of activity in occipital cortex. The magnitudes of early parietal activations were strongly predictive of the degree of attentional improvement in perceptual performance. These results show that parietal cortex, not frontal cortex, provides the initial signals to shift attention and indicate that top-down attentional control is not purely top down.     

Bilateral field advantage in visual enumeration

A number of recent studies have demonstrated superior visual processing when the information is distributed across the left and right visual fields than if the information is presented in a single hemifield (the bilateral field advantage). This effect is thought to reflect independent attentional resources in the two hemifields and the capacity of the neural responses to the left and right hemifields to process visual information in parallel. Here, we examined whether a bilateral field advantage can also be observed in a high-level visual task that requires the information from both hemifields to be combined. To this end, we used a visual enumeration task--a task that requires the assimilation of separate visual items into a single quantity--where the to-be-enumerated items were either presented in one hemifield or distributed between the two visual fields. We found that enumerating large number (>4 items), but not small number (<4 items), exhibited the bilateral field advantage: enumeration was more accurate when the visual items were split between the left and right hemifields than when they were all presented within the same hemifield. Control experiments further showed that this effect could not be attributed to a horizontal alignment advantage of the items in the visual field, or to a retinal stimulation difference between the unilateral and bilateral displays. These results suggest that a bilateral field advantage can arise when the visual task involves inter-hemispheric integration. This is in line with previous research and theory indicating that, when the visual task is attentionally demanding, parallel processing by the neural responses to the left and right hemifields can expand the capacity of visual information processing.     

Eye position affects orienting of visuospatial attention

The ability to detect an incoming visual stimulus is enhanced by knowledge of stimulus location (orienting of visuospatial attention). Although the brain mechanisms at the basis of this enhancement are not yet fully clarified, there is evidence that orienting of attention is accompanied by the activation of oculomotor circuits. It remains unclear, however, whether this oculomotor activity is an epiphenomenon or is functionally related to the attentional process. Attentional benefits are usually measured by the classical Posner paradigm. When subjects fixate centrally and are requested to detect a visual stimulus that could appear in an attended or unattended location, they react faster to stimuli appearing in the attended one. Here, we demonstrate that in monocular vision visuospatial attention was significantly modulated by the position of the eye in the orbit. When the screen was placed 40 degrees to the right or to the left of subjects' sagittal plane, attentional benefits for stimuli appearing in subjects' temporal spatial hemifield dramatically decayed, even if the retinal stimulation was exactly the same as in the classical paradigm. The finding that eyes and attention show a common limit stop point supports their close functional coupling.     

A Population Rate Code of Auditory Space in the Human Cortex

Background

Previous work on the human auditory cortex has revealed areas specialized in spatial processing but how the neurons in these areas represent the location of a sound source remains unknown.

Methodology/Principal Findings

Here, we performed a magnetoencephalography (MEG) experiment with the aim of revealing the neural code of auditory space implemented by the human cortex. In a stimulus-specific adaptation paradigm, realistic spatial sound stimuli were presented in pairs of adaptor and probe locations. We found that the attenuation of the N1m response depended strongly on the spatial arrangement of the two sound sources. These location-specific effects showed that sounds originating from locations within the same hemifield activated the same neuronal population regardless of the spatial separation between the sound sources. In contrast, sounds originating from opposite hemifields activated separate groups of neurons.

Conclusions/Significance

These results are highly consistent with a rate code of spatial location formed by two opponent populations, one tuned to locations in the left and the other to those in the right. This indicates that the neuronal code of sound source location implemented by the human auditory cortex is similar to that previously found in other primates.     

Transfer of Learning between Hemifields in Multiple Object Tracking: Memory Reduces Constraints of Attention

Many tasks involve tracking multiple moving objects, or stimuli. Some require that individuals adapt to changing or unfamiliar conditions to be able to track well. This study explores processes involved in such adaptation through an investigation of the interaction of attention and memory during tracking. Previous research has shown that during tracking, attention operates independently to some degree in the left and right visual hemifields, due to putative anatomical constraints. It has been suggested that the degree of independence is related to the relative dominance of processes of attention versus processes of memory. Here we show that when individuals are trained to track a unique pattern of movement in one hemifield, that learning can be transferred to the opposite hemifield, without any evidence of hemifield independence. However, learning is not influenced by an explicit strategy of memorisation of brief periods of recognisable movement. The findings lend support to a role for implicit memory in overcoming putative anatomical constraints on the dynamic, distributed spatial allocation of attention involved in tracking multiple objects.     

Transcranial magnetic stimulation reveals attentional feedback to area V1 during serial visual search

Visual search tasks have been used to understand how, where and when attention influences visual processing. Current theories suggest the involvement of a high-level "saliency map" that selects a candidate location to focus attentional resources. For a parallel (or "pop-out") task, the first chosen location is systematically the target, but for a serial (or "difficult") task, the system may cycle on a few distractors before finally focusing on the target. This implies that attentional effects upon early visual areas, involving feedback from higher areas, should be visible at longer latencies during serial search. A previous study from Juan & Walsh (2003) had used Transcranial Magnetic Stimulation (TMS) to support this conclusion; however, only a few post-stimulus delays were compared, and no control TMS location was used. Here we applied TMS double-pulses (sub-threshold) to induce a transient inhibition of area V1 at every post-stimulus delay between 100 ms and 500 ms (50 ms steps). The search array was presented either at the location affected by the TMS pulses (previously identified by applying several pulses at supra-threshold intensity to induce phosphene perception), or in the opposite hemifield, which served as a retinotopically-defined control location. Two search tasks were used: a parallel (+ among Ls) and a serial one (T among Ls). TMS specifically impaired the serial, but not the parallel search. We highlight an involvement of V1 in serial search 300 ms after the onset; conversely, V1 did not contribute to parallel search at delays beyond 100 ms. This study supports the idea that serial search differs from parallel search by the presence of additional cycles of a select-and-focus iterative loop between V1 and higher-level areas.     

Temporal Dynamics of Visual Attention Measured with Event-Related Potentials

How attentional modulation on brain activities determines behavioral performance has been one of the most important issues in cognitive neuroscience. This issue has been addressed by comparing the temporal relationship between attentional modulations on neural activities and behavior. Our previous study measured the time course of attention with amplitude and phase coherence of steady-state visual evoked potential (SSVEP) and found that the modulation latency of phase coherence rather than that of amplitude was consistent with the latency of behavioral performance. In this study, as a complementary report, we compared the time course of visual attention shift measured by event-related potentials (ERPs) with that by target detection task. We developed a novel technique to compare ERPs with behavioral results and analyzed the EEG data in our previous study. Two sets of flickering stimulus at different frequencies were presented in the left and right visual hemifields, and a target or distracter pattern was presented randomly at various moments after an attention-cue presentation. The observers were asked to detect targets on the attended stimulus after the cue. We found that two ERP components, P300 and N2pc, were elicited by the target presented at the attended location. Time-course analyses revealed that attentional modulation of the P300 and N2pc amplitudes increased gradually until reaching a maximum and lasted at least 1.5 s after the cue onset, which is similar to the temporal dynamics of behavioral performance. However, attentional modulation of these ERP components started later than that of behavioral performance. Rather, the time course of attentional modulation of behavioral performance was more closely associated with that of the concurrently recorded SSVEPs analyzed. These results suggest that neural activities reflected not by either the P300 or N2pc, but by the SSVEPs, are the source of attentional modulation of behavioral performance.     

Specific contributions of ventromedial, anterior cingulate, and lateral prefrontal cortex for attentional selection and stimulus valuation

Attentional control ensures that neuronal processes prioritize the most relevant stimulus in a given environment. Controlling which stimulus is attended thus originates from neurons encoding the relevance of stimuli, i.e. their expected value, in hand with neurons encoding contextual information about stimulus locations, features, and rules that guide the conditional allocation of attention. Here, we examined how these distinct processes are encoded and integrated in macaque prefrontal cortex (PFC) by mapping their functional topographies at the time of attentional stimulus selection. We find confined clusters of neurons in ventromedial PFC (vmPFC) that predominantly convey stimulus valuation information during attention shifts. These valuation signals were topographically largely separated from neurons predicting the stimulus location to which attention covertly shifted, and which were evident across the complete medial-to-lateral extent of the PFC, encompassing anterior cingulate cortex (ACC), and lateral PFC (LPFC). LPFC responses showed particularly early-onset selectivity and primarily facilitated attention shifts to contralateral targets. Spatial selectivity within ACC was delayed and heterogeneous, with similar proportions of facilitated and suppressed responses during contralateral attention shifts. The integration of spatial and valuation signals about attentional target stimuli was observed in a confined cluster of neurons at the intersection of vmPFC, ACC, and LPFC. These results suggest that valuation processes reflecting stimulus-specific outcome predictions are recruited during covert attentional control. Value predictions and the spatial identification of attentional targets were conveyed by largely separate neuronal populations, but were integrated locally at the intersection of three major prefrontal areas, which may constitute a functional hub within the larger attentional control network.     

Spatial and Temporal Attention Modulate the Early Stages of Face Processing: Behavioural Evidence from a Reaching Paradigm

A presently unresolved question within the face perception literature is whether attending to the location of a face modulates face processing (i.e. spatial attention). Opinions on this matter diverge along methodological lines – where neuroimaging studies have observed that the allocation of spatial attention serves to enhance the neural response to a face, findings from behavioural paradigms suggest face processing is carried out independently of spatial attention. In the present study, we reconcile this divide by using a continuous behavioural response measure that indexes face processing at a temporal resolution not available in discrete behavioural measures (e.g. button press). Using reaching trajectories as our response measure, we observed that although participants were able to process faces both when attended and unattended (as others have found), face processing was not impervious to attentional modulation. Attending to the face conferred clear benefits on sex-classification processes at less than 350ms of stimulus processing time. These findings constitute the first reliable demonstration of the modulatory effects of both spatial and temporal attention on face processing within a behavioural paradigm.     

Category learning induces position invariance of pattern recognition across the visual field

Human object recognition is considered to be largely invariant to translation across the visual field. However, the origin of this invariance to positional changes has remained elusive, since numerous studies found that the ability to discriminate between visual patterns develops in a largely location-specific manner, with only a limited transfer to novel visual field positions. In order to reconcile these contradicting observations, we traced the acquisition of categories of unfamiliar grey-level patterns within an interleaved learning and testing paradigm that involved either the same or different retinal locations. Our results show that position invariance is an emergent property of category learning. Pattern categories acquired over several hours at a fixed location in either the peripheral or central visual field gradually become accessible at new locations without any position-specific feedback. Furthermore, categories of novel patterns presented in the left hemifield are distinctly faster learnt and better generalized to other locations than those learnt in the right hemifield. Our results suggest that during learning initially position-specific representations of categories based on spatial pattern structure become encoded in a relational, position-invariant format. Such representational shifts may provide a generic mechanism to achieve perceptual invariance in object recognition.     

The Role of Right Inferior Parietal Cortex in Auditory Spatial Attention: A Repetitive Transcranial Magnetic Stimulation Study

Behavioral studies support the concept of an auditory spatial attention gradient by demonstrating that attentional benefits progressively diminish as distance increases from an attended location. Damage to the right inferior parietal cortex can induce a rightward attention bias, which implicates this region in the construction of attention gradients. This study used event-related potentials (ERPs) to define attention-related gradients before and after repetitive transcranial magnetic stimulation (rTMS) to the right inferior parietal cortex. Subjects (n = 16) listened to noise bursts at five azimuth locations (left to right: -90°, -45°, 0° midline, +45°, +90°) and responded to stimuli at one target location (-90°, +90°, separate blocks). ERPs as a function of non-target location were examined before (baseline) and after 0.9 Hz rTMS. Results showed that ERP attention gradients were observed in three time windows (frontal 230–340, parietal 400–460, frontal 550–750 ms). Significant transient rTMS effects were seen in the first and third windows. The first window had a voltage decrease at the farthest location when attending to either the left or right side. The third window had on overall increase in positivity, but only when attending to the left side. These findings suggest that rTMS induced a small contraction in spatial attention gradients within the first time window. The asymmetric effect of attended location on gradients in the third time window may relate to neglect of the left hemispace after right parietal injury. Together, these results highlight the role of the right inferior parietal cortex in modulating frontal lobe attention network activity.     

Feature-based attention increases the selectivity of population responses in primate visual cortex

BACKGROUND: Attending to the spatial location or to nonspatial features of visual stimuli can modulate neuronal responses in primate visual cortex. The modulation by spatial attention changes the gain of sensory neurons and strengthens the representation of attended locations without changing neuronal selectivities such as directionality, i.e., the ratio of responses to preferred and anti-preferred directions of motion. Whether feature-based attention acts in a similar manner is unknown. RESULTS: To clarify this issue, we recorded the responses of 135 direction-selective neurons in the middle temporal area (MT) of two macaques to an unattended moving random dot pattern (the distractor) positioned inside a neuron's receptive field while the animals attended to a second moving pattern positioned in the opposite hemifield. Responses to different directions of the distractor were modulated by the same factor (approximately 12%) as long as the attended direction remained unchanged. On the other hand, systematically changing the attended direction from a neuron's preferred to its anti-preferred direction caused a systematic change of the attentional modulation from an enhancement to a suppression, increasing directionality by about 20%. CONCLUSIONS: The results show that (1) feature-based attention exerts a multiplicative modulation upon neuronal responses and that the strength of this modulation depends on the similarity between the attended feature and the cell's preferred feature, in line with the feature-similarity gain model, and (2) at the level of the neuronal population, feature-based attention increases the selectivity for attended features by increasing the responses of neurons preferring this feature value while decreasing responses of neurons tuned to the opposite feature value.     

Modulation of backward pattern masking by focal visual attention

The effect of focal visual attention on backward pattern masking was investigated using an orientation discrimination task. The results show that attention reduces primarily the effect of interruption masking, the later component of pattern masking, which occurs when the delay between the target and mask onset is about 50-150 ms. The strongest spatial cueing effect, i.e. the strongest reduction of the orientation discrimination threshold due to focal attention, was observed at intermediate (approximately 100 ms) target-to-mask stimulus onset asynchrony (SOA). There was a weak effect of cueing at shorter SOAs, and no or a very weak attentional effect was present at longer target-to-mask SOAs, where the pattern masking effect is absent. The dynamics of attentional modulation of backward pattern masking correlates closely with the dynamics of the attentional modulation of neuronal responses in the early visual cortex.     

Visual search in peripheral vision: learning effects and set-size dependence.

Feature search for a light bar with one orientation (or color) embedded in an array of bars with a very different orientation (or color) is quick, easy and independent of the number of array elements. In contrast, search for a conjunction target has a linear response time dependence on the number of distractors. Training can improve performance of both these tasks. We report that these properties may not be valid for eccentric stimulus presentation. In general, the two hemifields are not equally suited to search, and training is most effective in the weaker hemifield. In addition, the feature-search independence of set-size may not always be valid for stimulus arrays that are presented peripherally. Subjects were tested on orientation and color feature tasks, and on orientation-color conjunction search with 3 array sizes presented at fixation or eccentrically in the right or left hemifield. During a second testing session, improvement was so much greater for the non-preferred hemifield that sometimes the preference was switched. Surprisingly, preferred hemifield performance actually declined for some subjects. Thus, the hemifield preference effect seems related to competition, and perhaps an automatic attention-directing mechanism. We confirmed the central presentation set-size independence for feature search but found a great difference between large and small arrays when presentation was lateral. There are two sources of this array size effect: 1. Target eccentricity, demonstrated by comparing performance for different target locations with the same array size. 2. Target location uncertainty, seen by comparing performance for different size arrays when the target elements appeared at the same locations. Training also affected the array-size dependence, changing search performance from set-size dependent to independent or vice versa at the point of greatest training effect.     

Mechanisms and asymmetries in visual perception of simultaneity and temporal order

Temporally overlapping, spatially separated visual stimuli were used for studying perception of simultaneity and temporal order. Pairs of flashes each of 100 ms duration were presented with stimulus onset asynchronies of 0, 30, 50, and 70 ms. Three spatial arrangements of flash presentation were tested: 1) both flashes were presented foveally; 2) one flash was presented foveally and the other at 9 deg in the left visual hemifield; 3) one flash was presented foveally and the other at 8 deg in the right visual hemifield. Onset asynchronies of 30 and 50 ms were not sufficient for correct identification of temporal order although the flashes were not perceived as simultaneous. Analysis of the response distributions suggests the existence of two-independent mechanisms for evaluating temporal interrelations: one for detecting simultaneity and the other for identifying temporal order. A better detection of simultaneity was found when synchroneous flashes were presented together with pairs of flashes separated by larger onset asynchronies. Reading habits may explain only part of the left-right asymmetries of the response distributions. The possible lateralization of the two suggested mechanisms within the cerebral hemispheres is discussed.     

Cross-modal links in spatial attention.

A great deal is now known about the effects of spatial attention within individual sensory modalities, especially for vision and audition. However, there has been little previous study of possible cross-modal links in attention. Here, we review recent findings from our own experiments on this topic, which reveal extensive spatial links between the modalities. An irrelevant but salient event presented within touch, audition, or vision, can attract covert spatial attention in the other modalities (with the one exception that visual events do not attract auditory attention when saccades are prevented). By shifting receptors in one modality relative to another, the spatial coordinates of these cross-modal interactions can be examined. For instance, when a hand is placed in a new position, stimulation of it now draws visual attention to a correspondingly different location, although some aspects of attention do not spatially remap in this way. Cross-modal links are also evident in voluntary shifts of attention. When a person strongly expects a target in one modality (e.g. audition) to appear in a particular location, their judgements improve at that location not only for the expected modality but also for other modalities (e.g. vision), even if events in the latter modality are somewhat more likely elsewhere. Finally, some of our experiments suggest that information from different sensory modalities may be integrated preattentively, to produce the multimodal internal spatial representations in which attention can be directed. Such preattentive cross-modal integration can, in some cases, produce helpful illusions that increase the efficiency of selective attention in complex scenes.     

Effects of cholinergic enhancement on visual stimulation, spatial attention, and spatial working memory

We compared behavioral and neural effects of cholinergic enhancement between spatial attention, spatial working memory (WM), and visual control tasks, using fMRI and the anticholinesterase physostigmine. Physostigmine speeded responses nonselectively but increased accuracy selectively for attention. Physostigmine also decreased activations to visual stimulation across all tasks within primary visual cortex, increased extrastriate occipital cortex activation selectively during maintained attention and WM encoding, and decreased parietal activation selectively during maintained attention. Finally, lateralization of occipital activation as a function of the visual hemifield toward which attention or memory was directed was decreased under physostigmine. In the case of attention, this effect correlated strongly with a decrease in a behavioral measure of selective spatial processing. Our results suggest that, while cholinergic enhancement facilitates visual attention by increasing activity in extrastriate cortex generally, it accomplishes this in a manner that reduces expectation-driven selective biasing of extrastriate cortex.