Atypical attentional filtering of visual information in youth with chromosome 22q11.2 deletion syndrome as indexed by event-related potentials.

BACKGROUND: Youth with chromosome 22q11.2 deletion syndrome (22q) face one of the highest genetic risk factors for the development of schizophrenia. Previous research suggests impairments in attentional control and potential interactions with elevated anxiety and reduced adaptive functioning may increase the risk for developing psychosis in this population. Here, we examined how variations in attentional control relate to the presence or severity of psychosis-proneness symptoms in these individuals. METHODS: To achieve this, we measured attentional control in youth (12-18 years) with 22q (N = 35) compared to a typically developing group (N = 45), using a flanker task (the Distractor Target task) while measuring neural activity with event-related potentials. RESULTS: Similar to previous findings observed in people with schizophrenia, greater attentional capture by, and reduced suppression of, non-target flanker stimuli characterized participants with 22q and was indexed by the N2pc (N2-posterior-contralateral) and PD (distractor positivity) components. Although we observed no relationships between these components and measures of psychosis-proneness in youth with 22q, these individuals endorsed a relatively low incidence of positive symptoms overall. CONCLUSIONS: Our results provide neural evidence of an attentional control impairment in youth with 22q that suggests these individuals experience sustained attentional focus on irrelevant information and reduced suppression of distracting stimuli in their environment. Impairments in attentional control might be a valid biomarker of the potential to develop attenuated positive symptoms or frank psychosis in high-risk individuals long before the age at which such symptoms typically arise. The evaluation of such a hypothesis, and the preventive potential for the putative biomarker, should be the focus of future studies.

Direct neurophysiological evidence for spatial suppression surrounding the focus of attention in vision.

The spatial focus of attention has traditionally been envisioned as a simple spatial gradient of enhanced activity that falls off monotonically with increasing distance. Here, we show with high-density magnetoencephalographic recordings in human observers that the focus of attention is not a simple monotonic gradient but instead contains an excitatory peak surrounded by a narrow inhibitory region. To demonstrate this center-surround profile, we asked subjects to focus attention onto a color pop-out target and then presented probe stimuli at various distances from the target. We observed that the electromagnetic response to the probe was enhanced when the probe was presented at the location of the target, but the probe response was suppressed in a narrow zone surrounding the target and then recovered at more distant locations. Withdrawing attention from the pop-out target by engaging observers in a demanding foveal task eliminated this pattern, confirming a truly attention-driven effect. These results indicate that neural enhancement and suppression coexist in a spatially structured manner that is optimal to attenuate the most deleterious noise during visual object identification.

How does attention attenuate target-distractor interference in vision?. Evidence from magnetoencephalographic recordings.

This study used magnetoencephalographic and electroencephalographic recordings to investigate the neural mechanisms that underlie the attentional resolution of ambiguous feature coding in visual search. We addressed this issue by comparing neural activity related to target discrimination under conditions of more versus less feature overlap between the target and distractor items. The results show that increasing feature overlap leads to a focal enhancement of neural activity in ventral occipito-temporal areas, consistent with the larger need to attenuate distractor interference. Furthermore, the results suggest that distractor attenuation proceeds as a stepwise operation, with different spatial locations containing interfering features being suppressed successively. These findings support theories of visual search that emphasize location-based attentional selection as a key mechanism in resolving ambiguous feature coding in vision.

Visual search remains efficient when visual working memory is full.

Many theories of attention have proposed that visual working memory plays an important role in visual search tasks. The present study examined the involvement of visual working memory in search using a dual-task paradigm in which participants performed a visual search task while maintaining no, two, or four objects in visual working memory. The presence of a working memory load added a constant delay to the visual search reaction times, irrespective of the number of items in the visual search array. That is, there was no change in the slope of the function relating reaction time to the number of items in the search array, indicating that the search process itself was not slowed by the memory load. Moreover, the search task did not substantially impair the maintenance of information in visual working memory. These results suggest that visual search requires minimal visual working memory resources, a conclusion that is inconsistent with theories that propose a close link between attention and working memory.

Storage of features, conjunctions and objects in visual working memory.

Working memory can be divided into separate subsystems for verbal and visual information. Although the verbal system has been well characterized, the storage capacity of visual working memory has not yet been established for simple features or for conjunctions of features. The authors demonstrate that it is possible to retain information about only 3-4 colors or orientations in visual working memory at one time. Observers are also able to retain both the color and the orientation of 3-4 objects, indicating that visual working memory stores integrated objects rather than individual features. Indeed, objects defined by a conjunction of four features can be retained in working memory just as well as single-feature objects, allowing many individual features to be retained when distributed across a small number of objects. Thus, the capacity of visual working memory must be understood in terms of integrated objects rather than individual features.

Neural sources of focused attention in visual search.

Previous studies of visual search in humans using event-related potentials (ERPs) have revealed an ERP component called 'N2pc' (180-280 ms) that reflects the focusing of attention onto potential target items in the search array. The present study was designed to localize the neuroanatomical sources of this component by means of magnetoencephalographic (MEG) recordings, which provide greater spatial precision than ERP recordings. MEG recordings were obtained with an array of 148 magnetometers from six normal adult subjects, one of whom was tested in multiple sessions so that both single-subject and group analyses could be performed. Source localization procedures revealed that the N2pc is composed of two distinct neural responses, an early parietal source (180-200 ms) and a later occipito-temporal source (220-240 ms). These findings are consistent with the proposal that parietal areas are used to initiate a shift of attention within a visual search array and that the focusing of attention is implemented by extrastriate areas of the occipital and inferior temporal cortex.

The visual N1 component as an index of a discrimination process.

Many previous studies have demonstrated that the visual N1 component is larger for attended-location stimuli than for unattended-location stimuli. This difference is observed typically only for tasks involving a discrimination of the attended-location stimuli, suggesting that the N1 wave reflects a discrimination process that is applied to the attended location. The present study tested this hypothesis by examining the N1 component elicited by attended stimuli under conditions that either required or did not require the subject to perform a discrimination. Specifically, the N1 elicited by foveal stimuli during choice-reaction time (RT) tasks was compared with the N1 elicited by identical stimuli during simple-RT tasks. In three experiments, a larger posterior N1 was observed in choice-RT tasks than in simple-RT tasks, even when several potential confounds were eliminated (e.g., arousal and motor preparation). This N1 discrimination effect was observed even when no motor response was required and was present for both color- and form-based discriminations. Moreover, this discrimination effect was equally large for easy and difficult discriminations, arguing against a simple resource-based explanation of the present results. Instead, the results of this study are consistent with the hypothesis that the visual N1 component reflects the operation of a discrimination process within the focus of attention.

What variety of attention is automatically captured by peripheral cues?

Previous studies have shown that the voluntary allocation of attention to a location in space can influence accuracy in two ways. First, additional processing resources can be allocated to the attended location, leading to an improvement in perceptual quality for objects presented at that location. Second, decision processes can be restricted to information arising from the attended location, which improves accuracy without influencing the perceptual representation. The present study examined the operation of these two attentional mechanisms when nonpredictive peripheral cues were used to capture attention automatically. Experiment 1 showed that, like predictive cues, nonpredictive cues influence accuracy by summoning perceptual resources and also by influencing decision processes. However, both the cues and the targets in this experiment were defined by luminance increments, making it possible that the cuing effects were mediated by a task-controlled attentional set rather than being fully automatic. Experiments 2 and 3 examined this possibility by using luminance-defined cues and color-defined targets; evidence was again obtained for both perceptual-level and decision-level attention effects. The capture of attention by a nonpredictive peripheral cue thus appears to influence both perceptual resource allocation and postperceptual decision processes.

Direct and indirect integration of event-related potentials, functional magnetic resonance images, and single-unit recordings.

Cognitive neuroimaging techniques vary along three primary dimensions: invasiveness, temporal resolution, and spatial resolution. Several of the major techniques excel on two of these three dimensions, but none of them excels on all three. In principle, multiple techniques with different strengths and weaknesses could be combined to obtain high temporal and spatial resolution data about human neural activity, and this article compares two approaches to combining microelectrode, hemodynamic, and electromagnetic measures of neural activity. The first approach involves using structural magnetic resonance images to provide a common reference frame for the mathematical estimation of neural activity, and the second approach involves parallel experimental manipulations and converging evidence. At present, neither approach is entirely satisfactory, and the integration of different measures of neural activity, therefore, requires a combination of direct and indirect approaches.

Electrophysiological measurement of rapid shifts of attention during visual search.

The perception of natural visual scenes that contain many objects poses computational problems that are absent when objects are perceived in isolation. Vision researchers have captured this attribute of real-world perception in the laboratory by using visual search tasks, in which subjects search for a target object in arrays containing varying numbers of non-target distractor objects. Under many conditions, the amount of time required to detect a visual search target increases as the number of objects in the stimulus array increases, and some investigators have proposed that this reflects the serial application of attention to the individual objects in the array. However, other investigators have argued that this pattern of results may instead be due to limitations in the processing capacity of a parallel processing system that identifies multiple objects concurrently. Here we attempt to address this longstanding controversy by using an electrophysiological marker of the moment-by-moment direction of attention-the N2pc component of the event-related potential waveform--to show that attention shifts rapidly among objects during visual search.

Electrophysiological evidence for a postperceptual locus of suppression during the attentional blink.

When an observer detects a target in a rapid stream of visual stimuli, there is a brief period of time during which the detection of subsequent targets is impaired. In this study, event-related potentials (ERPs) were recorded from normal adult observers to determine whether this "attentional blink" reflects a suppression of perceptual processes or an impairment in postperceptual processes. No suppression was observed during the attentional blink interval for ERP components corresponding to sensory processing (the P1 and N1 components) or semantic analysis (the N400 component). However, complete suppression was observed for an ERP component that has been hypothesized to reflect the updating of working memory (the P3 component). Results indicate that the attentional blink reflects an impairment in a postperceptual stage of processing.

Sensory gain control (amplification) as a mechanism of selective attention: electrophysiological and neuroimaging evidence.

Both physiological and behavioral studies have suggested that stimulus-driven neural activity in the sensory pathways can be modulated in amplitude during selective attention. Recordings of event-related brain potentials indicate that such sensory gain control or amplification processes play an important role in visual-spatial attention. Combined event-related brain potential and neuroimaging experiments provide strong evidence that attentional gain control operates at an early stage of visual processing in extrastriate cortical areas. These data support early selection theories of attention and provide a basis for distinguishing between separate mechanisms of attentional suppression (of unattended inputs) and attentional facilitation (of attended inputs).

Spatio-temporal dynamics of attention to color: evidence from human electrophysiology.

This study characterized patterns of brain electrical activity associated with selective attention to the color of a stimulus. Multichannel recordings of event-related potentials (ERPs) were obtained while subjects viewed randomized sequences of checkerboards consisting of isoluminant red or blue checks superimposed on a grey background. Stimuli were presented foveally at a rapid rate, and subjects were required to attend to the red or blue checks in separate blocks of trials and to press a button each time they detected a dimmer target stimulus of the attended color. An early negative ERP component with an onset latency of 50 ms was sensitive to stimulus color but was unaffected by the attentional manipulation. ERPs elicited by attended and unattended stimuli began to diverge after approximately 100 ms following stimulus onset. Inverse dipole modelling of the attended-minus-unattended difference waveform indicated that an initial positive deflection with an onset latency of 100 ms had a source in lateral occipital cortex, while a subsequent negative deflection with an onset at 160 ms had a source in inferior occipito-temporal cortex. Longer-latency attention-sensitive components were localized to premotor frontal areas (onset at 190 ms) and to more anterior regions of the fusiform gyrus (onset at 240 ms). These source localizations correspond closely with cortical areas that were identified in previous neuroimaging studies as being involved in color-selective processing. The present ERP data thus provide information about the time course of stimulus selection processes in cortical areas that subserve attention to color.

On the role of selective attention in visual perception.

What is the role of selective attention in visual perception? Before answering this question, it is necessary to differentiate between attentional mechanisms that influence the identification of a stimulus from those that operate after perception is complete. Cognitive neuroscience techniques are particularly well suited to making this distinction because they allow different attentional mechanisms to be isolated in terms of timing and/or neuroanatomy. The present article describes the use of these techniques in differentiating between perceptual and postperceptual attentional mechanisms and then proposes a specific role of attention in visual perception. Specifically, attention is proposed to resolve ambiguities in neural coding that arise when multiple objects are processed simultaneously. Evidence for this hypothesis is provided by two experiments showing that attention-as measured electrophysiologically-is allocated to visual search targets only under conditions that would be expected to lead to ambiguous neural coding.

The capacity of visual working memory for features and conjunctions.

Short-term memory storage can be divided into separate subsystems for verbal information and visual information, and recent studies have begun to delineate the neural substrates of these working-memory systems. Although the verbal storage system has been well characterized, the storage capacity of visual working memory has not yet been established for simple, suprathreshold features or for conjunctions of features. Here we demonstrate that it is possible to retain information about only four colours or orientations in visual working memory at one time. However, it is also possible to retain both the colour and the orientation of four objects, indicating that visual working memory stores integrated objects rather than individual features. Indeed, objects defined by a conjunction of four features can be retained in working memory just as well as single-feature objects, allowing sixteen individual features to be retained when distributed across four objects. Thus, the capacity of visual working memory must be understood in terms of integrated objects rather than individual features, which places significant constraints on cognitive and neurobiological models of the temporary storage of visual information.

Bridging the gap between monkey neurophysiology and human perception: an ambiguity resolution theory of visual selective attention.

When the visual system must process multiple objects simultaneously, as in the visual search paradigm, the neural coding of individual objects can become ambiguous due to the visual system's extensive use of coarse coding and distributed representations. Here we propose that the primary role of visual selective attention within the ventral object recognition pathway is to resolve these ambiguities. We begin by reviewing previous studies of the effects of attention on neural responses in monkeys, which provide the basis for this hypothesis, and then describe a new set of experiments showing that similar attentional mechanisms operate in the human brain. In these new experiments, event-related potentials (ERPs) were recorded from normal human observers while they performed tasks analogous to those used previously in monkeys. The central finding was that an attention-related ERP wave called the "N2pc component" was present under the same conditions that led to attentional modulations of neural responses in monkey visual cortex. These human electrophysiological results provide a bridge between cognitive-level theories of visual attention and the behavior of individual neurons in visual cortex.

Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex.

Many neurons in extrastriate visual cortex have large receptive fields, and this may lead to significant computational problems whenever multiple stimuli fall within a single field. Previous studies have suggested that when multiple stimuli fall within a cell's receptive field, they compete for the cell's response in a manner that can be biased in favor of attended stimuli. In the present study we examined this role of attention in areas V1, V2, and V4 of macaque monkeys with the use of a behavioral paradigm in which attention was directed to one of two stimulus locations. When two stimuli were presented simultaneously inside the cell's receptive field (which could be accomplished only in areas V2 and V4), we found that the cell's response was strongly influenced by which of the two stimuli was attended. The size of this attention effect was reduced when the attended and ignored stimuli were presented sequentially rather than simultaneously. In addition, the effects became very weak and inconsistent in these areas when only one of the two stimuli was located inside the receptive field. Attention thus modulated sensory responses primarily when two or more simultaneous stimuli competed for access to a neuron's receptive field. As in areas V2 and V4, attention did not modulate sensory responses in area V1 when only a single stimulus was inside the receptive field. In addition, the small receptive fields in this area precluded the simultaneous presentation of attended and ignored stimuli inside the receptive field, making it impossible to determine whether attention effects would be observed under the conditions that led to consistent attention effects in areas V2 and V4. Spontaneous firing rates in areas V2 and V4 were found to be 30-40% higher when attention was directed inside rather than outside the receptive field, even when no stimulus was present in the receptive field. Spontaneous firing rates also varied according to the particular location within the receptive field that was attended. These shifts in spontaneous activity may reflect a top-down signal that biases responses in favor of stimuli at the attended location.

Are the same attentional mechanisms used to detect visual search targets defined by color, orientation, and motion?

Motion information tends to be segregated from color and form information in the visual system, both perceptually and neuroanatomically, and it is therefore possible that different mechanisms of attention are used to select targets defined by these different feature types during visual search. To test this hypothesis, we recorded the N2pc component of the event-related potential waveform during visual search tasks with color, orientation, and motion targets. The N2pc component has previously been shown to reflect a specific attentional mechanism that is present for color and form targets, and we sought to determine whether this component would also be present for motion targets. The N2pc component was indeed observed for motion targets as well as color and orientation targets, consistent with the use of a common attentional mechanism across feature types. In addition, we found that motion singletons (i.e., individual items that moved in the opposite direction from the other items in the army) elicited an N2pc component even when they were task-irrelevant, indicating that motion discontinuities may produce an automatic orienting of attention.

Word meanings can be accessed but not reported during the attentional blink.

After the detection of a target item in a rapid stream of visual stimuli, there is a period of 400-600 ms during which subsequent targets are missed. This impairment has been labelled the 'attentional blink'. It has been suggested that, unlike an eye blink, the additional blink does not reflect a suppression of perceptual processing, but instead reflects a loss of information at a postperceptual stage, such as visual short-term memory. Here we provide electrophysiological evidence that words presented during the attentional blink period are analysed to the point of meaning extraction, even though these extracted meanings cannot be reported 1-2s later. This shows that the attentional blink does indeed reflect a loss of information at a postperceptual stage of processing, and provides a demonstration of the modularity of human brain function.