Training enables substantial decoupling of visual attention and saccade preparation.

Visual attention is typically shifted toward the targets of upcoming saccadic eye movements. This observation is commonly interpreted in terms of an obligatory coupling between attentional selection and oculomotor programming. Here, we investigated whether this coupling is facilitated by a habitual expectation of spatial congruence between visual and motor targets. To this end, we conducted a dual-task (i.e., concurrent saccade task and visual discrimination task) experiment in which male and female participants were trained to either anticipate spatial congruence or incongruence between a saccade target and an attention probe stimulus. To assess training-induced effects of expectation on premotor attention allocation, participants subsequently completed a test phase in which the attention probe position was randomized. Results revealed that discrimination performance was systematically biased toward the expected attention probe position, irrespective of whether this position matched the saccade target or not. Overall, our findings demonstrate that visual attention can be substantially decoupled from ongoing oculomotor programming and suggest an important role of habitual expectations in the attention-action coupling.

The role of habitual learning in premotor attention allocation.

Dual-task studies have demonstrated that goal-directed actions are typically preceded by a premotor shift of visual attention toward the movement goal location. This finding is often taken as evidence for an obligatory coupling between attention and motor preparation. Here, we examined whether this coupling entails a habitual component relating to an expectation of spatial congruence between visual and motor targets. In two experiments, participants had to identify a visual discrimination target (DT) while preparing variably delayed pointing movements to a motor target (MT). To induce distinct expectations regarding the DT position, different groups of participants performed a training phase in which the DT either always appeared at MT, opposite to MT, or at an unpredictable position. In a subsequent test phase, the DT position was randomized to assess the impact of learned expectancy on premotor attention allocation. Although we applied individually determined DT presentation times in the test phase of Experiment 1, a fixed DT presentation time was used in Experiment 2. Both experiments yielded evidence for attentional enhancement at the expected DT position. Although interpretability of this effect was limited in Experiment 1 because of between-group differences in DT presentation time, results of Experiment 2 were much clearer. Specifically, a marked discrimination benefit was observed at the position opposite to MT in participants anticipating the DT at this position, whereas no statistically significant benefit was found at MT. Crucially, this was observed at short movement delays, demonstrating that expectation of spatial incongruence between visual and motor targets allows for decoupling of attentional resources from ongoing motor preparation. Based on our findings, we suggest that premotor attention shifts entail a considerable habitual component rather than being the sole result of motor programming.

Eye and hand movements disrupt attentional control.

Voluntary attentional control is the ability to selectively focus on a subset of visual information in the presence of other competing stimuli-a marker of cognitive control enabling flexible, goal-driven behavior. To test its robustness, we contrasted attentional control with the most common source of attentional orienting in daily life: attention shifts prior to goal-directed eye and hand movements. In a multi-tasking paradigm, human participants attended at a location while planning eye or hand movements elsewhere. Voluntary attentional control suffered with every simultaneous action plan, even under reduced task difficulty and memory load-factors known to interfere with attentional control. Furthermore, the performance cost was limited to voluntary attention: We observed simultaneous attention benefits at two movement targets without attentional competition between them. This demonstrates that the visual system allows for the concurrent representation of multiple attentional foci. Since attentional control is extremely fragile and dominated by premotor attention shifts, we propose that action-driven selection plays the superordinate role for visual selection.

Sounds are remapped across saccades.

To achieve visual space constancy, our brain remaps eye-centered projections of visual objects across saccades. Here, we measured saccade trajectory curvature following the presentation of visual, auditory, and audiovisual distractors in a double-step saccade task to investigate if this stability mechanism also accounts for localized sounds. We found that saccade trajectories systematically curved away from the position at which either a light or a sound was presented, suggesting that both modalities are represented in eye-centered oculomotor centers. Importantly, the same effect was observed when the distractor preceded the execution of the first saccade. These results suggest that oculomotor centers keep track of visual, auditory and audiovisual objects by remapping their eye-centered representations across saccades. Furthermore, they argue for the existence of a supra-modal map which keeps track of multi-sensory object locations across our movements to create an impression of space constancy.

Visual attention and eye movement control during oculomotor competition.

Saccadic eye movements are typically preceded by selective shifts of visual attention. Recent evidence, however, suggests that oculomotor selection can occur in the absence of attentional selection when saccades erroneously land in between nearby competing objects (saccade averaging). This study combined a saccade task with a visual discrimination task to investigate saccade target selection during episodes of competition between a saccade target and a nearby distractor. We manipulated the spatial predictability of target and distractor locations and asked participants to execute saccades upon variably delayed go-signals. This allowed us to systematically investigate the capacity to exert top-down eye movement control (as reflected in saccade endpoints) based on the spatiotemporal dynamics of visual attention during movement preparation (measured as visual sensitivity). Our data demonstrate that the predictability of target and distractor locations, despite not affecting the deployment of visual attention prior to movement preparation, largely improved the accuracy of short-latency saccades. Under spatial uncertainty, a short go-signal delay likewise enhanced saccade accuracy substantially, which was associated with a more selective deployment of attentional resources to the saccade target. Moreover, we observed a systematic relationship between the deployment of visual attention and saccade accuracy, with visual discrimination performance being significantly enhanced at the saccade target relative to the distractor only before the execution of saccades accurately landing at the saccade target. Our results provide novel insights linking top-down eye movement control to the operation of selective visual attention during movement preparation.

Investigating the Deployment of Visual Attention Before Accurate and Averaging Saccades via Eye Tracking and Assessment of Visual Sensitivity.

This experimental protocol was designed to investigate whether visual attention is obligatorily deployed at the endpoint of saccades. To this end, we recorded the eye position of human participants engaged in a saccade task via eye tracking and assessed visual orientation discrimination performance at various locations during saccade preparation. Importantly, instead of using a single saccade target paradigm for which the saccade endpoint typically coincides roughly with the target, this protocol comprised the presentation of two nearby saccade targets, leading to a distinct spatial dissociation between target locations and saccade endpoint on a substantial number of trials. The paradigm allowed us to compare presaccadic visual discrimination performance at the endpoint of accurate saccades (landing at one of the saccade targets) and of averaging saccades (landing at an intermediate location in between the two targets). We observed a selective enhancement of visual sensitivity at the endpoint of accurate saccades but not at the endpoint of averaging saccades. Rather, before the execution of averaging saccades, visual sensitivity was equally enhanced at both targets, suggesting that saccade averaging follows from unresolved attentional selection among the saccade targets. These results argue against a mandatory coupling between visual attention and saccade programming based on a direct measure of presaccadic visual sensitivity rather than saccadic reaction times, which have been used in other protocols to draw similar conclusions. While our protocol provides a useful framework to investigate the relationship between visual attention and saccadic eye movements at the behavioral level, it can also be combined with electrophysiological measures to extend insights at the neuronal level.

Visual attention is not deployed at the endpoint of averaging saccades.

The premotor theory of attention postulates that spatial attention arises from the activation of saccade areas and that the deployment of attention is the consequence of motor programming. Yet attentional and oculomotor processes have been shown to be dissociable at the neuronal level in covert attention tasks. To investigate a potential dissociation at the behavioral level, we instructed human participants to move their eyes (saccade) towards 1 of 2 nearby, competing saccade targets. The spatial distribution of visual attention was determined using oriented visual stimuli presented either at the target locations, between them, or at several other equidistant locations. Results demonstrate that accurate saccades towards one of the targets were associated with presaccadic enhancement of visual sensitivity at the respective saccade endpoint compared to the nonsaccaded target location. In contrast, averaging saccades, landing between the 2 targets, were not associated with attentional facilitation at the saccade endpoint. Rather, attention before averaging saccades was equally deployed at the 2 target locations. Taken together, our results reveal that visual attention is not obligatorily coupled to the endpoint of a subsequent saccade. Rather, our results suggest that the oculomotor program depends on the state of attentional selection before saccade onset and that saccade averaging arises from unresolved attentional selection.