Aarlenne Z. Khan

Ocular dominance reverses as a function of horizontal gaze angle.

Ocular dominance is the tendency to prefer visual input from one eye to the other [e.g. Porac, C. & Coren, S. (1976). The dominant eye. Psychological Bulletin 83(5), 880-897]. In standard sighting tests, most people consistently fall into either the left- or right eye-dominant category [Miles, W. R. (1930). Ocular dominance in human adults. Journal of General Psychology 3, 412-420]. Here we show this static concept to be flawed, being based on the limited results of sighting with gaze pointed straight ahead. In a reach-grasp task for targets within the binocular visual field, subjects switched between left and right eye dominance depending on horizontal gaze angle. On average, ocular dominance switched at gaze angles of only 15.5 degrees off center.

The eye dominates in guiding attention during simultaneous eye and hand movements

Prior to the onset of a saccade or a reach, attention is directed to the goal of the upcoming movement. However, it remains unknown whether attentional resources are shared across effectors for simultaneous eye and hand movements. Using a 4-AFC shape discrimination task, we investigated attentional allocation during the planning of a saccade alone, reach alone, or combined saccade and reach to one of five peripheral locations. Target discrimination was better when the probe appeared at the goal of the impending movement than when it appeared elsewhere. However, discrimination performance at the movement goal was not better for combined eye-hand movements compared to either effector alone, suggesting a shared limited attentional resource rather than separate pools of effector-specific attention. To test which effector dominates in guiding attention, we then separated eye and hand movement goals in two conditions: (1) cued reach/fixed saccade--subjects made saccades to the same peripheral location throughout the block, while the reach goal was cued and (2) cued saccade/fixed reach--subjects made reaches to the same location, while the saccade goal was cued. For both conditions, discrimination performance was consistently better at the eye goal than the hand goal. This indicates that shared attentional resources are guided predominantly by the eye during the planning of eye and hand movements.

Pre-saccadic perceptual facilitation can occur without covert orienting of attention

The pre-motor theory of attention suggests that the mechanisms involved in target selection for eye movements are the same as those for spatial attention shifts. The pre-saccadic facilitation of perceptual discrimination at the location of a saccadic goal (paradigm of Deubel and Schneider, 1996) has been considered as an argument for this theory. We compared letter discrimination performance in a saccade (overt attention - pre-saccadic facilitation) and a fixation (covert attention) task in a patient with right posterior parietal damage and 4 controls. In the overt attention condition, the patient was instructed by a central cue to make a saccade to a target located at a peripheral location. During the saccade latency (in a period of time of 250 msec following the presentation of the cue), a letter was presented at the target location. Accuracy of leftward saccades was impaired compared to rightward saccades. To evaluate letter discrimination performance in this saccade task (i.e., the presence of pre-saccadic facilitation), we selected only those leftward saccades that were equivalent in accuracy (and latency) to the rightward ones. Within these selected trials, the patient was able to discriminate letters equally well in both visual fields. In contrast, he performed at chance level during the fixation task (covert attention condition) for letters presented at the same peripheral location with the same timing with respect to the cue presentation. The patient could thus discriminate the letter presented at 8° of visual eccentricity while he was preparing a saccade, whereas he was unable to perceive the letter in the fixation task. Remarkably, in the left visual field, letter discrimination was impossible even when a letter was presented as close as 2.5° of visual eccentricity in the fixation task. Altogether, these results suggest that pre-saccadic perceptual facilitation does not rely on the same processes as those of covert attention, as tested by fixation task. Instead, we propose that pre-saccadic perceptual facilitation results from a form of attention specific to action, which could correspond to a pre-saccadic remapping process.

The default allocation of attention is broadly ahead of smooth pursuit.

When moving through our environment, it is vital to preferentially process positions on our future path in order to react quickly to critical situations. During smooth pursuit, attention may be directed ahead with either a focused locus or a broad bias. We examined the 2D spatial extent of attention during a smooth pursuit task using both saccade (SRT) and manual (MRT) reaction times as measures of attentional allocation. Targets were flashed at various locations around current eye position while subjects pursued a moving target. Subjects made a saccade or pressed a button as soon as they perceived the target. Both SRTs and MRTs were shortest to targets flashed ahead of compared to behind the direction of pursuit across half of the visual field ahead of pursuit direction. Furthermore, we found an increase specific to SRTs at small target eccentricities directly ahead of pursuit, which may be related to an additional saccade trigger strategy; small saccades take longer to execute if smooth pursuit brings the eyes close to the target. In summary, both SRTs and MRTs revealed that attention is by default broadly allocated in the visual hemi-field ahead of the line of sight during smooth pursuit eye movements. This attentional bias may serve a predictive purpose for facilitating the processing of upcoming events.

Parietal Damage Dissociates Saccade Planning from Presaccadic Perceptual Facilitation

A well-known theory in the field of attention today is the premotor theory of attention which suggests that the mechanisms involved in eye movements are the same as those for spatial attention shifts. We tested a parietal damaged patient with unilateral optic ataxia and 4 controls on a dual saccade/attentional task and show a dissociation between saccadic eye movements and presaccadic perceptual enhancement at the saccade goal. Remarkably, though the patient was able to make the appropriate saccades to the left, impaired visual field (undistinguishable from saccades to his right, intact visual field), he was unable to discriminate the letter at the saccade goal (whereas his performance was like controls for letter discrimination in his right visual field). This suggests that saccade planning and presaccadic perceptual facilitation are separable--planning a saccade to a location does not necessitate that the processing of this location is enhanced. Based on these results, we suggest that the parietal cortex is necessary for the coupling between saccade planning and presaccadic perceptual facilitation.

Depth estimation from retinal disparity requires eye and head orientation signals

To reach for an object, one needs to know its egocentric distance (absolute depth). It remains an unresolved issue which signals are required by the brain to calculate this absolute depth information. We devised a geometric model of binocular 3D eye orientation and investigated the signals necessary to uniquely determine the depth of a non-foveated object accounting for naturalistic variations of eye and head orientations. Our model shows that, in the presence of noisy internal estimates of the ocular vergence angle, horizontal and vertical retinal disparities alone are insufficient to calculate the unique depth of a point-like target. Instead the brain must account for the 3D orientations of the eye and head. We tested the model in a behavioral experiment that involved reaches to targets in depth. Our analysis showed that a target with the same retinal disparity produced different estimates of reach depth that varied consistently with different eye and head orientations. The experimental results showed that subjects accurately account for this extraretinal information when they reach. In summary, when estimating the distance of point-like targets, all available signals about the objects location as well as body configuration are combined to provide accurate information about the objects distance.

Differential Influence of Attention on Gaze and Head Movements

A salient peripheral cue can capture attention, influencing subsequent responses to a target. Attentional cueing effects have been studied for head-restrained saccades; however, under natural conditions, the head contributes to gaze shifts. We asked whether attention influences head movements in combined eye-head gaze shifts and, if so, whether this influence is different for the eye and head components. Subjects made combined eye-head gaze shifts to horizontal visual targets. Prior to target onset, a behaviorally irrelevant cue was flashed at the same (congruent) or opposite (incongruent) location at various stimulus-onset asynchrony (SOA) times. We measured eye and head movements and neck muscle electromyographic signals. Reaction times for the eye and head were highly correlated; both showed significantly shorter latencies (attentional facilitation) for congruent compared with incongruent cues at the two shortest SOAs and the opposite pattern (inhibition of return) at the longer SOAs, consistent with attentional modulation of a common eye-head gaze drive. Interestingly, we also found that the head latency relative to saccade onset was significantly shorter for congruent than that for incongruent cues. This suggests an effect of attention on the head separate from that on the eyes.

Attentional cueing at the saccade goal, not at the target location, facilitates saccades

Presenting a behaviorally irrelevant cue shortly before a target at the same location decreases the latencies of saccades to the target, a phenomenon known as exogenous attention facilitation. It remains unclear whether exogenous attention interacts with early, sensory stages or later, motor planning stages of saccade production. To distinguish between these alternatives, we used a saccadic adaptation paradigm to dissociate the location of the visual target from the saccade goal. Three male and four female human subjects performed both control trials, in which saccades were made to one of two target eccentricities, and adaptation trials, in which the target was shifted from one location to the other during the saccade. This manipulation adapted saccades so that they eventually were directed to the shifted location. In both conditions, a behaviorally irrelevant cue was flashed 66.7 ms before target appearance at a randomly selected one of seven positions that included the two target locations. In control trials, saccade latencies were shortest when the cue was presented at the target location and increased with cue-target distance. In contrast, adapted saccade latencies were shortest when the cue was presented at the adapted saccade goal, and not at the visual target location. The dynamics of adapted saccades were also altered, consistent with prior adaptation studies, except when the cue was flashed at the saccade goal. Overall, the results suggest that attentional cueing facilitates saccade planning rather than visual processing of the target.

Saccade execution suppresses discrimination at distractor locations rather than enhancing the saccade goal location

As we have limited processing abilities with respect to the plethora of visual information entering our brain, spatial selection mechanisms are crucial. These mechanisms result in both enhancing processing at a location of interest and in suppressing processing at other locations; together, they enable successful further processing of locations of interest. It has been suggested that saccade planning modulates these spatial selection mechanisms; however, the precise influence of saccades on the distribution of spatial resources underlying selection remains unclear. To this end, we compared discrimination performance at different locations (six) within a work space during different saccade tasks. We used visual discrimination performance as a behavioral measure of enhancement and suppression at the different locations. A total of 14 participants performed a dual discrimination/saccade countermanding task, which allowed us to specifically isolate the consequences of saccade execution. When a saccade was executed, discrimination performance at the cued location was never better than when fixation was maintained, suggesting that saccade execution did not enhance processing at a location more than knowing the likelihood of its appearance. However, discrimination was consistently lower at distractor (uncued) locations in all cases where a saccade was executed compared with when fixation was maintained. Based on these results, we suggest that saccade execution specifically suppresses distractor locations, whereas attention shifts (with or without an accompanying saccade) are involved in enhancing perceptual processing at the goal location.

Dissociation between intentional and automatic remapping: different levels of inter-hemispheric transfer.

In order to efficiently interact with our environment we need to constantly to update the spatial representation of visual targets for movement. This is required not only when we move our eyes but also when we want to reach toward a location different from the actual physical target (for example symmetrical). These two types of remapping are very different in nature, one being automatic, and the other intentional. However, they both have been shown to involve the posterior parietal cortex (PPC). To further investigate the role of this brain region in automatic and intentional remapping processes and the level of inter-hemispheric transfer of visuo-motor information in these two conditions of reaching, we tested two patients with unilateral optic ataxia (OA) in two different tasks: reaching to a memorised visual target after an intervening eye movement (trans-saccadic remapping) and an anti-reaching task. We showed that lesions of the PPC had different implications for these two tasks. In the trans-saccadic remapping task, movements toward the contralesional field were disrupted, even when the visual target was presented in the ipsilesional field. In contrast, in the anti-reaching task, the patients were mostly impaired in conditions where the target was presented in the contralesional field, even if the movement was executed toward the ipsilesional field. We postulate that the transfer of the visuo-motor information between hemispheres occurs before the parietal cortex in trans-saccadic remapping (transfer of visual information), and at the parietal level or after in anti-reaching (transfer of visuo-motor information).