Parietal disruption impairs reflexive spatial attention within and between sensory modalities

Reflexive spatial attention is critical for controlling perception and action. An established body of evidence suggests that mechanisms of spatial attention operate both within and between sensory modalities; however the attentional mechanisms that link modalities in the human brain are unclear. Here we used transcranial magnetic stimulation (TMS) to explore the role of the parietal cortex in coordinating reflexive shifts of spatial attention between vision and touch. In two experiments, healthy participants localised visual and somatosensory targets that were preceded by non-informative visual or somatosensory spatial cues. To determine the role of parietal cortex in spatial orienting, TMS was delivered synchronously with cue onset for 100 ms. Results revealed a critical role of the right angular gyrus and supramarginal gyrus in reflexive orienting to visual and somatosensory targets that followed a somatosensory cue. In contrast, the same TMS protocol was ineffective in modulating reflexive orienting based on visual cues. This dependence on cue modality may reflect subcortical redundancy of visual orienting mechanisms. Overall, our results indicate a critical role of the inferior parietal cortex in mediating reflexive shifts of attention within and between sensory modalities.     

Orienting attention to points in time improves stimulus processing both within and across modalities

Spatial attention affects the processing of stimuli of both a task-relevant and a task-irrelevant modality. The present study investigated if similar cross-modal effects exist when attention is oriented to a point in time. Short (600 msec) and long (1,200 msec) empty intervals, marked by a tactile onset and an auditory or a tactile offset marker, were presented. In each block, the participants had to attend one interval and one modality. Event-related potentials (ERPs) to auditory and tactile offset markers of attended as compared to unattended intervals were characterized by an enhancement of early negative deflections of the auditory and somatosensory ERPs (audition, 100-140 msec; touch, 130-180 msec) when audition or touch was task relevant, respectively. Similar effects were found for auditory stimuli when touch was task relevant. An additional reaction time experiment revealed faster responses to both auditory and tactile stimuli at the attended as compared to the unattended point in time, irrespective of which modality was primary. Both behavioral and ERP data show that attention can be focused on a point in time, which results in a more efficient processing of auditory and tactile stimuli. The ERP data further suggest that a relative enhancement at perceptual processing stages contributes to the processing advantage for temporally attended stimuli. The existence of cross-modal effects of temporal attention underlines the importance of time as a feature for binding input across different modalities.     

Spatial attention and crossmodal interactions between vision and touch

In the present paper, we review several functional imaging studies investigating crossmodal interactions between vision and touch relating to spatial attention. We asked how the spatial unity of a multimodal event in the external world might be represented in the brain, where signals from different modalities are initially processed in distinct brain regions. The results highlight several links between visual and tactile spatial representations. First, we found that activity in the anterior part of the intraparietal sulcus was influenced by stimulus position independently of the modality of the stimulation. This is consistent with crossmodal interactions via sensory convergence from early modality-specific spatial maps to higher-order multimodal regions. Second, we found that stimulation in, or attention to, one modality could affect activity in areas dedicated to a different modality, in a spatially-specific manner. These spatial crossmodal effects in unimodal regions demonstrate congruous activity in anatomically distant brain areas that represent similar external locations, implicating a distributed network of spatial representations in crossmodal integration. Finally, the results suggest that the temporo-parietal junction may be involved in aspects of controlling spatial attention, for both vision and touch. A multimodal attentional system may influence activity in distinct brain areas representing common regions of space for different modalities, thus suggesting a link between spatial attention and crossmodal integration.     

An event‐related FMRI study of exogenous orienting across vision and audition

The orienting of attention to the spatial location of sensory stimuli in one modality based on sensory stimuli presented in another modality (i.e., cross‐modal orienting) is a common mechanism for controlling attentional shifts. The neuronal mechanisms of top‐down cross‐modal orienting have been studied extensively. However, the neuronal substrates of bottom‐up audio‐visual cross‐modal spatial orienting remain to be elucidated. Therefore, behavioral and event‐related functional magnetic resonance imaging (FMRI) data were collected while healthy volunteers (N = 26) performed a spatial cross‐modal localization task modeled after the Posner cuing paradigm. Behavioral results indicated that although both visual and auditory cues were effective in producing bottom‐up shifts of cross‐modal spatial attention, reorienting effects were greater for the visual cues condition. Statistically significant evidence of inhibition of return was not observed for either condition. Functional results also indicated that visual cues with auditory targets resulted in greater activation within ventral and dorsal frontoparietal attention networks, visual and auditory “where” streams, primary auditory cortex, and thalamus during reorienting across both short and long stimulus onset asynchronys. In contrast, no areas of unique activation were associated with reorienting following auditory cues with visual targets. In summary, current results question whether audio‐visual cross‐modal orienting is supramodal in nature, suggesting rather that the initial modality of cue presentation heavily influences both behavioral and functional results. In the context of localization tasks, reorienting effects accompanied by the activation of the frontoparietal reorienting network are more robust for visual cues with auditory targets than for auditory cues with visual targets. Hum Brain Mapp 35:964–974, 2014. © 2013 Wiley Periodicals, Inc.     

Intersensory selective attention and temporal orienting operate in parallel and are instantiated in spatially distinct sensory and motor cortices

Knowledge about the sensory modality in which a forthcoming event might occur permits anticipatory intersensory attention. Information as to when exactly an event occurs enables temporal orienting. Intersensory and temporal attention mechanisms are often deployed simultaneously, but as yet it is unknown whether these processes operate interactively or in parallel. In this human electroencephalography study, we manipulated intersensory attention and temporal orienting in the same paradigm. A continuous stream of bisensory visuo‐tactile inputs was presented, and a preceding auditory cue indicated to which modality participants should attend (visual or tactile). Temporal orienting was manipulated blockwise by presenting stimuli either at regular or irregular intervals. Using linear beamforming, we examined neural oscillations at virtual channels in sensory and motor cortices. Both attentional processes simultaneously modulated the power of anticipatory delta‐ and beta‐band oscillations, as well as delta‐band phase coherence. Modulations in sensory cortices reflected intersensory attention, indicative of modality‐specific gating mechanisms. Modulations in motor and partly in somatosensory cortex reflected temporal orienting, indicative of a supramodal preparatory mechanism. We found no evidence for interactions between intersensory attention and temporal orienting, suggesting that these two mechanisms act in parallel and largely independent of each other in sensory and motor cortices. Hum Brain Mapp 36:3246–3259, 2015. © 2015 Wiley Periodicals, Inc.     

Age-related changes in the attentional control of visual cortex: a selective problem in the left visual hemifield

To what extent does our visual-spatial attention change with age? In this regard, it has been previously reported that relative to young controls, seniors show delays in attention-related sensory facilitation. Given this finding, our study was designed to examine two key questions regarding age-related changes in the effect of spatial attention on sensory-evoked responses in visual cortex--are there visual field differences in the age-related impairments in sensory processing, and do these impairments co-occur with changes in the executive control signals associated with visual spatial orienting? Therefore, our study examined both attentional control and attentional facilitation in seniors (aged 66-74 years) and young adults (aged 18-25 years) using a canonical spatial orienting task. Participants responded to attended and unattended peripheral targets while we recorded event-related potentials (ERPs) to both targets and attention-directing spatial cues. We found that not only were sensory-evoked responses delayed in seniors specifically for unattended events in the left visual field as measured via latency shifts in the lateral occipital P1 elicited by visual targets, but seniors also showed amplitude reductions in the anterior directing attentional negativity (ADAN) component elicited by cues directing attention to the left visual field. At the same time, seniors also had significantly higher error rates for targets presented in the left vs. right visual field. Taken together, our data thus converge on the conclusion that age-related changes in visual spatial attention involve both sensory-level and executive attentional control processes, and that these effects appear to be strongly associated with the left visual field.     

Peripheral oculomotor palsy affects orienting of visuospatial attention.

Patients affected by VI cranial nerve palsy were required to orient their attention in monocular vision and to detect a stimulus appearing either in attended or in unattended locations. Results showed that while during non-paretic eye vision stimulus detection in the attended location was faster than that in the unattended one, during paretic eye vision no difference in detection speed was present. However, in this latter condition, detection speed in both attended and un attended locations were as fast as that measured during non-paretic eye vision in attended location. Demonstration that peripheral oculomotor impairment influences monocular covert orienting of visuospatial attention strongly support the idea that visuospatial attention and oculomotor mechanisms share similar cortical networks.     

Orienting and maintenance of spatial attention in audition and vision: an event-related brain potential study

We examined the effects of orienting and maintenance of attention on performance and event-related brain potentials (ERPs) in audition and vision. Our subjects selectively attended to sounds or pictures in one location (Maintenance of attention) or alternated the focus of their auditory or visual attention between left and right locations (Orienting of attention) in order to detect and press a response button to infrequent targets among the attended stimuli. Reaction times were longer in the Auditory Orienting condition and hit rates were lower and false alarm rates higher in the Visual Orienting condition than in the corresponding Maintenance conditions. Comparison of ERPs to the attended and unattended stimuli in the Auditory and Visual Orienting and Maintenance conditions revealed attention-related modulations of ERPs. In each modality, ERPs to attended stimuli were negatively displaced in relation to unattended stimuli at 100-250 ms from stimulus onset. These negative differences (Nds) showed modality-specific distributions and they were larger over the hemisphere contralateral to the attended sounds and pictures than over the ipsilateral hemisphere. Moreover, the Nd was larger in the Auditory Orienting condition than in the Auditory Maintenance condition, while no such difference was observed in the visual modality. In addition to the Nd, attended visual stimuli elicited a late positive response (LPR) in both Orienting and Maintenance conditions. In contrast to our recent functional magnetic resonance imaging (fMRI) study employing the same experimental paradigm and indicating orienting-related activity in the frontal and parietal cortices, no ERP responses specifically related to orienting were found in either modality.     

Audio-visual dynamic remapping in an endogenous spatial attention task

Several studies on cross-modal attention showed that remapping processes between sensory modalities occur in the spatial orienting of attention. One hypothesis that accounts for such links is that spatial attention operates upon representations of common locations in the external space. However, convincing evidence only exists for cross-modal links in spatial orienting, leaving the dynamics of these effects unexplored. Four experiments were designed to cope with this issue by having participants being involved in an endogenous orienting task to visual and auditory target stimuli. Targets on invalid trials were embedded into two different kinds of sequences of stimuli: (1) long sequences, wherein three valid trials in one modality preceded the invalid trial in the other modality; (2) short sequences, wherein only one valid trial in one modality preceded the invalid trial in the other modality. Results revealed modality-specific meridian effects in the short sequences, and a significant decrement of the modality-specific meridian effect in the long sequences. The results of these experiments indicate that cross-modal links in visual and auditory spatial attention are based on representations of common locations in the external space across sensory modalities. Moreover, the results strongly support the hypothesis that representations of space are dynamically built and updated according to task demands.     

Attentional orienting towards emotion: P2 and N400 ERP effects

Attention can be oriented to different spatial locations yielding faster processing of attended compared to unattended stimuli. Similarly attention can be oriented to a semantic category such as “animals” or “tools”. Words from the attended category will also be recognized faster than words from an unattended category. Here, we asked whether it is possible to orient attention to an emotional category, for example, “negative emotional stimuli”. Furthermore, we investigated which mechanisms facilitate processing of attended stimuli. In an attentional orienting paradigm in which cues are informative with regard to the spatial location, semantic category, or emotional category of subsequent target words, we found attention effects in all three cue conditions. Words at attended locations or of the attended semantic or emotional category were responded to faster than unattended categories. While spatial attention acted upon early visual processing and amplified occipital N1-P2 potentials, semantic cues modulated the N400 amplitude indexing semantic processing. Emotional cues also yielded an N400 modulation; however, in addition, a left anterior P2 effect was observed. The data clearly show that attention can be oriented to emotional categories. Emotional orienting yields facilitated processing of an attended emotional category through the modulation of early and late word processing stages.     

Cross-modal selective attention to visual and auditory stimuli modulates endogenous ERP components

In two experiments event-related potentials (ERPs) to visual and auditory stimuli were measured in 12 healthy subjects. A cross-modal and delayed response paradigm was used that allows ERPs to be obtained separately to attended and unattended stimuli under conditions in which unattended stimuli are less likely to be covertly or randomly attended. The results showed: (1) N1 enhancement with attention for standard stimuli in auditory and visual modalities and for deviant stimuli in the visual modality; (2) The onset time and scalp distribution of both the N1 for attend condition and Nd1 were similar regardless of standard or deviant stimuli in the auditory and visual modality; the onset time of Nd1 elicited by auditory and visual deviant stimuli was earlier than that of the unattended N1, and their scalp distributions were different; and (3) The Nd1 components elicited by auditory and visual deviant stimuli were distributed over the respective primary sensory areas, but Nd1 components evoked by auditory and visual standard stimuli were distributed over the frontal scalp. These results suggest that the attended N1 enhancement is primarily caused by a component with endogenous origins and that the early attention effect occurs before the exogenous components. The results support the view that the cross-modal attention to deviant stimuli modulates modality-specific processing in the brain, whereas attention to standard stimuli affects modality-nonspecific or supramodal brain systems.     

The neural circuitry underlying the executive control of auditory spatial attention

Although a fronto-parietal network has consistently been implicated in the control of visual spatial attention, the network that guides spatial attention in the auditory domain is not yet clearly understood. To investigate this issue, we measured brain activity using functional magnetic resonance imaging while participants performed a cued auditory spatial attention task. We found that cued orienting of auditory spatial attention activated a medial-superior distributed fronto-parietal network. In addition, we found cue-triggered increases of activity in the auditory sensory cortex prior to the occurrence of an auditory target, suggesting that auditory attentional control operates in part by biasing processing in sensory cortex in favor of expected target stimuli. Finally, an exploratory cross-study comparison further indicated several common frontal and parietal regions as being involved in the control of both visual and auditory spatial attention. Thus, the present findings not only reveal the network of brain areas underlying endogenous spatial orienting in the auditory modality, but also suggest that the control of spatial attention in different sensory modalities is enabled in part by some common, supramodal neural mechanisms.     

Temporal attention enhances early visual processing: a review and new evidence from event-related potentials

Two fundamental cognitive functions, selective attention and processing of time, have been simultaneously explored in recent studies of temporal orienting of attention. A temporal-orienting procedure may consist of a temporal analogue to the Posner's paradigm, such that symbolic cues indicate the most probable moment for target arrival. Behavioral measures suggest that performance is improved for events appearing at expected vs. unexpected moments. However, there is no agreement on the locus of stimulus processing at which temporal attention operates. Thus, it remains unclear whether early perceptual or just late motor processes can be modulated. This article reviews current ERP research on temporal orienting, with an emphasis on factors that might determine the modulation of temporal orienting at early stages of processing. We conclude that: First, late components (N2 and P300) are consistently modulated by temporal orienting, which suggests attentional preparation of decision and/or motor processes. Second, early components (e.g., N1) seem to be modulated only when the task is highly demanding in perceptual processing. Hence, we conducted an ERP experiment which aimed to observe a modulation of early visual processing by using a perceptually demanding task, such as letter discrimination. The results show, for the first time, that targets appearing at attended moments elicited a larger P1 component than unattended targets. Moreover, temporal attention modulated the amplitude and latency of N2 and P300 components. This suggests that temporal orienting of attention not only modulates late motor processing, but also early visual processing when perceptually demanding tasks are used.     

Influence of gaze direction on crossmodal modulation of visual ERPS by endogenous tactile spatial attention

Recent evidence indicates that the spatial direction of endogenous covert spatial attention in one sensory modality can crossmodally influence early processing of stimuli in a different modality. However, spatial locations are initially coded according to different frames of reference for different modalities (e.g., body-centered for touch versus retinocentric vision) and postural changes (e.g., gaze shifts) will realign these. Here, we used event-related potentials (ERPs) to investigate how the direction of endogenous tactile attention affects sensory-specific visual ERP components. Critically, by manipulating direction of gaze, we were able to test whether any crossmodal effects depend on visual and tactile projections to a common hemisphere, on common locations in external space, or on some combination of the two. We found that both P1 and N1 visual components were modulated according to the direction of endogenous tactile attention. While the P1 crossmodal effect followed purely hemispheric constraints, the attentional modulation of N1 appeared to combine both anatomical and external spatial constraints.     

A modified oddball paradigm "cross-modal delayed response" and the research on mismatch negativity

A modified oddball paradigm was developed to facilitate the focus of attention and to minimize target effects on deviant-related components of auditory and visual event-related potentials (ERPs) elicited with long interstimulus intervals. Subjects were required to focus on either the visual or auditory stimulus in each stimulus block. Deviant-related components were obtained by subtracting ERPs of the standard stimulus from that of the deviant stimulus for each modality with each stimulus condition. Results showed that auditory mismatch negativity (MMN) and a visual early deviant related negativity (DRN1) were elicited both when stimuli were attended and unattended. In contrast, N2b and P3 were produced only under the attended condition. In comparison of attended MMN and unattended MMN at three time windows (100-150 ms, 150-200 ms, and 200-250 ms) of MMN zone, different scalp distributions were shown, depending on the time windows. This result suggests that the attended auditory MMN is a mixed wave, consisting of genuine MMN, N2b, and possible P165. The effect of attention on MMN may stem from the contamination of these overlapping components. With the present paradigm, at least three sensory memory traces have to be maintained simultaneously in multiple sensory modalities to support automatic processing.     

Tri-modal integration of visual, tactile and auditory signals for the perception of sequences of events

We investigated the interactions between visual, tactile and auditory sensory signals for the perception of sequences of events. Sequences of flashes, taps and beeps were presented simultaneously. For each session, subjects were instructed to count the number of events presented in one modality (Target) and to ignore the stimuli presented in the other modalities (Background). The number of events presented in the background sequence could differ from the number of events in the target sequence. For each session, we quantified the Background-evoked bias by comparing subjects' responses with and without Background (Target presented alone). Nine combinations between vision, touch and audition were tested. In each session but two, the Background significantly biased the Target. Vision was the most susceptible to Background-evoked bias and the least efficient in biasing the other two modalities. By contrast, audition was the least susceptible to Background-evoked bias and the most efficient in biasing the other two modalities. These differences were strongly correlated to the relative reliability of each modality. In line with this, the evoked biases were larger when the Background consisted of two instead of only one modality. These results show that for the perception of sequences of events: (1) vision, touch and audition are automatically integrated; (2) the respective contributions of the three modalities to the integrated percept differ; (3) the relative contribution of each modality depends on its relative reliability (1/variability); (4) task-irrelevant stimuli have more weight when presented in two rather than only one modality.     

Mechanisms of selective inhibition in visual spatial attention are indexed by alpha-band EEG synchronization

Electroencephalographic studies in humans have demonstrated that orienting of visual attention induces a decrease in oscillatory alpha-band activity (alpha-desynchronization) over cortical areas tuned to the attended visual space. This is interpreted as reflecting intentionally enhanced excitability of these areas to facilitate upcoming visual processing. However, the inverse mechanism might also apply. Brain areas that process task-irrelevant space might be actively suppressed by increased alpha-activity (alpha-synchronization) to protect against input of distracter information. In the present study, we demonstrate that such suppression mechanisms are highly selective and are taking place even without distracters that need to be ignored. During voluntary orienting of attention, we found alpha-synchronization to dominate over desynchronization, to be topographically specific for each of eight attention positions, and to occur over areas processing unattended space in a retinotopically organized pattern. This indicates that alpha-synchronization is an important component of selective attention, serving active suppression of unattended positions during visual spatial orienting.     

Which aspects of visual attention are changed by deafness? The case of the Attentional Network Test

The loss of one sensory modality can lead to a reorganization of the other intact sensory modalities. In the case of individuals who are born profoundly deaf, there is growing evidence of changes in visual functions. Specifically, deaf individuals demonstrate enhanced visual processing in the periphery, and in particular enhanced peripheral visual attention. To further characterize those aspects of visual attention that may be modified by deafness, deaf and hearing individuals were compared on the Attentional Network Test (ANT). The ANT was selected as it provides a measure of the efficiency of three neurally distinct subsystems of visual attention: alerting, orienting and executive control. The alerting measure refers to the efficiency with which a temporal cue is used to direct attention towards a target event, and the orienting measure is an indicator of the efficiency with which a spatial cue focuses attention upon that target's spatial location. The executive control measure, on the other hand, is an indicator of the amount of interference from peripheral flankers on processing that central target. In two separate experiments, deaf and hearing individuals displayed similar alerting and orienting abilities indicating comparable attention across populations. As predicted by enhanced peripheral attention, deaf subjects were found to have larger flanker interference effects than hearing subjects. These results indicate that not all aspects of visual attention are modified by early deafness, suggesting rather specific effects of cross-modal plasticity.     

Top-down control of visual cortex in migraine populations

The pathophysiology of migraine includes a heightened excitability of visual cortex that persists between headache events and that has been linked to impaired inhibitory intracortical processes. Here we examined the hypothesis that this cortical pathophysiology would affect the top-down attentional control of visual cortex. We asked two groups of participants—migraineurs (N = 29) and non-migraine controls (N = 29)—to perform a probabilistic spatial orienting task as we measured visual sensory cortical responses via event-related potentials (ERPs). Data were then analyzed as a function of whether the ERP-eliciting stimulus was in the fovea vs. parafovea, and whether the stimulus’ location was attended or unattended. In this regard, we found two key between-groups differences in the effect of attention on sensory-evoked visual-cortical activity. First, relative to controls, migraineurs showed a larger attention effect in the visual N1 ERP component for events at the fovea. Second, unlike controls, migraineurs showed no early-phase attention effect in the P1 ERP component for events in the parafovea. Despite these altered ERP responses in migraineurs, however, corresponding behavioral data indicated that they also had heightened response performance. Taken together, our results support the hypothesis that migraineurs have an altered top-down attentional control of visual cortex, with the data suggesting that the effect may be tied to a reduced ability to suppress sensory-evoked activity for unattended events in the visual periphery.     

Orienting attention in time: behavioural and neuroanatomical distinction between exogenous and endogenous shifts

Temporal orienting of attention is the ability to focus resources at a particular moment in time in order to optimise behaviour, and is associated with activation of left parietal and premotor cortex [Coull, J. T., Nobre, A. C. Where and when to pay attention: the neural systems for directing attention to spatial locations and to time intervals as revealed by both PET and fMRI. Journal of Neuroscience, 1998, 18, 7426-7435]. In the present experiment, we explored the behavioural and anatomical correlates of temporal orienting to foveal visual stimuli, in order to eliminate any spatial attention confounds. We implemented a two-way factorial design in an event-related fMRI study to examine the factors of trial validity (predictability of target by cue), length of delay (cue-target interval), and their interaction. There were two distinct types of invalid trial: those where attention was automatically drawn to a premature target and those where attention was voluntarily shifted to a delayed time-point. Reaction times for valid trials were shorter than those for invalid trials, demonstrating appropriate allocation of attention to temporal cues. All trial-types activated a shared system, including frontoparietal areas bilaterally, showing that this network is consistently associated with attentional orienting and is not specific to spatial tasks. Distinct brain areas were sensitive to cue-target delays and to trial validity. Long cue-target intervals activated areas involved in motor preparation: supplementary motor cortex, basal ganglia and thalamus. Invalid trials, where temporal expectancies were breached, showed enhanced activation of left parietal and frontal areas, and engagement of orbitofrontal cortex bilaterally. Finally, trial validity interacted with length of delay. Appearance of targets prematurely selectively activated visual extrastriate cortex; while postponement of target appearance selectively activated right prefrontal cortex. These findings suggest that distinct brain areas are involved in redirecting attention based upon sensory events (bottom-up, exogenous shifts) and based upon cognitive expectations (top-down, endogenous shifts).