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.     

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.     

Attention modulates responses to motion reversals in human visual cortex

Selective attention modulates brain responses in visual cortex. A common finding, using functional magnetic resonance imaging or event-related potentials, is that responses to attended relative to unattended stimuli are potentiated. We report an exceptional circumstance in a motion-processing paradigm. Participants viewed superimposed stationary and moving dots and were instructed to attend to one or the other subset. Changes in the direction of dot motion triggered an event-related potential over posterior scalp sites, with a prominent negative peak at 200 ms that was larger when attention was directed at the stationary dots. This effect was localized to extrastriate visual cortex and may be due to reflexive effects of attention orienting triggered by unattended peripheral motion.     

Pre-target activity in visual cortex predicts behavioral performance on spatial and feature attention tasks

Physiological studies in humans and monkeys have revealed that, in response to an instruction to attend, areas of sensory cortex that code the attributes of the expected stimulus exhibit increases in neural activity prior to the arrival of the stimulus. Models of selective visual attention posit that these increases in activity give attended stimuli a processing advantage over distracting stimuli. Here, we test two key predictions of this view by using functional magnetic resonance imaging to record human brain activity during a cued voluntary orienting task. First, we tested whether pre-stimulus modulations are observed during both cued spatial and cued feature attention. Secondly, we tested whether the magnitude of pre-stimulus modulations predicts behavioral performance. Our results indicate that cue-triggered expectation of targets with particular spatial or nonspatial features activates areas of the visual cortex selective for these features. Furthermore, the magnitude of the cue-triggered modulations correlated with behavioral measures, such that those subjects who exhibited relatively large pre-stimulus modulations of activity performed better on the behavioral task. These findings support the view that top-down control systems bias activity in sensory cortices to favor the processing of expected target features and that this bias is related to behavior.     

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.     

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.     

Cross‐modal decoupling in temporal attention

Prior studies have repeatedly reported behavioural benefits to events occurring at attended, compared to unattended, points in time. It has been suggested that, as for spatial orienting, temporal orienting of attention spreads across sensory modalities in a synergistic fashion. However, the consequences of cross‐modal temporal orienting of attention remain poorly understood. One challenge is that the passage of time leads to an increase in event predictability throughout a trial, thus making it difficult to interpret possible effects (or lack thereof). Here we used a design that avoids complete temporal predictability to investigate whether attending to a sensory modality (vision or touch) at a point in time confers beneficial access to events in the other, non‐attended, sensory modality (touch or vision, respectively). In contrast to previous studies and to what happens with spatial attention, we found that events in one (unattended) modality do not automatically benefit from happening at the time point when another modality is expected. Instead, it seems that attention can be deployed in time with relative independence for different sensory modalities. Based on these findings, we argue that temporal orienting of attention can be cross‐modally decoupled in order to flexibly react according to the environmental demands, and that the efficiency of this selective decoupling unfolds in time.     

Attention and sensory interactions within the occipital cortex in the early blind: an fMRI study

Visual deprivation early in life results in occipital cortical responsiveness across a broad range of perceptual and cognitive tasks. In the reorganized occipital cortex of early blind (EB) individuals, the relative lack of specificity for particular sensory stimuli and tasks suggests that attention effects may play a prominent role in these areas. We wished to establish whether occipital cortical areas in the EB were responsive to stimuli across sensory modalities (auditory, tactile) and whether these areas maintained or altered their activity as a function of selective attention. Using a three-stimulus oddball paradigm and event-related functional magnetic resonance imaging, auditory and tactile tasks presented separately demonstrated that several occipital regions of interest (ROIs) in the EB, but not sighted controls (SCs), responded to targets and task-irrelevant distracter stimuli of both modalities. When auditory and tactile stimuli were presented simultaneously with subjects alternating attention between sensory streams, only the calcarine sulcus continued to respond to stimuli in both modalities. In all other ROIs, responses to auditory targets were as large or larger than those observed in the auditory-alone condition, but responses to tactile targets were attenuated or abolished by the presence of unattended auditory stimuli. Both auditory and somatosensory cortices responded consistently to auditory and tactile targets, respectively. These results reveal mechanisms of orienting and selective attention within the visual cortex of EB individuals and suggest that mechanisms of enhancement and suppression interact asymmetrically on auditory and tactile streams during bimodal sensory presentation.     

Effects of feature and spatial attention on visual change detection

In event-related brain potential studies using a visual S1-S2 matching task, stimulus changes elicit change-related positivity, which reflects the detection of visual changes. To investigate the effects of attention on change detection, we tested the elicitation of change-related positivity in response to changes in color and spatial frequency under three attention conditions: (i) changes in an unattended feature at an attended location, (ii) in an attended feature at an unattended location, and (iii) in an unattended feature at an unattended location. The results suggest that stimulus changes can be detected even when both feature and spatial attention are withdrawn, but change detection can also be inhibited, which might be because of biased-competition determined by the combination of feature and spatial attention conditions.     

Investigating category‐ and shape‐selective neural processing in ventral and dorsal visual stream under interocular suppression

Recent behavioral and neuroimaging studies using continuous flash suppression (CFS) have suggested that action‐related processing in the dorsal visual stream might be independent of perceptual awareness, in line with the “vision‐for‐perception” versus “vision‐for‐action” distinction of the influential dual‐stream theory. It remains controversial if evidence suggesting exclusive dorsal stream processing of tool stimuli under CFS can be explained by their elongated shape alone or by action‐relevant category representations in dorsal visual cortex. To approach this question, we investigated category‐ and shape‐selective functional magnetic resonance imaging‐blood‐oxygen level‐dependent responses in both visual streams using images of faces and tools. Multivariate pattern analysis showed enhanced decoding of elongated relative to non‐elongated tools, both in the ventral and dorsal visual stream. The second aim of our study was to investigate whether the depth of interocular suppression might differentially affect processing in dorsal and ventral areas. However, parametric modulation of suppression depth by varying the CFS mask contrast did not yield any evidence for differential modulation of category‐selective activity. Together, our data provide evidence for shape‐selective processing under CFS in both dorsal and ventral stream areas and, therefore, do not support the notion that dorsal “vision‐for‐action” processing is exclusively preserved under interocular suppression. Hum Brain Mapp,36:137–149, 2015. © 2014 Wiley Periodicals, Inc .     

An ERP investigation on visuotactile interactions in peripersonal and extrapersonal space: evidence for the spatial rule

The spatial rule of multisensory integration holds that cross-modal stimuli presented from the same spatial location result in enhanced multisensory integration. The present study investigated whether processing within the somatosensory cortex reflects the strength of cross-modal visuotactile interactions depending on the spatial relationship between visual and tactile stimuli. Visual stimuli were task-irrelevant and were presented simultaneously with touch in peripersonal and extrapersonal space, in the same or opposite hemispace with respect to the tactile stimuli. Participants directed their attention to one of their hands to detect infrequent tactile target stimuli at that hand while ignoring tactile targets at the unattended hand, all tactile nontarget stimuli, and any visual stimuli. Enhancement of ERPs recorded over and close to the somatosensory cortex was present as early as 100 msec after onset of stimuli (i.e., overlapping with the P100 component) when visual stimuli were presented next to the site of tactile stimulation (i.e., perihand space) compared to when these were presented at different locations in peripersonal or extrapersonal space. Therefore, this study provides electrophysiological support for the spatial rule of visual-tactile interaction in human participants. Importantly, these early cross-modal spatial effects occurred regardless of the locus of attention. In addition, and in line with previous research, we found attentional modulations of somatosensory processing only to be present in the time range of the N140 component and for longer latencies with an enhanced negativity for tactile stimuli at attended compared to unattended locations. Taken together, the pattern of the results from this study suggests that visuotactile spatial effects on somatosensory processing occur prior and independent of tactile-spatial attention.     

Effects of hand posture on preparatory control processes and sensory modulations in tactile-spatial attention.

OBJECTIVE: Event-related brain potentials (ERPs) were measured to investigate spatial coordinate systems involved in the control of preparatory tactile-spatial orienting, and in subsequent attentional modulations of somatosensory processing. METHODS: On each trial, a visual precue directed attention to the left or right hand, where infrequent tactile targets had to be detected. Hands were positioned either close together or wide apart. ERPs were recorded in the cue-target interval and in response to attended and unattended tactile non-targets. RESULTS: A frontal anterior directing attention negativity (ADAN) and a posterior late directing attention positivity (LDAP) were elicited in the cue-target interval contralateral to the direction of an attentional shift. The ADAN was unaffected by hand posture, but the LDAP was attenuated when hands were close together. N140 amplitudes were enhanced in response to tactile stimuli presented to the attended hand, and this effect was more pronounced when hands were wide apart. CONCLUSIONS: ADAN and LDAP are linked to separable anterior and posterior attentional control systems, which use coordinate systems based on somatotopic and external space, respectively. Effects of spatial attention on somatosensory stimulus processing are affected by variations in body posture. SIGNIFICANCE: Our results demonstrate that representations of body locations in external space play a central role in the control of tactile attention.     

The neuropsychological profile of early and continuously treated phenylketonuria: orienting,vigilance, and maintenance versus manipulation-functions of working memory

In this paper, we review neuropsychological test results of early and continuously treated Phenylketonuria (PKU) patients. To increase insight into the neuropsychological profile of this population, we have attempted to place the results within an attentional network model [Images of the mind, 1994], which proposes interacting but dissociable attentional networks for orienting, vigilance, and executive control of attention. Executive control of attention is discussed against the background of the process-specific theory of working memory (WM) [Handbook of neuropsychology, 1994], which postulates a distinction between the 'maintenance'-function of WM and the 'manipulation and monitoring'-function.Neuropsychological results are presented for 67 early and continuously treated PKU patients and 73 controls aged 7-14 years. Four neuropsychological tasks were employed to measure orienting, mnemonic processing, interference suppression, and top-down control in visual search. No differences were found in orienting and the maintenance-function of WM. In addition to previously reported impairments in sustained attention/vigilance and inhibition of prepotent responding, PKU patients exhibited deficits when top-down control was required in a visual search task, but showed no impairment when interference suppression was required. It is discussed how the specific neuropsychological impairments in PKU may be a consequence of mid-dorsolateral prefrontal cortex (DLPFC) dysfunctioning due to deficiencies in catecholamine modulation.     

Can attention be directed to opposite locations in different modalities? An ERP study.

OBJECTIVES: An event-related brain potential (ERP) study investigated whether spatially selective processing in vision and audition is controlled by a single supramodal system or by independent modality-specific systems. METHODS: Event-related brain potentials were recorded in response to visual and auditory stimuli at attended and unattended locations. In the 'Attend Same' condition, attention was directed to a single location in both modalities, while in the 'Attend Opposite' condition, visual and auditory attention had to be directed into opposite directions. RESULTS: Sensory-specific effects of attention on visual and auditory ERPs reflecting attentional modulations of perceptual processing were obtained in the 'Attend Same' condition, but not the 'Attend Opposite' condition. Beyond 200 ms post-stimulus, attentional ERP effects were also found in the 'Attend Opposite' condition. CONCLUSION: Results are inconsistent with the view that spatially selective processing is controlled by independent modality-specific systems. Effects of spatial attention on visual and auditory perceptual processing are closely linked, suggesting the existence of a supramodal attentional control system. At post-perceptual levels, attentional control may be more flexible.     

Orienting attention to instants in time

My colleagues and I have investigated whether the temporal framework can be used to guide selective attention, and have applied non-invasive methodology to reveal the brain systems and mechanisms involved. Our findings show that we are able to orient attention selectively to different points in time, enhancing behavioral performance. These effects are mediated by a left-hemisphere dominant parietal-frontal system, which partially overlaps with the networks involved in spatial orienting. The neural system for temporal orienting also includes brain areas associated with motor preparation and anticipation, suggesting that sensorimotor areas with different specializations can contribute to attentional orienting depending on the stimulus attributes guiding selection. The optimization of behavior by temporal orienting involves enhancement of the latency and amplitude of event-related potentials that are associated with motor responses and decisions. The effects are distinct from those during visual spatial attention, indicating that behavioral advantages can be conferred by multiple types of neural mechanisms. Taken together, the findings illustrate the flexibility of attentional functions in the human brain.     

Visual-spatial attention in developmental dyslexia

Orienting and focusing of visual attention are two processes strictly involved in reading. They were studied in a group of dyslexic children and normal readers. Shifting of attention by both peripheral and central visual cues was studied by means of the covert orienting paradigm. Focusing, consisting in the ability to control the size of the attentional focus, was investigated using simple reaction times in central vision. Results showed that dyslexics had a specific disability in the shifting of attention caused by a peripheral cue at short SOAs, and were also able to maintain attention focused for short periods of time only, presumably not long enough for efficient visual processing. Our results support the suggestion that visual selective attention deficits in disabled readers may be due to a specific difficulty in orienting and focusing.     

Orienting auditory spatial attention engages frontal eye fields and medial occipital cortex in congenitally blind humans

What happens in vision-related cortical areas when congenitally blind (CB) individuals orient attention to spatial locations? Previous neuroimaging of sighted individuals has found overlapping activation in a network of frontoparietal areas including frontal eye fields (FEF), during both overt (with eye movement) and covert (without eye movement) shifts of spatial attention. Since voluntary eye movement planning seems irrelevant in CB, their FEF neurons should be recruited for alternative functions if their attentional role in sighted individuals is only due to eye movement planning. Recent neuroimaging of the blind has also reported activation in medial occipital areas, normally associated with visual processing, during a diverse set of non-visual tasks, but their response to attentional shifts remains poorly understood. Here, we used event-related fMRI to explore FEF and medial occipital areas in CB individuals and sighted controls with eyes closed (SC) performing a covert attention orienting task with endogenous verbal cues and spatialized auditory targets. We found robust stimulus-locked FEF activation of all CB subjects, similar to and stronger than in SC, suggesting that FEF plays a role in endogenous orienting of covert spatial attention even in individuals in whom voluntary eye movements are irrelevant. We also found robust activation in bilateral medial occipital cortex in CB but not in SC subjects. The response decreased below baseline following endogenous verbal cues but increased following auditory targets, suggesting that the medial occipital area in CB does not directly engage during cued orienting of attention but may be recruited for processing of spatialized auditory targets.     

Spatial attention can modulate audiovisual integration at multiple cortical and subcortical sites

The role of attention in multisensory integration (MI) is presently uncertain, with some studies supporting an automatic, pre-attentive process and others suggesting possible modulation through selective attention. The goal of this functional magnetic resonance imaging study was to investigate the role of spatial attention on the processing of congruent audiovisual speech stimuli (here indexing MI). Subjects were presented with two simultaneous visual streams (speaking lips in the left and right visual hemifields) plus a single central audio stream (spoken words). In the selective attention conditions, the auditory stream was congruent with one of the two visual streams. Subjects attended to either the congruent or the incongruent visual stream, allowing the comparison of brain activity for attended vs. unattended MI while the amount of multisensory information in the environment and the overall attentional requirements were held constant. Meridian mapping and a lateralized 'speaking-lips' localizer were used to identify early visual areas and to localize regions responding to contralateral visual stimulations. Results showed that attention to the congruent audiovisual stimulus resulted in increased activation in the superior temporal sulcus, striate and extrastriate retinotopic visual cortex, and superior colliculus. These findings demonstrate that audiovisual integration and spatial attention jointly interact to influence activity in an extensive network of brain areas, including associative regions, early sensory-specific visual cortex and subcortical structures that together contribute to the perception of a fused audiovisual percept.     

The effect of variability of unattended information on global and local processing: evidence for lateralization at early stages of processing

Visual objects can often be analyzed as hierarchical in structure, composed of local elements that are spatially arranged to form a global shape. The brain mechanisms involved in the analysis of hierarchical figures have been under considerable scrutiny in recent years, and one of the many interesting features that have emerged is that there is an asymmetry across the two hemispheres for global (right hemisphere) vs local (left hemisphere) processing. Event-related potentials (ERP) were used to examine selective attention to global or local levels of hierarchical figures to determine the stage of processing at which the asymmetry first emerges. Two conditions were tested, one in which unattended information was variable from trial to trial, and one in which it was not. The variability of unattended information influenced the lateralization of processing. Presentation of invariable, neutral distractors resulted in global/local processing asymmetries at early stages (P1). In contrast, presentation of variable, task-relevant distractors resulted in processing asymmetries that occurred at much later stages (N2). Our hypothesis is that lateralized enhancement of neural populations in extrastriate cortex results from both selective attention to locations in the visual field, as well as selective attention to global or local information. We suggest that unattended information that varies from trial to trial is processed in parallel with attended information, masking hemisphere biases for local vs global information at early stages of processing.