An emergent mechanism of selective visual attention in Drosophila

Due to the limited computational capacity of visual systems and the limited capacity to perform several mental operations at once, animals only select a small proportion of the stimuli available at any one time. It remains to be clarified how this process is related to the spatio-temporal dynamics of cell assemblies in the brain. By employing the flight simulator, selective visual attention behavior is studied in Drosophila. It has been found that for the visual objects presented, the tethered fruitflies display various attention patterns. Specifically, the learning memory mutants dunce and amnesiac possess attention patterns totally different from that of the wild-type fly. To explain these results from the viewpoint of dynamic cell assemblies, a neural network has been developed in which a possible link between the activity of cell assemblies, encoding of sensory information, and selective attention in Drosophila is proposed. Received: 3 November 1998 / Accepted in revised form: 1 July 1999     

Distinct Acute Zones for Visual Stimuli in Different Visual Tasks in Drosophila

The fruit fly Drosophila melanogaster has a sophisticated visual system and exhibits complex visual behaviors. Visual responses, vision processing and higher cognitive processes in Drosophila have been studied extensively. However, little is known about whether the retinal location of visual stimuli can affect fruit fly performance in various visual tasks. We tested the response of wild-type Berlin flies to visual stimuli at several vertical locations. Three paradigms were used in our study: visual operant conditioning, visual object fixation and optomotor response. We observed an acute zone for visual feature memorization in the upper visual field when visual patterns were presented with a black background. However, when a white background was used, the acute zone was in the lower visual field. Similar to visual feature memorization, the best locations for visual object fixation and optomotor response to a single moving stripe were in the lower visual field with a white background and the upper visual field with a black background. The preferred location for the optomotor response to moving gratings was around the equator of the visual field. Our results suggest that different visual processing pathways are involved in different visual tasks and that there is a certain degree of overlap between the pathways for visual feature memorization, visual object fixation and optomotor response.     

Attention without awareness in blindsight.

The act of attending has frequently been equated with visual awareness. We examined this relationship in 'blindsight'--a condition in which the latter is absent or diminished as a result of damage to the primary visual cortex. Spatially selective visual attention is demonstrated when information that stimuli are likely to appear at a specific location enhances the speed or accuracy of detection of stimuli subsequently presented at that location. In a blindsight subject, we showed that attention can confer an advantage in processing stimuli presented at an attended location, without those stimuli entering consciousness. Attention could be directed both by symbolic cues in the subject's spared field of vision or cues presented in his blind field. Cues in his blind field were even effective in directing his attention to a second location remote from that at which the cue was presented. These indirect cues were effective whether or not they themselves elicited non-visual awareness. We concluded that the spatial selection of information by an attentional mechanism and its entry into conscious experience cannot be one and the same process.     

Shifting attention within memory representations involves early visual areas

Prior studies have shown that spatial attention modulates early visual cortex retinotopically, resulting in enhanced processing of external perceptual representations. However, it is not clear whether the same visual areas are modulated when attention is focused on, and shifted within a working memory representation. In the current fMRI study participants were asked to memorize an array containing four stimuli. After a delay, participants were presented with a verbal cue instructing them to actively maintain the location of one of the stimuli in working memory. Additionally, on a number of trials a second verbal cue instructed participants to switch attention to the location of another stimulus within the memorized representation. Results of the study showed that changes in the BOLD pattern closely followed the locus of attention within the working memory representation. A decrease in BOLD-activity (V1-V3) was observed at ROIs coding a memory location when participants switched away from this location, whereas an increase was observed when participants switched towards this location. Continuous increased activity was obtained at the memorized location when participants did not switch. This study shows that shifting attention within memory representations activates the earliest parts of visual cortex (including V1) in a retinotopic fashion. We conclude that even in the absence of visual stimulation, early visual areas support shifting of attention within memorized representations, similar to when attention is shifted in the outside world. The relationship between visual working memory and visual mental imagery is discussed in light of the current findings.     

Increased activity in human visual cortex during directed attention in the absence of visual stimulation

When subjects direct attention to a particular location in a visual scene, responses in the visual cortex to stimuli presented at that location are enhanced, and the suppressive influences of nearby distractors are reduced. What is the top-down signal that modulates the response to an attended versus an unattended stimulus? Here, we demonstrate increased activity related to attention in the absence of visual stimulation in extrastriate cortex when subjects covertly directed attention to a peripheral location expecting the onset of visual stimuli. Frontal and parietal areas showed a stronger signal increase during this expectation than did visual areas. The increased activity in visual cortex in the absence of visual stimulation may reflect a top-down bias of neural signals in favor of the attended location, which derives from a fronto-parietal network.     

Mislocalization of visual stimuli: independent effects of static and dynamic attention

Shifts of visual attention cause systematic distortions of the perceived locations of visual objects around the focus of attention. In the attention repulsion effect, the perceived location of a visual target is shifted away from an attention-attracting cue when the cue is presented before the target. Recently it has been found that, if the visual cue is presented after the target, the perceived location of the target shifts toward the location of the following cue. One unanswered question is whether a single mechanism underlies both attentional repulsion and attraction effects. We presented participants with two disks at diagonal locations as visual cues and two vertical lines as targets. Participants were asked to perform a forced-choice task to judge targets' positions. The present study examined whether the magnitude of the repulsion effect and the attraction effect would differ (Experiment 1), whether the two effects would interact (Experiment 2), and whether the location or the dynamic shift of attentional focus would determine the distortions effects (Experiment 3). The results showed that the effect size of the attraction effect was slightly larger than the repulsion effect and the preceding and following cues have independent influences on the perceived positions. The repulsion effect was caused by the location of attnetion and the attraction effect was due to the dynamic shift of attentional focus, suggesting that the underlying mechanisms for the retrospective attraction effect might be different from those for the repulsion effect.     

Intrinsic activity in the fly brain gates visual information during behavioral choices

The small insect brain is often described as an input/output system that executes reflex-like behaviors. It can also initiate neural activity and behaviors intrinsically, seen as spontaneous behaviors, different arousal states and sleep. However, less is known about how intrinsic activity in neural circuits affects sensory information processing in the insect brain and variability in behavior. Here, by simultaneously monitoring Drosophila's behavioral choices and brain activity in a flight simulator system, we identify intrinsic activity that is associated with the act of selecting between visual stimuli. We recorded neural output (multiunit action potentials and local field potentials) in the left and right optic lobes of a tethered flying Drosophila, while its attempts to follow visual motion (yaw torque) were measured by a torque meter. We show that when facing competing motion stimuli on its left and right, Drosophila typically generate large torque responses that flip from side to side. The delayed onset (0.1-1 s) and spontaneous switch-like dynamics of these responses, and the fact that the flies sometimes oppose the stimuli by flying straight, make this behavior different from the classic steering reflexes. Drosophila, thus, seem to choose one stimulus at a time and attempt to rotate toward its direction. With this behavior, the neural output of the optic lobes alternates; being augmented on the side chosen for body rotation and suppressed on the opposite side, even though the visual input to the fly eyes stays the same. Thus, the flow of information from the fly eyes is gated intrinsically. Such modulation can be noise-induced or intentional; with one possibility being that the fly brain highlights chosen information while ignoring the irrelevant, similar to what we know to occur in higher animals.     

A motion-dependent distortion of retinotopy in area V4

When one element in an apparent motion sequence differs in color from the others, it is perceived as shifted along the motion trajectory. We examined whether V4 neurons encode the physical or perceived location of this "flashed" element by recording neuronal responses while monkeys viewed these stimuli. The retinotopic locus of V4 activity evoked by the flashed element shifted along the motion trajectory. The magnitude of the shift is consistent with the perceptual shift in humans viewing identical stimuli. This retinotopic distortion depended on the presence of a flashed element but was observed for both color-selective and non-color-selective neurons. The distortion was undiminished when the flashed element terminated the sequence, a condition that reduced the perceptual shift in humans. These findings are consistent with a Bayesian model of localization in which perceived location is derived from position signals optimally integrated across visual areas.     

Deployment of Spatial Attention towards Locations in Memory Representations. An EEG Study

Recalling information from visual short-term memory (VSTM) involves the same neural mechanisms as attending to an actually perceived scene. In particular, retrieval from VSTM has been associated with orienting of visual attention towards a location within a spatially-organized memory representation. However, an open question concerns whether spatial attention is also recruited during VSTM retrieval even when performing the task does not require access to spatial coordinates of items in the memorized scene. The present study combined a visual search task with a modified, delayed central probe protocol, together with EEG analysis, to answer this question. We found a temporal contralateral negativity (TCN) elicited by a centrally presented go-signal which was spatially uninformative and featurally unrelated to the search target and informed participants only about a response key that they had to press to indicate a prepared target-present vs. -absent decision. This lateralization during VSTM retrieval (TCN) provides strong evidence of a shift of attention towards the target location in the memory representation, which occurred despite the fact that the present task required no spatial (or featural) information from the search to be encoded, maintained, and retrieved to produce the correct response and that the go-signal did not itself specify any information relating to the location and defining feature of the target.     

The multisensory attentional consequences of tool use: a functional magnetic resonance imaging study

Background

Tool use in humans requires that multisensory information is integrated across different locations, from objects seen to be distant from the hand, but felt indirectly at the hand via the tool. We tested the hypothesis that using a simple tool to perceive vibrotactile stimuli results in the enhanced processing of visual stimuli presented at the distal, functional part of the tool. Such a finding would be consistent with a shift of spatial attention to the location where the tool is used.

Methodology/Principal Findings

We tested this hypothesis by scanning healthy human participants'' brains using functional magnetic resonance imaging, while they used a simple tool to discriminate between target vibrations, accompanied by congruent or incongruent visual distractors, on the same or opposite side to the tool. The attentional hypothesis was supported: BOLD response in occipital cortex, particularly in the right hemisphere lingual gyrus, varied significantly as a function of tool position, increasing contralaterally, and decreasing ipsilaterally to the tool. Furthermore, these modulations occurred despite the fact that participants were repeatedly instructed to ignore the visual stimuli, to respond only to the vibrotactile stimuli, and to maintain visual fixation centrally. In addition, the magnitude of multisensory (visual-vibrotactile) interactions in participants'' behavioural responses significantly predicted the BOLD response in occipital cortical areas that were also modulated as a function of both visual stimulus position and tool position.

Conclusions/Significance

These results show that using a simple tool to locate and to perceive vibrotactile stimuli is accompanied by a shift of spatial attention to the location where the functional part of the tool is used, resulting in enhanced processing of visual stimuli at that location, and decreased processing at other locations. This was most clearly observed in the right hemisphere lingual gyrus. Such modulations of visual processing may reflect the functional importance of visuospatial information during human tool use.     

Retrospective Attention Gates Discrete Conscious Access to Past Sensory Stimuli

Cueing attention after the disappearance of visual stimuli biases which items will be remembered best. This observation has historically been attributed to the influence of attention on memory as opposed to subjective visual experience. We recently challenged this view by showing that cueing attention after the stimulus can improve the perception of a single Gabor patch at threshold levels of contrast. Here, we test whether this retro-perception actually increases the frequency of consciously perceiving the stimulus, or simply allows for a more precise recall of its features. We used retro-cues in an orientation-matching task and performed mixture-model analysis to independently estimate the proportion of guesses and the precision of non-guess responses. We find that the improvements in performance conferred by retrospective attention are overwhelmingly determined by a reduction in the proportion of guesses, providing strong evidence that attracting attention to the target’s location after its disappearance increases the likelihood of perceiving it consciously.     

Shared Visual Attention and Memory Systems in the Drosophila Brain

Background

Selective attention and memory seem to be related in human experience. This appears to be the case as well in simple model organisms such as the fly Drosophila melanogaster. Mutations affecting olfactory and visual memory formation in Drosophila, such as in dunce and rutabaga, also affect short-term visual processes relevant to selective attention. In particular, increased optomotor responsiveness appears to be predictive of visual attention defects in these mutants.

Methodology/Principal Findings

To further explore the possible overlap between memory and visual attention systems in the fly brain, we screened a panel of 36 olfactory long term memory (LTM) mutants for visual attention-like defects using an optomotor maze paradigm. Three of these mutants yielded high dunce-like optomotor responsiveness. We characterized these three strains by examining their visual distraction in the maze, their visual learning capabilities, and their brain activity responses to visual novelty. We found that one of these mutants, D0067, was almost completely identical to dunce¹ for all measures, while another, D0264, was more like wild type. Exploiting the fact that the LTM mutants are also Gal4 enhancer traps, we explored the sufficiency for the cells subserved by these elements to rescue dunce attention defects and found overlap at the level of the mushroom bodies. Finally, we demonstrate that control of synaptic function in these Gal4 expressing cells specifically modulates a 20–30 Hz local field potential associated with attention-like effects in the fly brain.

Conclusions/Significance

Our study uncovers genetic and neuroanatomical systems in the fly brain affecting both visual attention and odor memory phenotypes. A common component to these systems appears to be the mushroom bodies, brain structures which have been traditionally associated with odor learning but which we propose might be also involved in generating oscillatory brain activity required for attention-like processes in the fly brain.     

Color coding in the cortex: a modified approach to bottom-up visual attention

Itti and Koch’s (Vision Research 40:1489–1506, 2000) saliency-based visual attention model is a broadly accepted model that describes how attention processes are deployed in the visual cortex in a pure bottom-up strategy. This work complements their model by modifying the color feature calculation. Evidence suggests that S-cone responses are elicited in the same spatial distribution and have the same sign as responses to M-cone stimuli; these cells are tentatively referred to as red-cyan. For other cells, the S-cone input seems to be aligned with the L-cone input; these cells might be green-magenta cells. To model red-cyan and green-magenta double-opponent cells, we implement a center-surround difference approach of the aforementioned model. The resulting color maps elicited enhanced responses to color salient stimuli when compared to the classic ones at high statistical significance levels. We also show that the modified model improves the prediction of locations attended by human viewers.     

Enhanced tactile performance at the destination of an upcoming saccade

Previous work has demonstrated that upcoming saccades influence visual and auditory performance even for stimuli presented before the saccade is executed. These studies suggest a close relationship between saccade generation and visual/auditory attention. Furthermore, they provide support for Rizzolatti et al.'s premotor model of attention, which suggests that the same circuits involved in motor programming are also responsible for shifts in covert orienting (shifting attention without moving the eyes or changing posture). In a series of experiments, we demonstrate that saccade programming also affects tactile perception. Participants made speeded saccades to the left and right side as well as tactile discriminations of up versus down. The first experiment demonstrates that participants were reliably faster at responding to tactile stimuli near the location of upcoming saccades. In our second experiment, we had the subjects cross their hands and demonstrated that the effect occurs in visual space (rather than the early representations of touch). In our third experiment, the tactile events usually occurred on the opposite side of upcoming eye movement. We found that the benefit at the saccade target location vanished, suggesting that this shift is not obligatory but that it may be vetoed on the basis of expectation.     

Changes in visual receptive fields with microstimulation of frontal cortex

The influence of attention on visual cortical neurons has been described in terms of its effect on the structure of receptive fields (RFs), where multiple stimuli compete to drive neural responses and ultimately behavior. We stimulated the frontal eye field (FEF) of passively fixating monkeys and produced changes in V4 responses similar to known effects of voluntary attention. Subthreshold FEF stimulation enhanced visual responses at particular locations within the RF and altered the interaction between pairs of RF stimuli to favor those aligned with the activated FEF site. Thus, we could influence which stimulus drove the responses of individual V4 neurons. These results suggest that spatial signals involved in saccade preparation are used to covertly select among multiple stimuli appearing within the RFs of visual cortical neurons.     

The scope and limits of top-down attention in unconscious visual processing

Attentional selection plays a critical role in conscious perception. When attention is diverted, even salient stimuli fail to reach visual awareness. Attention can be voluntarily directed to a spatial location or a visual feature for facilitating the processing of information relevant to current goals. In everyday situations, attention and awareness are tightly coupled. This has led some to suggest that attention and awareness might be based on a common neural foundation, whereas others argue that they are mediated by distinct mechanisms. A body of evidence shows that visual stimuli can be processed at multiple stages of the visual-processing streams without evoking visual awareness. To illuminate the relationship between visual attention and conscious perception, we investigated whether top-down attention can target and modulate the neural representations of unconsciously processed visual stimuli. Our experiments show that spatial attention can target only consciously perceived stimuli, whereas feature-based attention can modulate the processing of invisible stimuli. The attentional modulation of unconscious signals implies that attention and awareness can be dissociated, challenging a simplistic view of the boundary between conscious and unconscious visual processing.     

Female‐borne cues affecting Psyttalia concolor (Hymenoptera: Braconidae) male behavior during courtship and mating

Knowledge of the mechanisms that regulate courtship and mating behavior in Psyttalia concolor (Szépligeti)–a koinobiont endophagous solitary parasitoid of the olive fruit fly, Bactrocera oleae (Rossi), and of other fruit flies–is essential to its mass rearing and management. Augmentative releases of P. concolor for olive fruit fly control started in the Mediterranean areas in the 1950s and still continue with limited success. We determined the influence of visual and chemical cues on courtship and mating behavior of this braconid and the possible effect of the mating status of males and females in the perception of these cues. Our results suggest that integration of visual and chemical stimuli are fundamental for mate location and courtship. Indeed, the optimal response of the male was achieved when physical and chemical cues were simultaneously presented and vision and olfaction worked synergistically.     

Saccade generation by the frontal eye fields in rhesus monkeys is separable from visual detection and bottom-up attention shift

The frontal eye fields (FEF), originally identified as an oculomotor cortex, have also been implicated in perceptual functions, such as constructing a visual saliency map and shifting visual attention. Further dissecting the area's role in the transformation from visual input to oculomotor command has been difficult because of spatial confounding between stimuli and responses and consequently between intermediate cognitive processes, such as attention shift and saccade preparation. Here we developed two tasks in which the visual stimulus and the saccade response were dissociated in space (the extended memory-guided saccade task), and bottom-up attention shift and saccade target selection were independent (the four-alternative delayed saccade task). Reversible inactivation of the FEF in rhesus monkeys disrupted, as expected, contralateral memory-guided saccades, but visual detection was demonstrated to be intact at the same field. Moreover, saccade behavior was impaired when a bottom-up shift of attention was not a prerequisite for saccade target selection, indicating that the inactivation effect was independent of the previously reported dysfunctions in bottom-up attention control. These findings underscore the motor aspect of the area's functions, especially in situations where saccades are generated by internal cognitive processes, including visual short-term memory and long-term associative memory.     

Pre-Saccadic Shifts of Visual Attention

The locations of visual objects to which we attend are initially mapped in a retinotopic frame of reference. Because each saccade results in a shift of images on the retina, however, the retinotopic mapping of spatial attention must be updated around the time of each eye movement. Mathôt and Theeuwes [1] recently demonstrated that a visual cue draws attention not only to the cue''s current retinotopic location, but also to a location shifted in the direction of the saccade, the “future-field”. Here we asked whether retinotopic and future-field locations have special status, or whether cue-related attention benefits exist between these locations. We measured responses to targets that appeared either at the retinotopic or future-field location of a brief, non-predictive visual cue, or at various intermediate locations between them. Attentional cues facilitated performance at both the retinotopic and future-field locations for cued relative to uncued targets, as expected. Critically, this cueing effect also occurred at intermediate locations. Our results, and those reported previously [1], imply a systematic bias of attention in the direction of the saccade, independent of any predictive remapping of attention that compensates for retinal displacements of objects across saccades [2].