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.     

Spatial attention modulates initial afferent activity in human primary visual cortex

It is well established that spatially directed attention enhances visual perceptual processing. However, the earliest level at which processing can be affected remains unknown. To date, there has been no report of modulation of the earliest visual event-related potential component "C1" in humans, which indexes initial afference in primary visual cortex (V1). Thus it has been suggested that initial V1 activity is impenetrable, and that the earliest modulations occur in extrastriate cortex. However, the C1 is highly variable across individuals, to the extent that uniform measurement across a group may poorly reflect the dynamics of V1 activity. In the present study we employed an individualized mapping procedure to control for such variability. Parameters for optimal C1 measurement were determined in an independent, preliminary "probe" session and later applied in a follow-up session involving a spatial cueing task. In the spatial task, subjects were cued on each trial to direct attention toward 1 of 2 locations in anticipation of an imperative Gabor stimulus and were required to detect a region of lower luminance appearing within the Gabor pattern 30% of the time at the cued location only. Our data show robust spatial attentional enhancement of the C1, beginning as early as its point of onset (57 ms). Source analysis of the attentional modulations points to generation in striate cortex. This finding demonstrates that at the very moment that visual information first arrives in cortex, it is already being shaped by the brain's attentional biases.     

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.     

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.     

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.     

The effects of stimulus modality and frequency of stimulus presentation on cross-modal distraction

Selective attention produces enhanced activity (attention-related modulations [ARMs]) in cortical regions corresponding to the attended modality and suppressed activity in cortical regions corresponding to the ignored modality. However, effects of behavioral context (e.g., temporal vs. spatial tasks) and basic stimulus properties (i.e., stimulus frequency) on ARMs are not fully understood. The current study used functional magnetic resonance imaging to investigate selectively attending and responding to either a visual or auditory metronome in the presence of asynchronous cross-modal distractors of 3 different frequencies (0.5, 1, and 2 Hz). Attending to auditory information while ignoring visual distractors was generally more efficient (i.e., required coordination of a smaller network) and less effortful (i.e., decreased interference and presence of ARMs) than attending to visual information while ignoring auditory distractors. However, these effects were modulated by stimulus frequency, as attempting to ignore auditory information resulted in the obligatory recruitment of auditory cortical areas during infrequent (0.5 Hz) stimulation. Robust ARMs were observed in both visual and auditory cortical areas at higher frequencies (2 Hz), indicating that participants effectively allocated attention to more rapidly presented targets. In summary, results provide neuroanatomical correlates for the dominance of the auditory modality in behavioral contexts that are highly dependent on temporal processing.     

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 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.     

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.      

Dorsal posterior parietal rTMS affects voluntary orienting of visuospatial attention

Patients with lesions in posterior parietal cortex (PPC) are relatively unimpaired in voluntarily directing visual attention to different spatial locations, while many neuroimaging studies in healthy subjects suggest dorsal PPC involvement in this function. We used an offline repetitive transcranial magnetic stimulation (rTMS) protocol to study this issue further. Ten healthy participants performed a cue-target paradigm. Cues prompted covert orienting of spatial attention under voluntary control to either a left or right visual field position. Targets were flashed subsequently at the cued or uncued location, or bilaterally. Following rTMS over right dorsal PPC, (i) the benefit for target detection at cued versus uncued positions was preserved irrespective of cueing direction (left- or rightward), but (ii) leftward cueing was associated with a global impairment in target detection, at all target locations. This reveals that leftward orienting was still possible after right dorsal PPC stimulation, albeit at an increased overall cost for target detection. In addition, rTMS (iii) impaired left, but (iv) enhanced right target detection after rightward cueing. The finding of a global drop in target detection during leftward orienting with a spared, relative detection benefit at the cued (left) location (i-ii) suggests that right dorsal PPC plays a subsidiary rather than pivotal role in voluntary spatial orienting. This finding reconciles seemingly conflicting results from patients and neuroimaging studies. The finding of attentional inhibition and enhancement occurring contra- and ipsilaterally to the stimulation site (iii-iv) supports the view that spatial attention bias can be selectively modulated through rTMS, which has proven useful to transiently reduce visual hemispatial neglect.     

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.     

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.     

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.     

Visual binding through reentrant connectivity and dynamic synchronization in a brain-based device

Effective visual object recognition requires mechanisms to bind object features (e.g. color, shape and motion) while distinguishing distinct objects. Synchronously active neuronal circuits among reentrantly connected cortical areas may provide a basis for visual binding. To assess the potential of this mechanism, we have constructed a mobile brain-based device, Darwin VIII, which is guided by simulated analogues of cortical and sub-cortical areas required for visual processing, decision-making, reward and motor responses. These simulated areas are reentrantly connected and each area contains neuronal units representing both the mean activity level and the relative timing of the activity of groups of neurons. Darwin VIII learns to discriminate among multiple objects with shared visual features and associates 'target' objects with innately preferred auditory cues. We observed the co-activation of globally distributed neuronal circuits that corresponded to distinct objects in Darwin VIII's visual field. These circuits, which are constrained by a reentrant neuroanatomy and modulated by behavior and synaptic plasticity, are necessary for successful discrimination. By situating Darwin VIII in a rich real-world environment involving continual changes in the size and location of visual stimuli due to self-generated movement, and by recording its behavioral and neuronal responses in detail, we were able to show that reentrant connectivity and dynamic synchronization provide an effective mechanism for binding the features of visual objects.     

Attention-dependent suppression of metabolic activity in the early stages of the macaque visual system

In this study we used a modified double-label deoxyglucose procedure to investigate attention-dependent modulations of deoxyglucose uptake at the earliest stages of the macaque visual system. Specifically, we compared activity levels evoked during two tasks with essentially identical visual stimulation requiring different attentional demands. During a featural-attention task, the subjects had to discriminate the orientation of a grating; during a control spatial-attention task, they had to localize the position of a target point. Comparison of the resulting activity maps revealed attention-dependent changes in metabolic activity in portions of the magnocellular layers of the lateral geniculate nucleus, and the magnocellular-recipient layers 4Calpha and 4B of the striate cortex. In these early stages of the visual system, attention to the orientation of the grating suppressed the metabolic activity in a retinotopically specific band peripheral to the representation of the stimulus. These results favor an early selection model of attention. After a thalamic attention-dependent gating mechanism, irrelevant visual information outside the focus of attention may be suppressed at the level of the striate cortex, which would then result in an increased signal-to-noise ratio for the processing of the attended feature in higher-tier, less retinotopically organized, extrastriate visual areas.     

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.     

Tuning curve shift by attention modulation in cortical neurons: a computational study of its mechanisms

Physiological studies of visual attention have demonstrated that focusing attention near a visual cortical neuron's receptive field (RF) results in enhanced evoked activity and RF shift. In this work, we explored the mechanisms of attention induced RF shifts in cortical network models that receive an attentional 'spotlight'. Our main results are threefold. First, whereas a 'spotlight' input always produces toward-attention shift of the population activity profile, we found that toward-attention shifts in RFs of single cells requires multiplicative gain modulation. Secondly, in a feedforward two-layer model, focal attentional gain modulation in first-layer neurons induces RF shift in second-layer neurons downstream. In contrast to experimental observations, the feedforward model typically fails to produce RF shifts in second-layer neurons when attention is directed beyond RF boundaries. We then show that an additive spotlight input combined with a recurrent network mechanism can produce the observed RF shift. Inhibitory effects in a surround of the attentional focus accentuate this RF shift and induce RF shrinking. Thirdly, we considered interrelationship between visual selective attention and adaptation. Our analysis predicts that the RF size is enlarged (respectively reduced) by attentional signal directed near a cell's RF center in a recurrent network (resp. in a feedforward network); the opposite is true for visual adaptation. Therefore, a refined estimation of the RF size during attention and after adaptation would provide a probe to differentiate recurrent versus feedforward mechanisms for RF shifts.     

Context-related frequency modulations of macaque motor cortical LFP beta oscillations

The local field potential (LFP) is a population measure, mainly reflecting local synaptic activity. Beta oscillations (12-40 Hz) occur in motor cortical LFPs, but their functional relevance remains controversial. Power modulation studies have related beta oscillations to a "resting" motor cortex, postural maintenance, attention, sensorimotor binding and planning. Frequency modulations were largely overlooked. We here describe context-related beta frequency modulations in motor cortical LFPs. Two monkeys performed a reaching task with 2 delays. The first delay demanded attention in time in expectation of the visual spatial cue, whereas the second delay involved visuomotor integration and movement preparation. The frequency in 2 beta bands (around 20 and 30 Hz) was systematically 2-5 Hz lower during cue expectancy than during visuomotor integration and preparation. Furthermore, the frequency was directionally selective during preparation, with about 3 Hz difference between preferred and nonpreferred directions. Direction decoding with frequency gave similar accuracy as with beta power, and decoding accuracy improved significantly when combining power and frequency, suggesting that frequency might provide an additional signal for brain-machine interfaces. In conclusion, multiple beta bands coexist in motor cortex, and frequency modulations within each band are as behaviorally meaningful as power modulations, reflecting the changing behavioral context and the movement direction during preparation.     

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.