Cerebral correlates of alerting, orienting and reorienting of visuospatial attention: an event-related fMRI study

The identification of brain systems contributing to different aspects of visuospatial attention is of both clinical and theoretical interest. Cued target detection tasks provide a simple means to dissociate attentional subcomponents, such as alerting, orienting or reorienting of attention. Event-related functional magnetic resonance imaging (fMRI) was used to study neural correlates of these distinct attentional processes. Volunteers were scanned while performing a centrally cued target detection task. Four different types of trials (no cue, neutral cue, valid cue and invalid cue trials) with targets appearing either in the right or left hemifield were randomly intermixed. Behaviourally, the data provided evidence for alerting, spatial orienting and reorienting of attention. Neurally, the alerting effect was seen in bilaterally increased extrastriatal blood oxygenation level-dependent (BOLD) activity in neutral as compared to no cue trials. Neural correlates of spatial orienting were seen in anterior cingulate cortex, which was more active during valid as compared to neutral cue trials. Neural correlates of reorienting of attention, that is, higher BOLD activity to invalid as compared to validly cued trials were evident in several brain regions including left and right intraparietal sulcus, right temporo-parietal junction and middle frontal gyrus bilaterally. The data suggest that frontal and parietal regions are specifically involved in reorienting rather than orienting attention to a spatial position. Alerting effects were seen in extrastriate regions which suggest that increased phasic alertness results in a top-down modulation of neural activity in visual processing areas.     

Directing spatial attention in mental representations: Interactions between attentional orienting and working-memory load

Orienting spatial attention to locations in the extrapersonal world has been intensively investigated during the past decades. Recently, it was demonstrated that it is also possible to shift attention to locations within mental representations held in working memory. This is an important issue, since the allocation of our attention is not only guided by external stimuli, but also by their internal representations and the expectations we build upon them. The present experiment used behavioural measures and event-related functional magnetic resonance imaging to investigate whether spatial orienting to mental representations can modulate the search and retrieval of information from working memory, and to identify the neural systems involved, respectively. Participants viewed an array of coloured crosses. Seconds after its disappearance, they were cued to locations in the array with valid or neutral cues. Subsequently, they decided whether a probe stimulus was presented in the array. The behavioural results indicated that orienting of spatial attention within working memory attenuates the well-known effect of decreasing performance when memory load is increased. So "internal" spatial orienting seems to highlight information or facilitate search within working memory, which leads to advantages in retrieval. Imaging enabled the separation of brain areas supporting spatial orienting functions from those sensitive to working-memory load. Orienting of spatial attention to the contents of working memory activated posterior parietal cortex bilaterally, the insula, and lateral and medial frontal cortices.     

Covert visual spatial orienting and saccades: overlapping neural systems

We used functional magnetic resonance imaging (fMRI) to investigate the functional anatomical relationship between covert orienting of visual spatial attention and execution of saccadic eye movements. Brain areas engaged by shifting spatial attention covertly and by moving the eyes repetitively toward visual targets were compared and contrasted directly within the same subjects. The two tasks activated highly overlapping neural systems and showed that common parietal and frontal regions are more activated during the covert task than the overt oculomotor condition. The possible nature of the relationship between these two operations is discussed.     

Hemispheric differences in hemodynamics elicited by auditory oddball stimuli

Evidence from neuroimaging studies suggests that the right hemisphere of the human brain might be more specialized for attention than the left hemisphere. However, differences between right and left hemisphere in the magnitude of hemodynamic activity (i.e., 'functional asymmetry') rarely have been explicitly examined in previous neuroimaging studies of attention. This study used a new voxel-based comparison method to examine hemispheric differences in the amplitude of the hemodynamic response in response to infrequent target, infrequent novel, and frequent standard stimuli during an event-related fMRI auditory oddball task in 100 healthy adult participants. Processing of low probability task-relevant target stimuli, or 'oddballs', and low probability task-irrelevant novel stimuli is believed to engage in orienting and attentional processes. It was hypothesized that greater right-hemisphere activation compared to left would be observed to infrequent target and novel stimuli. Consistent with predictions, greater right hemisphere than left frontal, temporal, and parietal lobe activity was observed for target detection and novelty processing. Moreover, asymmetry effects did not differ with respect to age or gender of the participants. The results (1) support the proposal that the right hemisphere is differentially engaged in processing salient stimuli and (2) demonstrate the successful use of a new voxel-based laterality analysis technique for fMRI data.     

A hedonically complex odor mixture produces an attentional capture effect in the brain

A counter-intuitive property of many pleasant and attractive stimuli is that they are hedonically complex, containing both pleasant and unpleasant components. A striking example is the floral scent of natural jasmine, which may contain more than 6% of indole, a pure chemical which is usually rated as unpleasant. Using fMRI we investigate the hypothesis that the interaction between the pleasant and unpleasant components in the hedonically complex natural jasmine produces an attentional capture effect in the brain. First, to localize brain areas involved in selective attention to odor, we compared neural activity in response to jasmine without indole when participants explicitly and selectively attended to either its pleasantness or intensity, with neural activity when no selective attention was required. We then show that the superior frontal gyrus has increased activity both when selective attention is being paid to jasmine without indole, and also when no selective attention is required but an unpleasant component is added to it to produce a hedonically complex mixture. The attentional capture effect in the superior frontal gyrus by the mixture was related to the hedonic complexity of the mixture across subjects; could not be explained by salience, intensity, or pleasantness; and was specific to the superior frontal gyrus in that it was not found in other prefrontal areas activated by selective attention. The investigation supports the new hypothesis that the affective potency of stimuli with mixed pleasant and unpleasant components is related at least in part to the recruitment of mechanisms in the brain involved in attentional capture and enhancement.     

右侧额顶网络在空间注意认知过程中的作用机制

目的:探讨右侧额顶网络(FPN)与视空间注意认知功能的关联性和作用机制.方法:选取志愿受试者60人参加本实验,随机分为顶叶组和额叶组.采用持续短阵快速脉冲(cTBS)经颅磁刺激(rTMS)右侧背外侧前额叶(DLPFC)和后顶叶皮质(DPC)后进行注意网络测试(ANT),所有受试者均按照随机顺序进行真/假刺激.结果:持续短阵快速脉冲经颅磁刺激施加于前额叶和后顶叶,不同提示和刺激类型的平均反应时均无明显改变.右侧后顶叶抑制,警觉和定向功能受损(P＜0.05);右侧额叶抑制,执行功能受损(P＜0.05),而定向功能增强(P＜0.05).结论:在视空间注意过程中,右侧后顶叶是定向功能的关键区,右侧前额叶是执行功能的关键区,并且右侧额顶区之间存在竞争性抑制现象.     

Neural mechanisms of top-down control during spatial and feature attention

Theories of visual selective attention posit that both spatial location and nonspatial stimulus features (e.g., color) are elementary dimensions on which top-down attentional control mechanisms can selectively influence visual processing. Neuropsychological and neuroimaging studies have demonstrated that regions of superior frontal and parietal cortex are critically involved in the control of visual-spatial attention. This frontoparietal control network has also been found to be activated when attention is oriented to nonspatial stimulus features (e.g., motion). To test the generality of the frontoparietal network in attentional control, we directly compared spatial and nonspatial attention in a cuing paradigm. Event-related fMRI methods permitted the isolation of attentional control activity during orienting to a location or to a nonspatial stimulus feature (color). Portions of the frontoparietal network were commonly activated to the spatial and nonspatial cues. However, direct statistical comparisons of cue-related activity revealed subregions of the frontoparietal network that were significantly more active during spatial than nonspatial orienting when all other stimulus, task, and attentional factors were equated. No regions of the frontal-parietal network were more active for nonspatial cues in comparison to spatial cues. These findings support models suggesting that subregions of the frontal-parietal network are highly specific for controlling spatial selective attention.     

Endogenous and exogenous attention shifts are mediated by the same large-scale neural network

Event-related fMRI was used to examine the neural basis of endogenous (top-down) and exogenous (bottom-up) spatial orienting. Shifts of attention were induced by central (endogenous) or peripheral (exogenous) cues. Reaction times on subsequently presented targets showed the expected pattern of facilitation and inhibition in both conditions. No difference in brain activity was observed when the two orienting conditions were contrasted with a liberal threshold, showing that both forms of orienting were mediated by the same neural network. Compared to within-block control trials, both endogenous and exogenous orienting activated a fronto-parietal network consisting of premotor cortex, posterior parietal cortex, medial frontal cortex and right inferior frontal cortex. Within these regions, equally strong activation was observed for both orienting conditions. It is concluded that endogenous and exogenous orienting are mediated by the same large-scale network of frontal and parietal brain areas.     

Conflict monitoring in the human anterior cingulate cortex during selective attention to global and local object features

Parallel processing affords the brain many advantages, but processing multiple bits of information simultaneously presents formidable challenges. For example, while one is listening to a speaker at a noisy social gathering, processing irrelevant conversations may lead to the activation of irrelevant perceptual, semantic, and response representations that conflict with those evoked by the speaker. In these situations, specialized brain systems may be recruited to detect and resolve conflict before it leads to incorrect perception and/or behavior. Consistent with this view, recent findings indicate that dorsal/caudal anterior cingulate cortex (dACC), on the medial walls of the frontal lobes, detects conflict between competing motor responses primed by relevant versus irrelevant stimuli. Here, we used a cued global/local selective attention task to investigate whether the dACC plays a general role in conflict detection that includes monitoring for conflicting perceptual or semantic representations. Using event-related functional magnetic resonance imaging (fMRI), we found that the dACC was activated by response conflict in both the global and the local task, consistent with results from prior studies. However, dACC was also activated by perceptual and semantic conflict arising from global distracters during the local task. The results from the local task have implications for recent theories of attentional control in which the dACC's contribution to conflict monitoring is limited to response stages of processing, as well as for our understanding of clinical disorders in which disruptions of attention are associated with dACC dysfunction.     

Exploring the visual world: the neural substrate of spatial orienting

Inspecting the visual environment, humans typically direct their attention across space by means of voluntary saccadic eye movements. Neuroimaging studies in healthy subjects have identified the superior parietal cortex and intraparietal sulcus as important structures involved in visual search. However, in apparent contrast, spatial disturbance of free exploration typically is observed after damage of brain structures located far more ventrally. Lesion studies in such patients disclosed the inferior parietal lobule (IPL) and temporo-parietal junction (TPJ), the superior temporal gyrus (STG) and insula, as well as the inferior frontal gyrus (IFG) of the right hemisphere. Here we used functional magnetic resonance imaging to investigate the involvement of these areas in active visual exploration in the intact brain. We conducted a region of interest analysis comparing free visual exploration of a dense stimulus array with the execution of stepwise horizontal and vertical saccades. The comparison of BOLD responses revealed significant signal increases during exploration in TPJ, STG, and IFG. This result calls for a reappraisal of the previous thinking on the function of these areas in visual search processes. In agreement with lesion studies, the data suggest that these areas are part of the network involved in human spatial orienting and exploration. The IPL dorsally of TPJ seem to be of minor importance for free visual exploration as these areas appear to be equally involved in the execution of spatially predetermined saccades.     

Functional anatomy of visual search: regional segregations within the frontal eye fields and effective connectivity of the superior colliculus

The ability to find targets embedded within complex visual environments requires the dynamic programming of visuomotor search behaviors. Functional magnetic resonance imaging was used to image subjects while they visually searched for targets embedded among foils. Visuomotor search activated the posterior parietal cortex and the frontal eye fields. Both regions showed a greater number of activated voxels on the right, consistent with the known pattern of right hemispheric dominance for spatial attention. The superior colliculus showed prominent activation in the search versus eye movement contrast, demonstrating, for the first time in humans, activation of this region specifically related to an exploratory attentional contingency. An analysis of effective connectivity demonstrated that the search-dependent variance in the activity of the superior colliculus was significantly influenced by the activity in a network of cortical regions including the right frontal eye fields and bilateral parietal and occipital cortices. These experiments also revealed the presence of a mosaic of activated sites within the frontal eye field region wherein saccadic eye movements, covert shifts of attention, and visuomotor search elicited overlapping but not identical zones of activation. In contrast to the existing literature on functional imaging, which has focused on covert shifts of spatial attention, this study helps to characterize the functional anatomy of overt spatial exploration.     

Attentional modulation of stimulus representation in human fronto-parietal cortex

Evidence from primates suggests that prefrontal and parietal regions selectively represent information that is relevant for current behavior. In humans, whilst functional imaging has shown that fronto-parietal areas are activated by a range of different cognitive demands, the actual content of representation remains unclear. The current report describes two studies designed to address this issue using fMRI adaptation. In both studies, participants completed a delayed matching task where they attended to either the color or the shape of a series of sample stimuli and indicated whether occasional test stimuli matched the preceding sample on the attended dimension. Whole brain contrasts showed that changes to the value of the currently attended dimension produced significantly greater responses in frontal and parietal areas than events where the value was repeated. In addition, prefrontal and parietal regions of interest showed strong interactions between the currently attended dimension and the type of stimulus change, reflecting an attentional modulation of responses to stimulus change. Further comparisons suggested that the differences between attended changes and stimulus repetitions carried information about specific stimulus values, and did not simply reflect a generic response to attended changes.     

Neuroimaging reveals automatic speech coding during perception of written word meaning

The extent to which visual word perception engages speech codes (i.e., phonological recoding) remains a crucial question in understanding mechanisms of reading. In this study, we used functional magnetic resonance imaging techniques combined with behavioral response measures to examine neural responses to focused versus incidental phonological and semantic processing of written words. Three groups of subjects made simple button-pressing responses in either phonologically (rhyming-judgment) or semantically (category-judgment) focused tasks or both tasks with identical sets of visual stimuli. In the phonological tasks, subjects were given both words and pseudowords separated in different scan runs. The baseline task required feature search of scrambled letter strings created from the stimuli for the experimental conditions. The results showed that cortical regions associated with both semantic and phonological processes were strongly activated when the task required active processing of word meaning. However, when subjects were actively processing the speech sounds of the same set of written words, brain areas typically engaged in semantic processing became silent. In addition, subjects who performed both the rhyming and the semantic tasks showed diverse and significant bilateral activation in the prefrontal, temporal, and other brain regions. Taken together, the pattern of brain activity provides evidence of a neural basis supporting the theory that in normal word reading, phonological recoding is automatic and facilitates semantic processing of written words, while rapid comprehension of word meaning requires devoted attention. These results also raise questions about including multiple cognitive tasks in the same neuroimaging sessions.     

Two brain pathways for attended and ignored words

The dependency of word processing on spare attentional resources has been debated for several decades. Recent research in the study of selective attention has emphasized the role of task load in determining the fate of ignored information. In parallel to behavioral evidence, neuroimaging data show that the activation generated by unattended stimuli is eliminated in task-relevant brain regions during high attentional load tasks. We conducted an fMRI experiment to explore how word encoding proceeds in a high load situation. Participants saw a rapid series of stimuli consisting of overlapping drawings and letter strings (words or nonwords). In different blocks, task instructions directed attention to either the drawings or the letters, and subjects responded to immediate repetition of items in the attended dimension. To look at the effect of attention on word processing, we compared brain activations for words and nonwords under the two attentional conditions. As compared to nonwords, word stimuli drove responses in left frontal, left temporal and parietal areas when letters were attended. However, although the behavioral measures suggested that ignored words were not analyzed when drawings were attended, a comparison of ignored words to ignored nonwords indicated the involvement of several regions including left insula, right cerebellum and bilateral pulvinar. Interestingly, word-specific activations found when attended and ignored words were compared showed no anatomical overlap, suggesting a change in processing pathways for attended and ignored words presented in a high attentional load task.     

Frontoparietal mechanisms supporting attention to location and intensity of painful stimuli

Attention can profoundly shape the experience of pain. However, little is known about the neural mechanisms that support directed attention to nociceptive information. In the present study, subjects were cued to attend to either the spatial location or the intensity of sequentially presented pairs of painful heat stimuli during a delayed match-to-sample discrimination task. We hypothesized that attention-related brain activation would be initiated after the presentation of the attentional cue and would be sustained through the discrimination task. Conjunction analysis confirmed that bilateral portions of the posterior parietal cortex (intraparietal sulcus [IPS] and superior parietal lobule) exhibited this sustained activity during attention to spatial but not intensity features of pain. Analyses contrasting activation during spatial and intensity attention tasks revealed that the right IPS region of the posterior parietal cortex was consistently more activated across multiple phases of the spatial task. However, attention to either feature of the noxious stimulus was associated with activation of frontoparietal areas (IPS and frontal eye fields) as well as priming of the primary somatosensory cortex. Taken together, these results delineate the neural substrates that support selective amplification of different features of noxious stimuli for utilization in discriminative processes.     

Functional specificity of superior parietal mediation of spatial shifting

Using event-related functional magnetic resonance imaging (fMRI) we determined how brain activity changes when an attended target shifts its location. In the main experiment, a white square could appear at 10 possible eccentricities along the horizontal meridian. It remained on the screen for a variable period of time and then changed location. At any time the stimulus could dim briefly. Subjects had to press a button when the stimulus dimmed. In order to perform this task attention had to be locked onto the target and shift with it. Half of the runs were performed overtly and half covertly. The event of interest consisted of the shift in the location of the attentional target. The state of maintained attention occurring in between the shifts constituted the baseline. The superior parietal gyrus was activated bilaterally in response to attentional shifts. No other area showed a significant response to shifting. On the left side the amplitude of the superior parietal response correlated positively with the distance of the shift. On the right side a significant correlation was present only for overt shifts. In a separate experiment we compared the maintaining of attention at a single spatial location to passive fixation: the frontal eye fields, anterior cingulate, right dorsolateral prefrontal cortex, and inferior parietal lobule were significantly activated, indicating that the absence of a shift-related response in these areas in the main experiment was due to the fact that they were equally activated by maintaining and shifting attention. The response to spatial shifts and the correlation with the distance between the original and the new location points to a specific role of the superior parietal gyrus in shifting the locus of spatial attention.     

Control networks and hemispheric asymmetries in parietal cortex during attentional orienting in different spatial reference frames

Neuropsychological research has consistently demonstrated that spatial attention can be anchored in one of several coordinate systems, including those defined with respect to an observer (viewer-centered), to the gravitational vector (environment-centered), or to individual objects (object-centered). In the present study, we used hemodynamic correlates of brain function to investigate the neural systems that mediate attentional control in two competing reference frames. Healthy volunteers were cued to locations defined in either viewer-centered or object-centered space to discriminate the shape of visual targets subsequently presented at the cued locations. Brain responses to attention-directing cues were quantified using event-related functional magnetic resonance imaging. A fronto-parietal control network was activated by attention-directing cues in both reference frames. Voluntary shifts of attention produced increased neural activity bilaterally in several cortical regions including the intraparietal sulcus, anterior cingulate cortex, and the frontal eye fields. Of special interest was the observation of hemispheric asymmetries in parietal cortex; there was significantly greater activity in left parietal cortex than in the right, but this asymmetry was more pronounced for object-centered shifts of attention, relative to viewer-centered shifts of attention. Measures of behavioral performance did not differ significantly between the two reference frames. We conclude that a largely overlapping, bilateral, cortical network mediates our ability to orient spatial attention in multiple coordinate systems, and that the left intraparietal sulcus plays an additional role for orienting in object-centered space. These results provide neuroimaging support for related claims based on findings of deficits in object-based orienting in patients with left parietal lesions.     

The activation of attentional networks

Alerting, orienting, and executive control are widely thought to be relatively independent aspects of attention that are linked to separable brain regions. However, neuroimaging studies have yet to examine evidence for the anatomical separability of these three aspects of attention in the same subjects performing the same task. The attention network test (ANT) examines the effects of cues and targets within a single reaction time task to provide a means of exploring the efficiency of the alerting, orienting, and executive control networks involved in attention. It also provides an opportunity to examine the brain activity of these three networks as they operate in a single integrated task. We used event-related functional magnetic resonance imaging (fMRI) to explore the brain areas involved in the three attention systems targeted by the ANT. The alerting contrast showed strong thalamic involvement and activation of anterior and posterior cortical sites. As expected, the orienting contrast activated parietal sites and frontal eye fields. The executive control network contrast showed activation of the anterior cingulate along with several other brain areas. With some exceptions, activation patterns of these three networks within this single task are consistent with previous fMRI studies that have been studied in separate tasks. Overall, the fMRI results suggest that the functional contrasts within this single task differentially activate three separable anatomical networks related to the components of attention.     

Neural networks underlying endogenous and exogenous visual-spatial orienting

The orienting of visual-spatial attention is fundamental to most organisms and is controlled through external (exogenous) or internal (endogenous) processes. Exogenous orienting is considered to be reflexive and automatic, whereas endogenous orienting refers to the purposeful allocation of attentional resources to a predetermined location in space. Although behavioral, electrophysiological and lesion research in both primates and humans suggests that separate neural systems control these different modes of orienting, previous human neuroimaging studies have largely reported common neuronal substrates. Therefore, event-related FMRI (ER-FMRI) was used to independently examine different components of the orienting response including endogenous facilitation, exogenous facilitation and inhibition of return (IOR). In contrast to previous studies, endogenous versus exogenous facilitation resulted in widespread cortical activation including bilateral temporoparietal junction, bilateral superior temporal gyrus, right middle temporal gyrus, right frontal eye field and left intraparietal sulcus. Conversely, IOR compared to endogenous facilitation resulted in only a single focus of activation in the left superior temporal gyrus. These findings suggest that endogenous orienting activates a large cortical network to achieve internally generated shifts of attentional resources versus the automatic orienting that occurs with exogenous cues. However, similar networks may mediate endogenous orienting and IOR. The activation of the temporoparietal junction suggests that it is involved in more effortful processes, such as endogenous orienting, as well as in attentional reorienting and locating targets. Current results are discussed in terms of the functional development of the visual-spatial attentional system.     

Neuroanatomic overlap of working memory and spatial attention networks: a functional MRI comparison within subjects

Frontal and posterior parietal activations have been reported in numerous studies of working memory and visuospatial attention. To directly compare the brain regions engaged by these two cognitive functions, the same set of subjects consecutively participated in tasks of working memory and spatial attention while undergoing functional MRI (fMRI). The working memory task required the subject to maintain an on-line representation of foveally displayed letters against a background of distracters. The spatial attention task required the subject to shift visual attention covertly in response to a centrally presented directional cue. The spatial attention task had no working memory requirement, and the working memory task had no covert spatial attention requirement. Subjects' ability to maintain central fixation was confirmed outside the MRI scanner using infrared oculography. According to cognitive conjunction analysis, the set of activations common to both tasks included the intraparietal sulcus, ventral precentral sulcus, supplementary motor area, frontal eye fields, thalamus, cerebellum, left temporal neocortex, and right insula. Double-subtraction analyses yielded additional activations attributable to verbal working memory in premotor cortex, left inferior prefrontal cortex, right inferior parietal lobule, precuneus, and right cerebellum. Additional activations attributable to covert spatial attention included the occipitotemporal junction and extrastriate cortex. The use of two different tasks in the same set of subjects allowed us to provide an unequivocal demonstration that the neural networks subserving spatial attention and working memory intersect at several frontoparietal sites. These findings support the view that major cognitive domains are represented by partially overlapping large-scale neural networks. The presence of this overlap also suggests that spatial attention and working memory share common cognitive features related to the dynamic shifting of attentional resources.