Zooming in and zooming out of the attentional focus: an FMRI study

Visuospatial attention can either be "narrowly" focused on (zooming in) or "widely" distributed to (zooming out) different locations in space. In the current functional magnetic resonance imaging study, we investigated the shared and differential neural mechanisms underlying the dynamic "zooming in" and "zooming out" processes while potential distance confounds from visual inputs between zooming in and zooming out were controlled for. When compared with zooming out, zooming in differentially implicated left anterior intraparietal sulcus (IPS), which may reflect the functional specificity of left anterior IPS in focusing attention on local object features. By contrast, zooming out differentially activated right inferior frontal gyrus, which may reflect higher demands on cognitive control processes associated with enlarging the attentional focus. A conjunction analysis between zooming in and zooming out revealed significant shared activations in right middle temporal gyrus, right superior occipital gyrus, and right superior parietal cortex. The latter result suggests that the right posterior temporal-occipital-parietal system, which is known to be crucial for the control of spatial attention, is involved in updating the internal representation of the spatial locations that attentional processing is associated with.     

Neuronal responses in area 7a to multiple-stimulus displays: I. neurons encode the location of the salient stimulus.

The primate posterior parietal cortex (PPC) plays an important role in representing and recalling spatial relationships and in the ability to orient visual attention. This is evidenced by the parietal activation observed in brain imaging experiments performed during visuo- spatial tasks, and by the contralateral neglect syndrome that often accompanies parietal lesions. Individual neurons in monkey parietal cortex respond vigorously to the appearance of single, behaviorally relevant stimuli, but little is known about how they respond to more complex visual displays. The current experiments addressed this issue by recording activity from single neurons in area 7a of the PPC in monkeys performing a spatial version of a match-to-sample task. The task required them to locate salient stimuli in multiple-stimulus displays and release a lever after a subsequent stimulus appeared at the same location. Neurons responded preferentially to the appearance of salient stimuli inside their receptive fields. The presence of multiple stimuli did not affect appreciably the spatial tuning of responses in the majority of neurons or the population code for the location of the salient stimulus. Responses to salient stimuli could be distinguished from background stimuli approximately 100 ms after the onset of the cue. These results suggest that area 7a neurons represent the location of the stimulus attracting the animal's attention and can provide the spatial information required for directing attention to a salient stimulus in a complex scene.     

Fractionating attentional control using event-related fMRI

Despite numerous functional neuroimaging and lesion studies of human executive function, the precise neuroanatomical correlates of specific components of attentional control remain controversial. Using a novel approach that focused upon volunteer behavior rather than experimental manipulations, specific components of attentional shifting were fractionated, and their neural correlates differentiated using event-related fMRI. The results demonstrate that the ventrolateral prefrontal cortex is involved in switching attention "between" stimulus dimensions, whereas the posterior parietal cortex mediates changes in stimulus-response mapping. Furthermore, reversals based on negative feedback activated the lateral orbitofrontal cortex, whereas positive feedback modulated activity in the medial orbital frontal cortex. Finally, the dorsolateral prefrontal cortex was active throughout solution search. These findings support the hypothesis that lateral prefrontal, orbital, and parietal areas form a supervisory network that controls the focus of attention and suggests that these regions can be fractionated in terms of their specific contributions.     

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.     

Directing attention to locations and to sensory modalities: multiple levels of selective processing revealed with PET

We used positron emission tomography (PET) to investigate the neural correlates of selective attention in humans. We examined the effects of attending to one side of space versus another (spatial selection) and to one sensory modality versus another (intermodal selection) during bilateral, bimodal stimulation of vision and touch. Attention toward one side resulted in greater activity in several contralateral areas. In somatosensory cortex, these spatial attentional modulations were found only when touch was relevant. In the intraparietal sulcus, spatial attentional effects were multimodal, independent of the modality attended. In occipital areas, spatial modulations were also found during both visual and tactile attention, indicating that tactile attention can affect activity in visual cortex; but occipital areas also showed more activity overall during visual attention. This suggests that while spatial attention can exert multimodal influences on visual areas, these still maintain their specificity for the visual modality. Additionally, irrespective of the attended side, attending to vision activated posterior parietal and superior premotor cortices, while attending to touch activated the parietal operculi. We conclude that attentional selection operates at multiple levels, with attention to locations and attention to modalities showing distinct effects. These jointly contribute to boost processing of stimuli at the attended location in the relevant modality.     

Dissociation of stimulus relevance and saliency factors during shifts of visuospatial attention

The control of visuospatial attention entails multiple processes, including both voluntary (endogenous) factors and stimulus-driven (exogenous) factors. Exogenous processes can be triggered by visual targets presented at a previously unattended location, thus capturing attention in a stimulus-driven manner. However, little is known about the relative role of stimulus salience and behavioral relevance for this type of spatial reorienting. Here, we directly assessed how salience and relevance affect activation of the frontoparietal attentional system, using either low-salience but task-relevant target stimuli or salient but task-irrelevant flickering checkerboards. We compared event-related functional magnetic resonance imaging responses for stimuli presented at the unattended versus attended side (invalid minus valid trials), separately for the 2 categories of visual stimuli. We found that task-relevant invalid targets activated the frontoparietal attentional network, demonstrating that this system engages when target stimuli are presented at an unattended location, even when these have a low perceptual salience. Conversely, the presentation of high-salience checkerboards in one hemifield while endogenous attention was engaged elsewhere did not activate the attentional network. These findings indicate that task relevance is critical for stimulus-driven engagement of the attentional network when attentional resources are endogenously allocated somewhere else.     

Endogenous auditory spatial attention modulates obligatory sensory activity in auditory cortex

Endogenous attention is the self-directed focus of attention to a region or feature of the environment. In this study, we assess the effects of endogenous attention on temporally detailed responses to continuous and competing auditory stimuli obtained using the novel auditory evoked spread spectrum analysis (AESPA) method. There is some debate as to whether an enhancement of sensory processing is involved in endogenous attention. It has been suggested that attentional effects are not due to increased sensory activity but are due to engagement of separate temporally overlapping nonsensory attention-related activity. There are also issues with the fact that the influence of exogenous attention grabbing mechanisms may hamper studies of endogenous attention. Due to the nature of the AESPA method, the obtained responses represent activity directly related to the stimulus envelope and thus predominantly correspond to obligatory sensory processing. In addition, the continuous nature of the stimuli minimizes exogenous attentional influence. We found attentional modulations at ~136 ms (during the Nc component of the AESPA response) and localized this to auditory cortex. Although the involvement of separate nonsensory attentional centers cannot be ruled out, these findings clearly demonstrate that endogenous attention does modulate obligatory sensory activity in auditory cortex.     

Maintaining and shifting attention within left or right hemifield

Positron emission tomography (PET) was used to examine two questions: (i) which structures of the intact human brain change their activity with the direction of attention to left or right visual field; and (ii) how does activity in these structures, and in parietal cortex in particular, depend on the frequency of attentional shifts? Subjects were required to discriminate the orientation of peripheral gratings. The two main experimental variables were the attended hemifield (left or right) and the proportion of trials requiring a shift within that hemifield (20% or 80%). A detection control condition was also included. Behaviourally, subjects were less accurate and significantly slower when a trial required a shift than when it did not. Ventral and lateral occipital areas showed significantly higher blood flow levels contralateral to the direction of attention. Replicating previous work, there was also a significant main effect of the direction of attention in left lateral prefrontal cortex: blood flow levels were higher during leftward attention in comparison both to baseline and to rightward attention. This left frontal effect reached significance in single subjects in whom several activation sites could be distinguished within left middle and inferior frontal gyrus. Right and left parietal cortex were activated during both left- and right-field attention conditions, with a tendency for higher activity levels when attention was directed contralaterally. Contrary to the experimental hypothesis, however, parietal regions were not activated differentially by high versus low numbers of attentional shifts. The current experiment confirms that left frontal convexity is sensitive to manipulations of the direction of visuospatial attention. The results do not indicate a specific role of parietal cortex in attentional shifting.     

Cross-modal binding and activated attentional networks during audio-visual speech integration: a functional MRI study

We evaluated the neural substrates of cross-modal binding and divided attention during audio-visual speech integration using functional magnetic resonance imaging. The subjects (n = 17) were exposed to phonemically concordant or discordant auditory and visual speech stimuli. Three different matching tasks were performed: auditory-auditory (AA), visual-visual (VV) and auditory-visual (AV). Subjects were asked whether the prompted pair were congruent or not. We defined the neural substrates for the within-modal matching tasks by VV-AA and AA-VV. We defined the cross-modal area as the intersection of the loci defined by AV-AA and AV-VV. The auditory task activated the bilateral anterior superior temporal gyrus and superior temporal sulcus, the left planum temporale and left lingual gyrus. The visual task activated the bilateral middle and inferior frontal gyrus, right occipito-temporal junction, intraparietal sulcus and left cerebellum. The bilateral dorsal premotor cortex, posterior parietal cortex (including the bilateral superior parietal lobule and the left intraparietal sulcus) and right cerebellum showed more prominent activation during AV compared with AA and VV. Within these areas, the posterior parietal cortex showed more activation during concordant than discordant stimuli, and hence was related to cross-modal binding. Our results indicate a close relationship between cross-modal attentional control and cross-modal binding during speech reading.     

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.     

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.     

Parietal damage dissociates saccade planning from presaccadic perceptual facilitation

A well-known theory in the field of attention today is the premotor theory of attention which suggests that the mechanisms involved in eye movements are the same as those for spatial attention shifts. We tested a parietal damaged patient with unilateral optic ataxia and 4 controls on a dual saccade/attentional task and show a dissociation between saccadic eye movements and presaccadic perceptual enhancement at the saccade goal. Remarkably, though the patient was able to make the appropriate saccades to the left, impaired visual field (undistinguishable from saccades to his right, intact visual field), he was unable to discriminate the letter at the saccade goal (whereas his performance was like controls for letter discrimination in his right visual field). This suggests that saccade planning and presaccadic perceptual facilitation are separable--planning a saccade to a location does not necessitate that the processing of this location is enhanced. Based on these results, we suggest that the parietal cortex is necessary for the coupling between saccade planning and presaccadic perceptual facilitation.     

Human ventral parietal cortex plays a functional role on visuospatial attention and primary consciousness. A repetitive transcranial magnetic stimulation study

In this paper, we used repetitive transcranial magnetic stimulation (rTMS) in 18 normal subjects to investigate whether the ventral posterior parietal cortex (PPC) plays a causal role on visuospatial attention and primary consciousness and whether these 2 functions are linearly correlated with each other. Two distinct experimental conditions involved a similar visual stimuli recognition paradigm. In "Consciousness" experiment, number of consciously perceived visual stimuli was lower by about 10% after rTMS (300 ms, 20 Hz, motor threshold intensity) on left or right PPC than after sham (pseudo) rTMS. In "Attentional" Posner's experiment, these stimuli were always consciously perceived. Compared with sham condition, parietal rTMS slowed of about 25 ms reaction time to go stimuli, thus disclosing effects on endogenous covert spatial attention. No linear correlation was observed between the rTMS-induced impairment on attention and conscious perception. Results suggest that PPC plays a slight but significant causal role in both visuospatial attention and primary consciousness. Furthermore, these high-level cognitive functions, as modulated by parietal rTMS, do not seem to share either linear or simple relationships.     

Additive effects of emotional content and spatial selective attention on electrocortical facilitation

Affectively arousing visual stimuli have been suggested to automatically attract attentional resources in order to optimize sensory processing. The present study crosses the factors of spatial selective attention and affective content, and examines the relationship between instructed (spatial) and automatic attention to affective stimuli. In addition to response times and error rate, electroencephalographic data from 129 electrodes were recorded during a covert spatial attention task. This task required silent counting of random-dot targets embedded in a 10 Hz flicker of colored pictures presented to both hemifields. Steady-state visual evoked potentials (ssVEPs) were obtained to determine amplitude and phase of electrocortical responses to pictures. An increase of ssVEP amplitude was observed as an additive function of spatial attention and emotional content. Statistical parametric mapping of this effect indicated occipito-temporal and parietal cortex activation contralateral to the attended visual hemifield in ssVEP amplitude modulation. This difference was most pronounced during selection of the left visual hemifield, at right temporal electrodes. In line with this finding, phase information revealed accelerated processing of aversive arousing, compared to affectively neutral pictures. The data suggest that affective stimulus properties modulate the spatiotemporal process along the ventral stream, encompassing amplitude amplification and timing changes of posterior and temporal cortex.     

Neuronal responses in area 7a to multiple stimulus displays: II. responses are suppressed at the cued location.

Everyday visual scenes contain a variety of stimuli that vary in their significance. The companion paper demonstrates that neurons in the posterior parietal cortex (PPC) are capable of encoding the spatial locations of the salient stimulus in multiple stimulus scenes. The present experiment sought to address how neuronal responses to stimuli appearing in the receptive field are modulated after attention has been drawn to one of multiple stimuli in a visual scene. We recorded from area 7a of the PPC in monkeys trained to do a spatial version of a match-to-sample task. The results show that neuronal responses are greatly suppressed when stimuli appear at previously attended locations. No reduction in responsiveness is observed for locations where stimuli had previously appeared but did not draw attention. These results support the hypothesis that area 7a has a role in redirecting attention to stimuli appearing at novel, unattended locations.     

Representations of pleasant and painful touch in the human orbitofrontal and cingulate cortices

The cortical areas that represent affectively positive and negative aspects of touch were investigated using functional magnetic resonance imaging (fMRI) by comparing activations produced by pleasant touch, painful touch produced by a stylus, and neutral touch, to the left hand. It was found that regions of the orbitofrontal cortex were activated more by pleasant touch and by painful stimuli than by neutral touch and that different areas of the orbitofrontal cortex were activated by the pleasant and painful touches. The orbitofrontal cortex activation was related to the affective aspects of the touch, in that the somatosensory cortex (SI) was less activated by the pleasant and painful stimuli than by the neutral stimuli. This dissociation was highly significant for both the pleasant touch (P < 0.006) and for the painful stimulus (P < 0.02). Further, it was found that a rostral part of the anterior cingulate cortex was activated by the pleasant stimulus and that a more posterior and dorsal part was activated by the painful stimulus. Regions of the somatosensory cortex, including SI and part of SII in the mid-insula, were activated more by the neutral touch than by the pleasant and painful stimuli. Part of the posterior insula was activated only in the pain condition and different parts of the brainstem, including the central grey, were activated in the pain, pleasant and neutral touch conditions. The results provide evidence that different areas of the human orbitofrontal cortex are involved in representing both pleasant touch and pain, and that dissociable parts of the cingulate cortex are involved in representing pleasant touch and pain.     

Modulation of connectivity in visual pathways by attention: cortical interactions evaluated with structural equation modelling and fMRI

Electrophysiological and neuroimaging studies have shown that attention to visual motion can increase the responsiveness of the motion- selective cortical area V5 and the posterior parietal cortex (PP). Increased or decreased activation in a cortical area is often attributed to attentional modulation of the cortical projections to that area. This leads to the notion that attention is associated with changes in connectivity. We have addressed attentional modulation of effective connectivity using functional magnetic resonance imaging (fMRI). Three subjects were scanned under identical stimulus conditions (visual motion) while varying only the attentional component of the task. Haemodynamic responses defined an occipito-parieto-frontal network, including the, primary visual cortex (V1), V5 and PR A structural equation model of the interactions among these dorsal visual pathway areas revealed increased connectivity between V5 and PP related to attention. On the basis of our analysis and the neuroanatomical pattern of projections from the prefrontal cortex to PP we attributed the source of modulatory influences, on the posterior visual pathway, to the prefrontal cortex (PFC). To test this hypothesis we included the PFC in our model as a 'modulator' of the pathway between V5 and PP, using interaction terms in the structural equation model. This analysis revealed a significant modulatory effect of prefrontal regions on V5 afferents to posterior parietal cortex.      

Cortical mechanisms for shifting and holding visuospatial attention

Access to visual awareness is often determined by covert, voluntary deployments of visual attention. Voluntary orienting without eye movements requires decoupling attention from the locus of fixation, a shift to the desired location, and maintenance of attention at that location. We used event-related functional magnetic resonance imaging to dissociate these components while observers shifted attention among 3 streams of letters and digits, one located at fixation and 2 in the periphery. Compared with holding attention at the current location, shifting attention between the peripheral locations was associated with transient increases in neural activity in the superior parietal lobule (SPL) and frontal eye fields (FEF), as in previous studies. The supplementary eye fields and separate portions of SPL and FEF were more active for decoupling attention from fixation than for shifting attention to a new location. Large segments of precentral sulcus (PreCS) and posterior parietal cortex (PPC) were more active when attention was maintained in the periphery than when it was maintained at fixation. We conclude that distinct subcomponents of the dorsal frontoparietal network initiate redeployments of covert attention to new locations and disengage attention from fixation, while sustained activity in lateral regions of PPC and PreCS represents sustained states of peripheral attention.     

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.     

Attentional modulation of SSVEP power depends on the network tagged by the flicker frequency

Modulation of the steady-state visual evoked potential (SSVEP) by attention was studied in detail using 15 'tag' frequencies in the range of 2.5-20 Hz. The stimuli were two series of random disc search arrays superimposed on two concentric color-marked annuli respectively. Two series of arrays were updated independently; one updated at one fixed frequency (flicker) and the other updated randomly according to a white noise distribution (random broadband flicker, rbbf). On each trial, the observer was instructed to attend one annulus and to detect a target (a triangle) that occasionally appeared in a random disc array in the attended annulus. The SSVEP results show that the choice of flicker frequency selects which cortical network synchronizes to the flicker two distinct cortical networks showed different effects of attention. SSVEP power and the effects of attention on SSVEP power strongly depend on both flicker frequency and radial position of rbbf annulus. At flicker frequencies in the delta band (2-4 Hz), and in the upper alpha band (10-11 Hz), an occipital-frontal network appears to phase-lock to the flicker when attending to the flicker, increasing the magnitude of the SSVEP. At flicker frequencies in the lower alpha band (8-10 Hz), a global response to a peripheral flickering stimulus, that includes parietal cortex and posterior frontal cortex, has higher amplitude when attention is directed away from the flickering peripheral stimulus and towards a competing rbbf stimulus in the fovea. Increases in SSVEP power when attention is directed to peripheral flicker are always associated with increases in phase locking. By contrast, at frequencies in the lower alpha band, increases in SSVEP power when attention is directed away from the flicker and towards foveal stimuli are not associated with changes in phase-locking. Thus, whether attention to a flicker stimulus increases or decreases SSVEP amplitude and phase locking depends on which of two cortical networks, which have distinct spatial and dynamic properties, is selected by the flicker frequency.