Remapping attentional priorities: differential contribution of superior parietal lobule and intraparietal sulcus

Seeking and selectively attending to significant extrapersonal stimuli in a dynamic environment requires the updating of an attentional priority map. Using functional magnetic resonance imaging, we investigated the role of posterior parietal cortex in such remappings of attentional priorities where the configuration, location, and significance of stimuli were systematically varied. Our data revealed a functional dissociation between 2 juxtaposed posterior parietal regions: one in the superior parietal lobule (SPL) and another in the intraparietal sulcus (IPS). SPL was preferentially activated in all conditions where a spatial displacement occurred in the location of the target, the location of the distracter, or the focus of attention (exogenous and endogenous shifts of spatial attention). Shifts of the attentional focus also activated the IPS but principally if they were guided endogenously by internal rules of relevance rather than stimulus displacement per se (endogenous attention shifts). Only the IPS region was activated by transient resetting of target significance when the stimulus configuration changed but the attentional focus remained spatially fixed (feature attention shifts). These 2 components of the large-scale frontoparietal spatial attention network therefore have common and distinctive functions. In specific, the IPS component is more closely related to the compilation of an attentional priority map, including the endogenous recalibration of attentional weights. The SPL component, on the other hand, is more closely related to the modification of spatial coordinates linked to attentional priorities (spatial shifting). Collectively, these 2 areas allow posterior parietal cortex to dynamically encode extrapersonal events according to their spatial coordinates and valence.     

Attentional load and sensory competition in human vision: modulation of fMRI responses by load at fixation during task-irrelevant stimulation in the peripheral visual field

Perceptual suppression of distractors may depend on both endogenous and exogenous factors, such as attentional load of the current task and sensory competition among simultaneous stimuli, respectively. We used functional magnetic resonance imaging (fMRI) to compare these two types of attentional effects and examine how they may interact in the human brain. We varied the attentional load of a visual monitoring task performed on a rapid stream at central fixation without altering the central stimuli themselves, while measuring the impact on fMRI responses to task-irrelevant peripheral checkerboards presented either unilaterally or bilaterally. Activations in visual cortex for irrelevant peripheral stimulation decreased with increasing attentional load at fixation. This relative decrease was present even in V1, but became larger for successive visual areas through to V4. Decreases in activation for contralateral peripheral checkerboards due to higher central load were more pronounced within retinotopic cortex corresponding to 'inner' peripheral locations relatively near the central targets than for more eccentric 'outer' locations, demonstrating a predominant suppression of nearby surround rather than strict 'tunnel vision' during higher task load at central fixation. Contralateral activations for peripheral stimulation in one hemifield were reduced by competition with concurrent stimulation in the other hemifield only in inferior parietal cortex, not in retinotopic areas of occipital visual cortex. In addition, central attentional load interacted with competition due to bilateral versus unilateral peripheral stimuli specifically in posterior parietal and fusiform regions. These results reveal that task-dependent attentional load, and interhemifield stimulus-competition, can produce distinct influences on the neural responses to peripheral visual stimuli within the human visual system. These distinct mechanisms in selective visual processing may be integrated within posterior parietal areas, rather than earlier occipital cortex.     

Brain mechanisms mediating auditory attentional capture in humans

The ability to detect and preferentially process salient auditory stimuli, even when irrelevant to a current task, is often critical for adaptive behavior. This stimulus-driven allocation of processing resources is known as "attentional capture." Here we used functional magnetic resonance imaging in humans to investigate brain activity and behavioral effects related to such auditory attentional capture. Participants searched a sequence of tones for a target tone that was shorter or longer than the nontarget tones. An irrelevant singleton feature in the tone sequence resulted in behavioral interference (attentional capture) and activation of parietal and prefrontal cortices only when the singleton was associated with a nontarget tone (nontarget singleton) and not when associated with a target tone (target singleton). In contrast, the presence (vs. absence) of a singleton feature in the sequence was associated with activation of frontal and temporal loci previously associated with auditory change detection. These results suggest that a ventral network involving superior temporal and inferior frontal cortices responds to acoustic variability, regardless of attentional significance, but a dorsal frontoparietal network responds only when a feature singleton captures attention.     

Reflexive orienting in spatial neglect is biased towards behaviourally salient stimuli

Patients with spatial neglect are impaired when detecting contralesional targets presented shortly after an ipsilesional cue. This "disengagement" deficit is believed to reflect reflexive orienting towards ipsilesional stimuli that is independent of behavioural goals. Here, we show that the extent of this spatial bias depends on the behavioural salience of ipsilesional stimuli. Healthy participants, brain-injured patients without neglect and neglect patients reacted to ipsilesional and contralesional visual targets. Prior to target presentation, a visual cue similar or dissimilar to the target was presented at target position or opposite the target. Although participants did not react to the similar cue, it had high behavioural salience since it shared features with the target stimulus. Neglect patients showed dramatically increased reaction times to contralesional targets, but only when these followed behaviourally relevant ipsilesional cues. No decrease of performance was observed with irrelevant cues. This performance pattern was not due to perceptual similarity, since the same effect was found when cue and target were semantically related but differed perceptually. Importantly, semantically related cues ceased to attract attention when they were defined as behaviourally irrelevant. These results show that neglect patients only orient attention reflexively towards ipsilesional stimuli with high behavioural salience.     

Attention modulates gamma-band oscillations differently in the human lateral occipital cortex and fusiform gyrus

We studied the existence, localization and attentional modulation of gamma-band oscillatory activity (30-130 Hz) in the human intracranial region. Two areas known to play a key role in visual object processing: the lateral occipital (LO) cortex and the fusiform gyrus. These areas consistently displayed large gamma oscillations during visual stimulus encoding, while other extrastriate areas remained systematically silent, across 14 patients and 291 recording sites scattered throughout extrastriate visual cortex. The lateral extent of the responsive regions was small, in the range of 5 mm. Induced gamma oscillations and evoked potentials were not systematically co-localized. LO and the fusiform gyrus displayed markedly different patterns of attentional modulation. In the fusiform gyrus, attention enhanced stimulus-driven gamma oscillations. In LO, attention increased the baseline level of gamma oscillations during the expectation period preceding the stimulus. Subsequent gamma oscillations produced by attended stimuli were smaller than those produced by unattended, irrelevant stimuli. Attentional modulations of gamma oscillations in LO and the fusiform gyrus were thus very different, both in their time-course (preparatory period and/or stimulus processing) and direction of modulation (increase or decrease). Our results thus suggest that the functional role of gamma oscillations depends on the area in which they occur.     

Neural system for controlling the contents of object working memory in humans

Working memory (WM), the active maintenance of currently relevant information, is a flexible system allowing for fast and frequent goal-directed changes of rehearsed information. Successful WM maintenance prevents interference from distracting stimuli while allowing new task-relevant information to update the contents of WM. We used functional magnetic resonance imaging to show that when WM contents were updated, regardless of stimulus type (faces or houses), a frontoparietal network showed transient increases in activation. Some of these regions are highly similar to those identified in studies of shifting attention, supporting the idea that updating WM involves a change in the attentional priority afforded to the current perceptual input. A region within the mid-ventrolateral prefrontal cortex, near the junction of the inferior frontal sulcus and precentral sulcus (inferior frontal junction), that has previously been implicated in cognitive control, demonstrated transient increases in activity during updating as well as sustained maintenance activity. A more anterior prefrontal region, middle frontal gyrus, previously implicated in protecting the contents of WM from interfering stimuli during maintenance, demonstrated transient increases in activity during updating. The current study suggests that updating WM results from a combination of increased attention to the visual stimulus and a change in the system's interference protection state.     

The spatial attention network interacts with limbic and monoaminergic systems to modulate motivation-induced attention shifts

How does the human brain integrate information from multiple domains to guide spatial attention according to motivational needs? To address this question, we measured hemodynamic responses to central cues predicting locations of peripheral attentional targets (food or tool images) in a novel covert spatial attention paradigm. The motivational relevance of food-related attentional targets was experimentally manipulated via hunger and satiety. Amygdala, posterior cingulate, locus coeruleus, and substantia nigra showed selective sensitivity to food-related cues when hungry but not when satiated, an effect that did not generalize to tools. Posterior parietal cortex (PPC), including intraparietal sulcus, posterior cingulate, and the orbitofrontal cortex displayed correlations with the speed of attentional shifts that were sensitive not just to motivational state but also to the motivational value of the target. Stronger functional coupling between PPC and posterior cingulate occurred during attentional biasing toward motivationally relevant food targets. These results reveal conjoint limbic and monoaminergic encoding of motivational salience in spatial attention. They emphasize the interactive role of posterior parietal and cingulate cortices in integrating motivational information with spatial attention, a process that is critical for selective allocation of attentional resources in an environment where target position and relevance can change rapidly.     

Top-down controlled visual dimension weighting: an event-related fMRI study

Target detection in visual singleton feature search is slowed when consecutive targets are defined in different visual dimensions. Behavioral data provide evidence that attentional weight needs to be shifted between dimension-specific processing modules. We found similar dimension-specific change effects in a conjunction search task, in which observers searched for an odd-one-out target defined by a unique combination of size and color or, respectively, size and motion direction. Changes of the secondary target dimension (color or motion) across trials, but not target feature changes within a dimension, increased the time required to detect the target. Dimensional change costs were greatly increased for singleton conjunction search compared to singleton feature search. This suggests involvement of top-down control processes in dimensional change in conjunction search, in contrast to stimulus-driven dimensional change in singleton feature search. The functional anatomical correlates of top-down controlled visual dimension changes were investigated in two event-related functional magnetic resonance imaging (fMRI) experiments. In Experiment 1, dimensional change in singleton conjunction search was accompanied by transient activations in a fronto-posterior network of brain areas that was largely non-overlapping with the general network activated during visual search. Experiment 2, which contrasted singleton feature and conjunction search within the same session, revealed a double dissociation in anterior prefrontal cortex: left frontopolar cortex was selectively involved in stimulus-driven dimension changes but not in top-down controlled dimension changes, whereas the reverse was observed in frontomedian cortex.     

Retinotopy and attention in human occipital, temporal, parietal, and frontal cortex

Novel mapping stimuli composed of biological motion figures were used to study the extent and layout of multiple retinotopic regions in the entire human brain and to examine the independent manipulation of retinotopic responses by visual stimuli and by attention. A number of areas exhibited retinotopic activations, including full or partial visual field representations in occipital cortex, the precuneus, motion-sensitive temporal cortex (extending into the superior temporal sulcus), the intraparietal sulcus, and the vicinity of the frontal eye fields in frontal cortex. Early visual areas showed mainly stimulus-driven retinotopy; parietal and frontal areas were driven primarily by attention; and lateral temporal regions could be driven by both. We found clear spatial specificity of attentional modulation not just in early visual areas but also in classical attentional control areas in parietal and frontal cortex. Indeed, strong spatiotopic activity in these areas could be evoked by directed attention alone. Conversely, motion-sensitive temporal regions, while exhibiting attentional modulation, also responded significantly when attention was directed away from the retinotopic stimuli.     

Neural basis for priming of pop-out during visual search revealed with fMRI

Maljkovic and Nakayama first showed that visual search efficiency can be influenced by priming effects. Even "pop-out" targets (defined by unique color) are judged quicker if they appear at the same location and/or in the same color as on the preceding trial, in an unpredictable sequence. Here, we studied the potential neural correlates of such priming in human visual search using functional magnetic resonance imaging (fMRI). We found that repeating either the location or the color of a singleton target led to repetition suppression of blood oxygen level-dependent (BOLD) activity in brain regions traditionally linked with attentional control, including bilateral intraparietal sulci. This indicates that the attention system of the human brain can be "primed," in apparent analogy to repetition-suppression effects on activity in other neural systems. For repetition of target color but not location, we also found repetition suppression in inferior temporal areas that may be associated with color processing, whereas repetition of target location led to greater reduction of activation in contralateral inferior parietal and frontal areas, relative to color repetition. The frontal eye fields were also implicated, notably when both target properties (color and location) were repeated together, which also led to further BOLD decreases in anterior fusiform cortex not seen when either property was repeated alone. These findings reveal the neural correlates for priming of pop-out search, including commonalities, differences, and interactions between location and color repetition. fMRI repetition-suppression effects may arise in components of the attention network because these settle into a stable "attractor state" more readily when the same target property is repeated than when a different attentional state is required.     

Attentional Bias in Posttraumatic Stress Disorder

This study investigated preferential encoding of threat material in subjects with posttraumatic stress disorder (PTSD) with a modified dot-probe paradigm. This paradigm indexes attentional bias by measuring response latency to name neutral target words that are presented adjacent to or distant from threat words. Motor vehicle accident survivors with PTSD (n = 15), subclinical PTSD (n = 15), and low anxiety (n = 15) were required to name target words that were presented either adjacent to or distant from strong threat, mild threat, positive, and neutral words. PTSD subjects named targets faster when they were in close proximity to mild threat words. Results suggested that PTSD subjects' attention was drawn to the mild threat stimuli and are discussed in the context of network models of PTSD.     

Activity in right temporo-parietal junction is not selective for theory-of-mind

Recent researchers have suggested that a region of right temporo-parietal junction (RTPJ) selectively subserves the attribution of beliefs to other people (Saxe R, Kanwisher N. 2003. People thinking about thinking people: fMRI investigations of theory of mind. NeuroImage. 19:1835-1842; Saxe R, Powell LJ. 2006. It's the thought that counts: specific brain regions for one component of theory of mind. Psychol Sci. 17:692-699; Saxe R, Wexler A. 2005. Making sense of another mind: the role of the right temporo-parietal junction. Neuropsychologia. 43:1391-1399). At the same time, a similar RTPJ region has been observed repeatedly in a variety of nonsocial tasks that require participants to redirect attention to task-relevant stimuli (e.g., Corbetta M, Shulman GL. 2002. Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci. 3:201-215; Serences JT, Shomstein S, Leber AB, Golay X, Egeth HE, Yantis S. 2005. Coordination of voluntary and stimulus-driven attentional control in human cortex. Psychol Sci. 16:114-122). However, because these 2 sets of tasks have never been compared within the same participants, it remains unclear whether these observations refer to the exact same region of RTPJ or may instead involve neighboring regions with distinct functional profiles. To test the claim that there is a region of RTPJ selective for belief attribution, the current study used functional neuroimaging to examine the extent to which cortical loci identified by a "theory-of-mind localizer" also distinguish between trials on a target detection task that varied demands to reorient attention (i.e., a version of the "Posner cueing task"). Results were incompatible with claims of RTPJ selectivity for mental state attribution. Regardless of whether regions were defined from group analyses or were individually tailored for each participant, RTPJ activity was also modulated by the nonsocial attentional task. The overlap between theory-of-mind and attentional reorienting suggests the need for new accounts of RTPJ function that integrate across these disparate task comparisons.     

Control of object-based attention in human cortex

Visual attention is a mechanism by which observers select relevant or important information from the current visual array. Previous investigations have focused primarily on the ability to select a region of space for further visual analysis. These studies have revealed a distributed frontoparietal circuit that is responsible for the control of spatial attention. However, vision must ultimately represent objects and in real scenes objects often overlap spatially; thus attention must be capable of selecting objects and their properties nonspatially. Little is known about the neural basis of object-based attentional control. In two experiments, human observers shifted attention between spatially superimposed faces and houses. Event-related functional magnetic resonance imaging (fMRI) revealed attentional modulation of activity in face- and house-selective cortical regions. Posterior parietal and frontal regions were transiently active when attention was shifted between spatially superimposed perceptual objects. The timecourse of activity provides insight into the functional role that these brain regions play in attentional control processes.     

Cingulate activation increases dynamically with response speed under stimulus unpredictability

Functional magnetic resonance imaging studies of cognition require repeated and consistent engagement of the cognitive process under investigation. Activation is generally averaged across trials that are assumed to tax a specific mental operation or state, whereas intraindividual variability in performance between trials is usually considered error variance. A more recent analysis approach postulates that these fluctuations can reflect variation in the very process taxed by the particular trial type. In the present study, participants responded to targets presented randomly in 1 of 4 peripheral locations. By employing a function of reaction time (RT) of individual trials as a linear regressor, brain regions were identified whose activation varied with RT on a trial-by-trial basis. Whole-brain analysis revealed that the anterior cingulate, posterior cingulate, and left angular/superior temporal gyri were more active in trials with faster RT but only when the target location was unpredictable. No such association was seen in trials where the target location was predicted by a central cue. These results suggest a role for the cingulate and angular gyri in the dynamic regulation of attention to unpredictable events. This is in accordance with the function of a default network that is active in the absence of top-down-focused attention and is thought to continuously provide resources for broad and spontaneous information gathering. Exploiting intertrial performance variability may be particularly suitable for capturing such spontaneous and elusive phenomena as stimulus-driven processes of attention.     

Enhanced processing of threat stimuli under limited attentional resources

The ability to process stimuli that convey potential threat, under conditions of limited attentional resources, confers adaptive advantages. This study examined the neurobiology underpinnings of this capacity. Employing an attentional blink paradigm, in conjunction with functional magnetic resonance imaging, we manipulated the salience of the second of 2 face target stimuli (T2), by varying emotionality. Behaviorally, fearful T2 faces were identified significantly more than neutral faces. Activity in fusiform face area increased with correct identification of T2 faces. Enhanced activity in rostral anterior cingulate cortex (rACC) accounted for the benefit in detection of fearful stimuli reflected in a significant interaction between target valence and correct identification. Thus, under conditions of limited attention resources activation in rACC correlated with enhanced processing of emotional stimuli. We suggest that these data support a model in which a prefrontal "gate" mechanism controls conscious access of emotional information under conditions of limited attentional resources.     

Impaired filtering of distracter stimuli by TE neurons following V4 and TEO lesions in macaques

Directing attention to a behaviorally relevant visual stimulus can overcome the distracting effects of other nearby stimuli. Correspondingly, physiological studies indicate that attention serves to filter distracting stimuli from receptive fields (RFs) in several extrastriate areas. Moreover, a recent study demonstrated that lesions of extrastriate areas V4 and TEO produce impairments in attentional filtering. A critical remaining question concerns why lesions of ventral stream areas cause attentional filtering impairments. To address this question, we tested the effects of restricted area V4 and TEO lesions on both behavioral performance and the responses of downstream neurons in area TE. The lesions impaired behavioral discrimination thresholds and altered neuronal selectivity for target stimuli in the presence of distracters. With attention to the target, but in the absence of V4 and/or TEO inputs, TE neurons responded as though attentional inputs could no longer be used to filter distracters from their RFs. This presumably occurred because top-down attentional signals were no longer able to filter distracters from the RFs of the cells that provide TE with major input. Consistent with this interpretation, increasing the spatial separation between targets and distracters, such that they no longer fell within a typical V4 RF dimension, restored both behavioral performance and neuronal selectivity in the portion of TE RFs affected by the V4 lesion.     

Large-scale gamma-band phase synchronization and selective attention

Explaining the emergence of a coherent conscious percept and an intentional agent from the activity of distributed neurons is key to understanding how the brain produces higher cognitive processes. Gamma-band synchronization has been proposed to be a mechanism for the functional integration of neural populations that together form a transitory, large-scale, task- and/or percept-specific network. The operation of this mechanism in the context of attention orienting entails that cortical regions representing attended locations should show more gamma-band synchronization with other cortical areas than would those representing unattended locations. This increased synchronization should be apparent in the same time frame as that of the deployment of attention to a particular location. In order to observe this effect, we made electroencephalogram recordings while subjects attended to one side or the other of the visual field (which we confirmed by event-related potential analysis) and calculated phase-locking statistics between the signals recorded at relevant electrode pairs. We observed increased gamma-band phase synchronization between visual cortex contralateral to the attended location and other, widespread, cortical areas approximately 240-380 ms after the directional cue was presented, confirming the prediction of a large-scale gamma synchronous network oriented to the cued location.     

Dorsal anterior cingulate cortex resolves conflict from distracting stimuli by boosting attention toward relevant events

In everyday life, we often focus greater attention on behaviorally relevant stimuli to limit the processing of distracting events. For example, when distracting voices intrude upon a conversation at a noisy social gathering, we concentrate more attention on the speaker of interest to better comprehend his or her speech. In the present study, we investigated whether dorsal/caudal regions of the anterior cingulate cortex (dACC), thought to make a major contribution to cognitive control, boost attentional resources toward behaviorally relevant stimuli as a means for limiting the processing of distracting events. Sixteen healthy participants performed a cued global/local selective attention task while brain activity was recorded with event-related functional magnetic resonance imaging. Consistent with our hypotheses, greater dACC activity during distracting events predicted reduced behavioral measures of interference from those same events. dACC activity also differed for cues to attend to global versus local features of upcoming visual objects, further indicating a role in directing attention toward task-relevant stimuli. Our findings indicate a role for dACC in focusing attention on behaviorally relevant stimuli, especially when the achievement of our behavioral goals is threatened by distracting events.     

Spatially selective representations of voluntary and stimulus-driven attentional priority in human occipital, parietal, and frontal cortex

When multiple objects are present in a visual scene, they compete for cortical processing in the visual system; selective attention biases this competition so that representations of behaviorally relevant objects enter awareness and irrelevant objects do not. Deployments of selective attention can be voluntary (e.g., shift or attention to a target's expected spatial location) or stimulus driven (e.g., capture of attention by a target-defining feature such as color). Here we use functional magnetic resonance imaging to show that both of these factors induce spatially selective attentional modulations within regions of human occipital, parietal, and frontal cortex. In addition, the voluntary attentional modulations are temporally sustained, indicating that activity in these regions dynamically tracks the locus of attention. These data show that a convolution of factors, including prior knowledge of location and target-defining features, determines the relative competitive advantage of visual stimuli within multiple stages of the visual system.     

Attentional functions of parietal and frontal cortex

A model of normal attentional function, based on the concept of competitive parallel processing, is used to compare attentional deficits following parietal and frontal lobe lesions. Measurements are obtained for visual processing speed, capacity of visual short-term memory (VSTM), spatial bias (bias to left or right hemifield) and top-down control (selective attention based on task relevance). The results show important differences, but also surprising similarities, in parietal and frontal lobe patients. For processing speed and VSTM, deficits are selectively associated with parietal lesions, in particular lesions of the temporoparietal junction. We discuss explanations based on either grey matter or white matter lesions. In striking contrast, measures of attentional weighting (spatial bias and top-down control) are predicted by simple lesion volume. We suggest that attentional weights reflect competition between broadly distributed object representations. Parietal and frontal mechanisms work together, both in weighting by location and weighting by task context.