Automatic versus contingent mechanisms of sensory-driven neural biasing and reflexive attention

Recent studies have generated debate regarding whether reflexive attention mechanisms are triggered in a purely automatic stimulus-driven manner. Behavioral studies have found that a nonpredictive "cue" stimulus will speed manual responses to subsequent targets at the same location, but only if that cue is congruent with actively maintained top-down settings for target detection. When a cue is incongruent with top-down settings, response times are unaffected, and this has been taken as evidence that reflexive attention mechanisms were never engaged in those conditions. However, manual response times may mask effects on earlier stages of processing. Here, we used event-related potentials to investigate the interaction of bottom-up sensory-driven mechanisms and top-down control settings at multiple stages of processing in the brain. Our results dissociate sensory-driven mechanisms that automatically bias early stages of visual processing from later mechanisms that are contingent on top-down control. An early enhancement of target processing in the extrastriate visual cortex (i.e., the P1 component) was triggered by the appearance of a unique bright cue, regardless of top-down settings. The enhancement of visual processing was prolonged, however, when the cue was congruent with top-down settings. Later processing in posterior temporal-parietal regions (i.e., the ipsilateral invalid negativity) was triggered automatically when the cue consisted of the abrupt appearance of a single new object. However, in cases where more than a single object appeared during the cue display, this stage of processing was contingent on top-down control. These findings provide evidence that visual information processing is biased at multiple levels in the brain, and the results distinguish automatically triggered sensory-driven mechanisms from those that are contingent on top-down control settings.     

Attentional control of the processing of neural and emotional stimuli

A typical scene contains many different objects that compete for neural representation due to the limited processing capacity of the visual system. At the neural level, competition among multiple stimuli is evidenced by the mutual suppression of their visually evoked responses and occurs most strongly at the level of the receptive field. The competition among multiple objects can be biased by both bottom-up sensory-driven mechanisms and top-down influences, such as selective attention. Functional brain imaging studies reveal that biasing signals due to selective attention can modulate neural activity in visual cortex not only in the presence but also in the absence of visual stimulation. Although the competition among stimuli for representation is ultimately resolved within visual cortex, the source of top-down biasing signals likely derives from a distributed network of areas in frontal and parietal cortex. Competition suggests that once attentional resources are depleted, no further processing is possible. Yet, existing data suggest that emotional stimuli activate brain regions "automatically," largely immune from attentional control. We tested the alternative possibility, namely, that the neural processing of stimuli with emotional content is not automatic and instead requires some degree of attention. Our results revealed that, contrary to the prevailing view, all brain regions responding differentially to emotional faces, including the amygdala, did so only when sufficient attentional resources were available to process the faces. Thus, similar to the processing of other stimulus categories, the processing of facial expression is under top-down control.     

Spatial attention triggered by eye gaze increases and speeds up early visual activity

What are the neuronal correlates of reflexive shifts of attention triggered by eye gaze direction? Event related potentials (ERPs) were measured on 14 subjects performing a spatial attention task where eye gaze direction of a face cued the location of a forthcoming target. Subjects were faster in detecting a validly cued target, i.e. one appearing at the location the eye was gazing at, compared to invalidly cued targets, despite the non-predictive value of the eye cues. ERP results showed an enhanced and earlier occipito-parietal P1 and N1 for valid trials, demonstrating the early modulation of visual input by attentional allocation. These findings provide the first evidence that social attention can rapidly modify the processing of visual information in extrastriate cortex.     

The neural basis of biased competition in human visual cortex

A typical scene contains many different objects that compete for neural representation due to the limited processing capacity of the visual system. At the neural level, competition among multiple stimuli is evidenced by the mutual suppression of their visually evoked responses and occurs most strongly at the level of the receptive field. The competition among multiple objects can be biased by both bottom-up sensory-driven mechanisms and top-down influences, such as selective attention. Functional brain imaging studies reveal that biasing signals due to selective attention can modulate neural activity in visual cortex not only in the presence, but also in the absence of visual stimulation. Although the competition among stimuli for representation is ultimately resolved within visual cortex, the source of top-down biasing signals likely derives from a distributed network of areas in frontal and parietal cortex. Attention-related activity in frontal and parietal areas does not reflect attentional modulation of visually evoked responses, but rather the attentional operations themselves.     

Objects are highlighted by spatial attention

Selective attention may be focused upon a region of interest within the visual surroundings, thereby improving the perceptual quality of stimuli at that location. It has been debated whether this spatially selective mechanism plays a role in the attentive selection of whole objects in a visual scene. The relationship between spatial and object-selective attention was investigated here through recordings of event-related brain potentials (ERPs) supplemented with functional magnetic brain imaging (fMRI). Subjects viewed a display consisting of two bar-shaped objects and directed attention to sequences of stimuli (brief corner offsets) at one end of one of the bars. Unattended stimuli belonging to the same object as the attended stimuli elicited spatiotemporal patterns of neural activity in the visual cortex closely resembling those elicited by the attended stimuli themselves, albeit smaller in amplitude. This enhanced neural activity associated with object-selective attention was localized by use of ERP dipole modeling and fMRI to the lateral occipital extrastriate cortex. We conclude that object-selective attention shares a common neural mechanism with spatial attention that entails the facilitation of sensory processing of stimuli within the boundaries of an attended object.     

Motion direction tuning in human visual cortex

A number of electrophysiological studies have been conducted in recent years in order to clarify the dynamics of visual motion processing in the human brain. Using a variety of event-related potential (ERP) measures, several parameters such as onset, offset, contrast and velocity have been investigated, while a critical aspect of visual motion, that of direction, has received less attention. Here we used multichannel electroencephalography and distributed source localization to study brain activity for different directions of visual motion using random dot stimuli. Our data reveal differential extrastriate activation at 164–226 ms after motion onset that coded for motion direction with different ERP maps and underlying electrical generators for each tested direction. This activation was paralleled initially (164–186 ms) by a distinct extrastriate activation encoding whether the motion stimulus consisted of directed motion stimuli (as above) or contained undirected incoherent motion (control stimulus). Application of a linear inverse solution localized the brain activity for each tested motion direction to distinct brain regions within the same larger network of extrastriate brain regions. These regions included bilateral temporo-occipital and bilateral parieto-occipital cortex. The present data in healthy subjects are compatible with extrastriate activity that is tuned to different directions of visual motion. This extends previous clinical data and suggests the presence of distributed macroscopic motion direction tuning in primate extrastriate cortex that may complement the classical microscopic motion tuning at the columnar level.     

Priming of control: implicit contextual cuing of top-down attentional set

Cognitive models have long distinguished between "automatic" associative processes that can be triggered in a bottom-up fashion, and "controlled" processes, where internal goals guide information processing in a deliberate, top-down manner. However, recent behavioral studies have cast doubt on the validity of this dichotomy, showing that implicit contextual cues can modulate performance in a way suggestive of an associative triggering of specific top-down control states. Here, we harnessed functional magnetic resonance imaging in humans to test whether these behavioral findings truly reflect online, bottom-up priming of top-down attentional control settings. Using a flanker interference task where stimulus location cued the likelihood of incongruent trials, we found that the behavioral phenomenon of implicit, context-specific improvements in interference resolution was mirrored in hemodynamic activity in the medial superior parietal lobule (mSPL), previously implicated in voluntary (as opposed to primed) attention shifts. Moreover, the mSPL displayed context-specific functional coupling with visual regions involved in processing the flanker stimuli, and the modulation of the latter was predictive of the behavioral effects. Finally, the implementation of this contextual control was "on the fly," that is, it was primed online by a switch to the context associated with high conflict. These results suggest that top-down control states can be bound into episodic event representations and can subsequently be primed by other features of those representations. Together, our findings illustrate a more intimate link between associative and controlled processing than is traditionally assumed, and place the neural substrate of that linkage in the posterior parietal cortex.     

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.     

Dissociable effects of top-down and bottom-up attention during episodic encoding

It is well established that the formation of memories for life's experiences-episodic memory-is influenced by how we attend to those experiences, yet the neural mechanisms by which attention shapes episodic encoding are still unclear. We investigated how top-down and bottom-up attention contribute to memory encoding of visual objects in humans by manipulating both types of attention during fMRI of episodic memory formation. We show that dorsal parietal cortex-specifically, intraparietal sulcus (IPS)-was engaged during top-down attention and was also recruited during the successful formation of episodic memories. By contrast, bottom-up attention engaged ventral parietal cortex-specifically, temporoparietal junction (TPJ)-and was also more active during encoding failure. Functional connectivity analyses revealed further dissociations in how top-down and bottom-up attention influenced encoding: while both IPS and TPJ influenced activity in perceptual cortices thought to represent the information being encoded (fusiform/lateral occipital cortex), they each exerted opposite effects on memory encoding. Specifically, during a preparatory period preceding stimulus presentation, a stronger drive from IPS was associated with a higher likelihood that the subsequently attended stimulus would be encoded. By contrast, during stimulus processing, stronger connectivity with TPJ was associated with a lower likelihood the stimulus would be successfully encoded. These findings suggest that during encoding of visual objects into episodic memory, top-down and bottom-up attention can have opposite influences on perceptual areas that subserve visual object representation, suggesting that one manner in which attention modulates memory is by altering the perceptual processing of to-be-encoded stimuli.     

Emotionally negative stimuli can overcome attentional deficits in patients with visuo-spatial hemineglect

Left unilateral spatial neglect resulting from right brain damage is characterized by loss of awareness for stimuli in the contralesional side of space, despite intact visual pathways. We examined using fMRI whether patients with neglect are more likely to consciously detect in the neglected hemifield, emotionally negative complex scenes rather than visually similar neutral pictures and if so, what neural mechanisms mediate this effect. Photographs of emotional and neutral scenes taken from the IAPS were presented in a divided visual field paradigm. As expected, the detection rate for emotional stimuli presented in the neglected field was higher than for neutral ones. Successful detection of emotional scenes as opposed to neutral stimuli in the left visual field (LVF) produced activations in the parahippocampal and anterior cingulate areas in the right hemisphere. Detection of emotional stimuli presented in the intact right visual field (RVF) activated a distributed network of structures in the left hemisphere, including anterior and posterior cingulate cortex, insula, as well as visual striate and extrastriate areas. LVF-RVF contrasts for emotional stimuli revealed activations in right and left attention related prefrontal areas whereas RVF-LVF comparison showed activations in the posterior cingulate and extrastriate visual cortex in the left hemisphere. An additional analysis contrasting detected vs. undetected emotional LVF stimuli showed involvement of left anterior cingulate, right frontal and extrastriate areas. We hypothesize that beneficial role of emotion in overcoming neglect is achieved by activation of frontal and limbic lobe networks, which provide a privileged access of emotional stimuli to attention by top-down modulation of processing in the higher-order extrastriate visual areas. Our results point to the importance of top-down regulatory role of the frontal attentional systems, which might enhance visual activations and lead to greater salience of emotional stimuli for perceptual awareness.     

Brain mechanisms of involuntary visuospatial attention: an event-related potential study

The brain mechanisms mediating visuospatial attention were investigated by recording event-related potentials (ERPs) during a line-orientation discrimination task. Nonpredictive peripheral cues were used to direct participant's attention involuntarily to a spatial location. The earliest attentional modulation was observed in the P1 component (peak latency about 130 ms), with the valid trials eliciting larger P1 than invalid trials. Moreover, the attentional modulations on both the amplitude and latency of the P1 and N1 components had a different pattern as compared to previous studies with voluntary attention tasks. In contrast, the earliest visual ERP component, C1 (peak latency about 80 ms), was not modulated by attention. Low-resolution brain electromagnetic tomography (LORETA) showed that the earliest attentional modulation occurred in extrastriate cortex (middle occipital gyrus, BA 19) but not in the primary visual cortex. Later attention-related reactivations in the primary visual cortex were found at about 110 ms after stimulus onset. The results suggest that involuntary as well as voluntary attention modulates visual processing at the level of extrastriate cortex; however, at least some different processes are involved by involuntary attention compared to voluntary attention. In addition, the possible feedback from higher visual cortex to the primary visual cortex is faster and occurs earlier in involuntary relative to voluntary attention task.     

Reduced P300 and P600 amplitude in the hollow-mask illusion in patients with schizophrenia

Illusions provide a useful tool to study the mechanisms by which top-down and bottom-up processes interact in perception. Patients suffering from schizophrenia are not as subject to the hollow-mask illusion as healthy controls, since studies have shown that controls perceive a hollow mask as a normal face, while patients with schizophrenia do not. This insusceptibility to the illusion is indicating a weakened top-down processing in schizophrenia and little is understood about the neurobiology of this phenomenon. We used event-related potentials to investigate the hollow-mask illusion in patients with schizophrenia and healthy controls. We hypothesized that there would be a visible reduction of top-down processing in the patients' group and that this reduction would occur in the late stages of processing. We found significantly decreased amplitudes in the P300 and P600 components in the patients' group, indicating that visual information does not benefit from frontal, parietal or temporal activity for perceiving incoming stimuli. We propose that a deficit in functional connectivity may be responsible for impaired top-down visual processing in schizophrenia. These data further the understanding of the time course of top-down processing in patients with schizophrenia.     

Deficits of reflexive attention induced by abduction of the eye

Attention mediates access of sensory events to higher cognitive systems and can be driven by either top-down voluntary mechanisms or in a bottom-up, reflexive fashion by the sensory properties of a stimulus. The exact mechanisms underlying these different modes of attention are controversial, but both types of attention appear to be tightly coupled to the systems used for the control of eye-movements. Indeed, recent data indicates that patients with opthalmoplegia (paralysis of the eyes) have difficulty voluntarily attending to locations to which saccades cannot be made (Craighero, Carta, & Fadiga, 2001) and experimentally induced opthalmoplegia disrupts voluntary attention in normal participants. However, the extent to which reflexive attention is mediated by the ability to make eye-movements in normal participants remains unclear. Here, we address this issue by investigating the effect of an experimentally induced opthalmoplegia on voluntary and reflexive attentional orienting during visual search. We observed that abducting the eye into the temporal hemifield elicited deficits of both voluntary and reflexive attention for targets that appeared beyond the oculomotor range. This result confirms the link between oculomotor control and voluntary attention observed in opthalmoplegic patients and demonstrates for the first time that reflexive attention is mediated by the ability to make eye-movements in normal participants.     

Category-related activation for written words in the posterior fusiform is task specific

Category-related brain activations have been reported in the posterior fusiform gyri when people view pictures of tools and animals, but only a single study has observed this pattern when the stimuli were words, rather than pictures. Here we replicate these category effects with words and provide evidence that distinctive patterns of activation are task specific. The results suggest that category-related activation in the posterior fusiform gyri can be driven either "bottom-up" by visual processing of images or "top-down" by word processing.     

Depth of conceptual knowledge modulates visual processes during word reading

Recent evidence suggests that conceptual knowledge modulates early visual stages of object recognition. The present study investigated whether similar modulations can be observed also for the recognition of object names, that is, for symbolic representations with only arbitrary relationships between their visual features and the corresponding conceptual knowledge. In a learning paradigm, we manipulated the amount of information provided about initially unfamiliar visual objects while controlling for perceptual stimulus properties and exposure. In a subsequent test session with electroencephalographic recordings, participants performed several tasks on either the objects or their written names. For objects as well as names, knowledge effects were observed as early as about 120 msec in the P1 component of the ERP, reflecting perceptual processing in extrastriate visual cortex. These knowledge-dependent modulations of early stages of visual word recognition suggest that information about word meanings may modulate the perception of arbitrarily related visual features surprisingly early.     

Shifting visual attention in space: an electrophysiological analysis using high spatial resolution mapping.

OBJECTIVES: Evidence from cortical electrophysiology and functional imaging converges on the view that visual spatial selective attention results in a facilitation of early sensory processing in visual cortical structures. Little is known, however, about the neural control processes that lead to this facilitation. The present study was aimed at further investigating these control processes and their neural correlates by analyzing high spatial resolution maps of brain activity that were evoked by attention-directing cues, but occurred prior to presentation of the target stimulus. METHODS: Subjects (n=14) were presented with central arrow cues that instructed them to attend covertly to either a left or right field location in order to compare two subsequent target stimuli simultaneously presented to the location. On half of the trials, targets were presented to the cued location, while in the other half, targets were presented to the opposite visual field location. Subjects had to respond via button press on 16% of the trials when target stimuli were identical. Event-related potentials (ERPs) were recorded from 92 scalp electrodes which allowed a sufficiently finegrained analysis of the regional specificity of the ERP components. RESULTS: In response to the cues, an initial component over occipital-parietal electrode sites was consistent with an early involvement of the posterior-parietal cortex, perhaps in the initial step of attentional orienting. A second component over the lateral-prefrontal cortex is consistent with the voluntary control and maintenance of attention, a function known to be subserved by frontal cortical structures. A late component narrowly focussed over occipital-temporal electrode sites is most plausibly related to activation of parts of the ventral extrastriate cortex. CONCLUSIONS: The data support the current view that voluntarily orienting visual attention in space leads to top-down modulations in cortical excitability of ventral extrastriate regions initiated by posterior-parietal and mediated by lateral-prefrontal cortical structures.     

Attentional capture by salient distractors during visual search is determined by temporal task demands

The question whether attentional capture by salient but task-irrelevant visual stimuli is triggered in a bottom-up fashion or depends on top-down task settings is still unresolved. Strong support for bottom-up capture was obtained in the additional singleton task, in which search arrays were visible until response onset. Equally strong evidence for top-down control of attentional capture was obtained in spatial cueing experiments in which display durations were very brief. To demonstrate the critical role of temporal task demands on salience-driven attentional capture, we measured ERP indicators of capture by task-irrelevant color singletons in search arrays that could also contain a shape target. In Experiment 1, all displays were visible until response onset. In Experiment 2, display duration was limited to 200 msec. With long display durations, color singleton distractors elicited an N2pc component that was followed by a late Pd component, suggesting that they triggered attentional capture, which was later replaced by location-specific inhibition. When search arrays were visible for only 200 msec, the distractor-elicited N2pc was eliminated and was replaced by a Pd component in the same time range, indicative of rapid suppression of capture. Results show that attentional capture by salient distractors can be inhibited for short-duration search displays, in which it would interfere with target processing. They demonstrate that salience-driven capture is not a purely bottom-up phenomenon but is subject to top-down control.     

Neural correlates of top-down letter processing

This fMRI study investigated top-down letter processing with an illusory letter detection task. Participants responded whether one of a number of different possible letters was present in a very noisy image. After initial training that became increasingly difficult, they continued to detect letters even though the images consisted of pure noise, which eliminated contamination from strong bottom-up input. For illusory letter detection, greater fMRI activation was observed in several cortical regions. These regions included the precuneus, an area generally involved in top-down processing of objects, and the left superior parietal lobule, an area previously identified with the processing of valid letter and word stimuli. In addition, top-down letter detection also activated the left inferior frontal gyrus, an area that may be involved in the integration of general top-down processing and letter-specific bottom-up processing. These findings suggest that these regions may play a significant role in top-down as well as bottom-up processing of letters and words, and are likely to have reciprocal functional connections to more posterior regions in the word and letter processing network.     

Expectation affects neural repetition suppression in infancy

Recent work provides evidence that the infant brain is able to make top-down predictions, but this has been explored only in limited contexts and domains. We build upon this evidence of predictive processing in infants using a new paradigm to examine auditory repetition suppression (RS). RS is a well-documented neural phenomenon in which repeated presentations of the same stimulus result in reduced neural activation compared to non-repeating stimuli. Many theories explain RS using bottom-up mechanisms, but recent work has posited that top-down expectation and predictive coding may bias, or even explain, RS. Here, we investigate whether RS in the infant brain is similarly sensitive to top-down mechanisms. We use fNIRS to measure infants’ neural response in two experimental conditions, one in which variability in stimulus presentation is expected (occurs 75% of the time) and a control condition where variability and repetition are equally likely (50% of the time). We show that 6-month-old infants exhibit attenuated frontal lobe response to blocks of variable auditory stimuli during contexts when variability is expected as compared to the control condition. These findings suggest that young infants’ neural responses are modulated by predictions gained from experience and not simply by bottom-up mechanisms.