Distribution of attention modulates salience signals in early visual cortex

Previous research has shown that the extent to which people spread attention across the visual field plays a crucial role in visual selection and the occurrence of bottom-up driven attentional capture. Consistent with previous findings, we show that when attention was diffusely distributed across the visual field while searching for a shape singleton, an irrelevant salient color singleton captured attention. However, while using the very same displays and task, no capture was observed when observers initially focused their attention at the center of the display. Using event-related fMRI, we examined the modulation of retinotopic activity related to attentional capture in early visual areas. Because the sensory display characteristics were identical in both conditions, we were able to isolate the brain activity associated with exogenous attentional capture. The results show that spreading of attention leads to increased bottom-up exogenous capture and increased activity in visual area V3 but not in V2 and V1.     

Goal-related activity in V4 during free viewing visual search. Evidence for a ventral stream visual salience map

Natural exploration of complex visual scenes depends on saccadic eye movements toward important locations. Saccade targeting is thought to be mediated by a retinotopic map that represents the locations of salient features. In this report, we demonstrate that extrastriate ventral area V4 contains a retinotopic salience map that guides exploratory eye movements during a naturalistic free viewing visual search task. In more than half of recorded cells, visually driven activity is enhanced prior to saccades that move the fovea toward the location previously occupied by a neuron's spatial receptive field. This correlation suggests that bottom-up processing in V4 influences the oculomotor planning process. Half of the neurons also exhibit top-down modulation of visual responses that depends on search target identity but not visual stimulation. Convergence of bottom-up and top-down processing streams in area V4 results in an adaptive, dynamic map of salience that guides oculomotor planning during natural vision.     

The role of attention in figure-ground segregation in areas V1 and V4 of the visual cortex

Our visual system segments images into objects and background. Figure-ground segregation relies on the detection of feature discontinuities that signal boundaries between the figures and the background and on a complementary region-filling process that groups together image regions with similar features. The neuronal mechanisms for these processes are not well understood and it is unknown how they depend on visual attention. We measured neuronal activity in V1 and V4 in a task where monkeys either made an eye movement to texture-defined figures or ignored them. V1 activity predicted the timing and the direction of the saccade if the figures were task relevant. We found that boundary detection is an early process that depends little on attention, whereas region filling occurs later and is facilitated by visual attention, which acts in an object-based manner. Our findings are explained by a model with local, bottom-up computations for boundary detection and feedback processing for region filling.     

Feature-based attention in the frontal eye field and area V4 during visual search

When we search for a target in a crowded visual scene, we often use the distinguishing features of the target, such as color or shape, to guide our attention and eye movements. To investigate the neural mechanisms of feature-based attention, we simultaneously recorded neural responses in the frontal eye field (FEF) and area V4 while monkeys performed a visual search task. The responses of cells in both areas were modulated by feature attention, independent of spatial attention, and the magnitude of response enhancement was inversely correlated with the number of saccades needed to find the target. However, an analysis of the latency of sensory and attentional influences on responses suggested that V4 provides bottom-up sensory information about stimulus features, whereas the FEF provides a top-down attentional bias toward target features that modulates sensory processing in V4 and that could be used to guide the eyes to a searched-for target.     

Empirical mode decomposition of field potentials from macaque V4 in visual spatial attention

Empirical mode decomposition (EMD) has recently been introduced as a local and fully data-driven technique for the analysis of non-stationary time-series. It allows the frequency and amplitude of a time-series to be evaluated with excellent time resolution. In this article we consider the application of EMD to the analysis of neuronal activity in visual cortical area V4 of a macaque monkey performing a visual spatial attention task. We show that, by virtue of EMD, field potentials can be resolved into a sum of intrinsic components with different degrees of oscillatory content. Low-frequency components in single-trial recordings contribute to the average visual evoked potential (AVEP), whereas high-frequency components do not, but are identified as gamma-band (30–90 Hz) oscillations. The magnitude of time-varying gamma activity is shown to be enhanced when the monkey attends to a visual stimulus as compared to when it is not attending to the same stimulus. Comparison with Fourier analysis shows that EMD may offer better temporal and frequency resolution. These results support the idea that the magnitude of gamma activity reflects the modulation of V4 neurons by visual spatial attention. EMD, coupled with instantaneous frequency analysis, is demonstrated to be a useful technique for the analysis of neurobiological time-series.     

Active vision and visual activation in area V4

During normal vision, the focus of gaze continually jumps from one important image feature to the next. In this issue of Neuron, Mazer and Gallant analyze neural activity in higher-level visual cortex during this kind of active visual exploration, and they demonstrate a localized enhancement of visual responses that predicts the target of the upcoming eye movement.     

Time course of attention reveals different mechanisms for spatial and feature-based attention in area V4

Attention can facilitate visual processing, emphasizing specific locations and highlighting stimuli containing specific features. To dissociate the mechanisms of spatial and feature-based attention, we compared the time course of visually evoked responses under different attention conditions. We recorded from single neurons in area V4 during a delayed match-to-sample task that controlled both spatial and feature-based attention. Neuronal responses increased when spatial attention was directed toward the receptive field and were modulated by the identity of the target of feature-based attention. Modulation by spatial attention was weaker during the early portion of the visual response and stronger during the later portion of the response. In contrast, modulation by feature-based attention was relatively constant throughout the response. It appears that stimulus onset transients disrupt spatial attention, but not feature attention. We conclude that spatial attention reflects a combination of stimulus-driven and goal-driven processes, while feature-based attention is purely goal driven.     

Cell-type-specific synchronization of neural activity in FEF with V4 during attention

Shifts of gaze and shifts of attention are closely linked and it is debated whether they result from the same neural mechanisms. Both processes involve the frontal eye fields (FEF), an area which is also a source of top-down feedback to area V4 during covert attention. To test the relative contributions of oculomotor and attention-related FEF signals to such feedback, we recorded simultaneously from both areas in a covert attention task and in a saccade task. In the attention task, only visual and visuomovement FEF neurons showed enhanced responses, whereas movement cells were unchanged. Importantly, visual, but not movement or visuomovement cells, showed enhanced gamma frequency synchronization with activity in V4 during attention. Within FEF, beta synchronization was increased for movement cells during attention but was suppressed in the saccade task. These findings support the idea that the attentional modulation of visual processing is not mediated by movement neurons.     

Toward a unified theory of visual area V4

Visual area V4 is a midtier cortical area in the ventral visual pathway. It is crucial for visual object recognition and has been a focus of many studies on visual attention. However, there is no unifying view of V4's role in visual processing. Neither is there an understanding of how its role in feature processing interfaces with its role in visual attention. This review captures our current knowledge of V4, largely derived from electrophysiological and imaging studies in the macaque monkey. Based on recent discovery of functionally specific domains in V4, we propose that the unifying function of V4 circuitry is to enable selective extraction of specific functional domain-based networks, whether it be by bottom-up specification of object features or by top-down attentionally driven selection.     

Computational modelling of visual attention

Five important trends have emerged from recent work on computational models of focal visual attention that emphasize the bottom-up, image-based control of attentional deployment. First, the perceptual saliency of stimuli critically depends on the surrounding context. Second, a unique 'saliency map' that topographically encodes for stimulus conspicuity over the visual scene has proved to be an efficient and plausible bottom-up control strategy. Third, inhibition of return, the process by which the currently attended location is prevented from being attended again, is a crucial element of attentional deployment. Fourth, attention and eye movements tightly interplay, posing computational challenges with respect to the coordinate system used to control attention. And last, scene understanding and object recognition strongly constrain the selection of attended locations. Insights from these five key areas provide a framework for a computational and neurobiological understanding of visual attention.     

Shape perception: complex contour representation in visual area V4

A recent study has put forward a physiologically plausible population model that implements a parts-based shape-coding scheme for macaque visual area V4.     

The role of attention in visual processing

Attention to a visual stimulus typically increases the responses of cortical neurons to that stimulus. Because many studies have shown a close relationship between the performance of individual neurons and behavioural performance of animal subjects, it is important to consider how attention affects this relationship. Measurements of behavioural and neuronal performance taken from rhesus monkeys while they performed a motion detection task with two attentional states show that attention alters the relationship between behaviour and neuronal response. Notably, attention affects the relationship differently in different cortical visual areas. This indicates that a close relationship between neuronal and behavioural performance on a given task persists over changes in attentional state only within limited regions of visual cortex.     

Splitting the spotlight of visual attention

Can the brain attend to more than a single location at one time? In this issue of Neuron, McMains and Somers report psychophysical and fMRI evidence showing that subjects can attend to two separate locations concurrently and that divided spatial attention leads to separate zones of attentional enhancement in early visual cortex.     

The dark side of visual attention

The limited capacity of neural processing restricts the number of objects and locations that can be attended to. Selected events are readily enhanced: the bright side of attention. However, such focal processing comes at a cost, namely, functional blindness for unattended events: the dark side of visual attention. Recent work has advanced our understanding of the neural mechanisms that facilitate visual processing, as well as the neural correlates of unattended, unconscious visual events. Also, new results have revealed how attentional deployment is optimized by non-visual factors such as behavioral set, past experience, and emotional salience.     

Alpha ERD and human visual selective attention

We compared the alpha band EEG depression (event-related desynchnization, ERD) level in two tasks, involving activation of different attentional processes: visual search for a deviant relevant stimulus among many similar ones and visual oddball. Control data for the visual search task consisted of simple viewing of several stimuli being of the same shape as the relevant stimulus in the search trials. Gaze position was verified by eye tracking method. We interpreted alpha band ERD as a correlate of activation of attentional processes. Fixating the target in visual search task caused a significantly larger ERD than fixating the same stimuli in control trials over all leads. We suppose this to be related with task and visual environment complexities. The frontal ERD domination may indicate attentional control over voluntary movements execution (top-down attention). The caudal ERD may be related with updating of visual information as a result of search process (bottom-up attention). Both relevant and irrelevant stimuli in the oddball task also induced alpha band ERD, but it was larger in response to relevant one and reached maximum level over occipital leads. Domination of caudal ERD in oddball task is supposed to indicate bottom-up attention processes.     

Orientation of attention in the visual space]

The display was composed of four boxes, horizontally aligned above the fixation point. In Experiment I, each box was cued by a digit shown at fixation. In Experiment II there were only two numeric cues, signalling the inner or the outer boxes, depending on the experimental condition. The subject was instructed to orient attention to the cued box, and to respond to the imperative stimulus as fast as possible, wherever it appeared. By using four time interval (SOAs), we tried to determine the route covered by attention movements. In Experiment I, with the shortest SOA (100 msec), it was shown that attention does not reach the cued box through a direct path. Rather it moves first on the inner boxes, thereafter focusing on the cued location. The same results were obtained in Experiment II, where the cue directed attention to the inner boxes. When the external boxes were cued, however, this trend was not observed.     

Differential attention-dependent response modulation across cell classes in macaque visual area V4

The cortex contains multiple cell types, but studies of attention have not distinguished between them, limiting understanding of the local circuits that transform attentional feedback into improved visual processing. Parvalbumin-expressing inhibitory interneurons can be distinguished from pyramidal neurons based on their briefer action potential durations. We recorded neurons in area V4 as monkeys performed an attention-demanding task. We find that the distribution of action potential durations is strongly bimodal. Neurons with narrow action potentials have higher firing rates and larger attention-dependent increases in absolute firing rate than neurons with broad action potentials. The percentage increase in response is similar across the two classes. We also find evidence that attention increases the reliability of the neuronal response. This modulation is more than two-fold stronger among putative interneurons. These findings lead to the surprising conclusion that the strongest attentional modulation occurs among local interneurons that do not transmit signals between areas.