Manon Mulckhuyse

Unconscious attentional orienting to exogenous cues: A review of the literature

The present paper reviews research that focuses on the dissociation between bottom-up attention and consciousness. In particular, we focus on studies investigating spatial exogenous orienting in the absence of awareness. We discuss studies that use peripheral masked onset cues and studies that use gaze cueing. The results from these studies show that the classic biphasic pattern of facilitation and inhibition, which is characteristic of conscious exogenous cueing can also be obtained with subliminal spatial cues. It is hypothesized that unconscious attentional orienting is mediated by the subcortical retinotectal pathway. Moreover, a possible neural network including superior colliculus, pulvinar and amygdala is suggested as the underlying mechanism.

Grabbing attention without knowing : Automatic capture of attention by subliminal spatial cues

The present study shows that an abrupt onset cue that is not consciously perceived can cause attentional facilitation followed by inhibition at the cued location. The observation of this classic biphasic effect of facilitation followed by inhibition of return (IOR) suggests that the subliminal cue captured attention in a purely exogenous way. Since IOR is not observed following endogenous shifts of spatial attention, but is observed following exogenous, stimulus-driven shifts of spatial attention, it is unlikely that top-down control settings or other non-attentional effects played a role. The current findings are interpreted in terms of a neurobiological model of visual awareness.

Early and Late Modulation of Saccade Deviations by Target Distractor Similarity

In this study, we investigated the time course of oculomotor competition between bottom-up and top-down selection processes using saccade trajectory deviations as a dependent measure. We used a paradigm in which we manipulated saccade latency by offsetting the fixation point at different time points relative to target onset. In experiment 1, observers made a saccade to a filled colored circle while another irrelevant distractor circle was presented. The distractor was either similar (i.e., identical) or dissimilar to the target. Results showed that the strength of saccade deviation was modulated by target distractor similarity for short saccade latencies. To rule out the possibility that the similar distractor affected the saccade trajectory merely because it was identical to the target, the distractor in experiment 2 was a square shape of which only the color was similar or dissimilar to the target. The results showed that deviations for both short and long latencies were modulated by target distractor similarity. When saccade latencies were short, we found less saccade deviation away from a similar than from a dissimilar distractor. When saccade latencies were long, the opposite pattern was found: more saccade deviation away from a similar than from a dissimilar distractor. In contrast to previous findings, our study shows that task-relevant information can already influence the early processes of oculomotor control. We conclude that competition between saccadic goals is subject to two different processes with different time courses: one fast activating process signaling the saliency and task relevance of a location and one slower inhibitory process suppressing that location.

Capture of the eyes by relevant and irrelevant onsets

During early visual processing the eyes can be captured by salient visual information in the environment. Whether a salient stimulus captures the eyes in a purely automatic, bottom-up fashion or whether capture is contingent on task demands is still under debate. In the first experiment, we manipulated the relevance of a salient onset distractor. The onset distractor could either be similar or dissimilar to the target. Error saccade latency distributions showed that early in time, oculomotor capture was driven purely bottom-up irrespective of distractor similarity. Later in time, top-down information became available resulting in contingent capture. In the second experiment, we manipulated the saliency information at the target location. A salient onset stimulus could be presented either at the target or at a non-target location. The latency distributions of error and correct saccades had a similar time-course as those observed in the first experiment. Initially, the distributions overlapped but later in time task-relevant information decelerated the oculomotor system. The present findings reveal the interaction between bottom-up and top-down processes in oculomotor behavior. We conclude that the task relevance of a salient event is not crucial for capture of the eyes to occur. Moreover, task-relevant information may integrate with saliency information to initiate saccades, but only later in time.

Faster, more intense! The relation between electrophysiological reflections of attentional orienting, sensory gain control, and speed of responding

Selective visual attention is thought to facilitate goal-directed behavior by biasing the system in advance to favor certain stimuli over others, resulting in their selective processing. The aim of the present study was to gain more insight into the link between control processes that induce a spatial attention bias, target selection processes and speed of responding. To this end, participants performed a spatial cueing task while their brain activity was recorded using EEG. In this task, cues either validly or invalidly predicted the location (left or right) of a forthcoming imperative stimulus or provided no information regarding its location. Cues directing attention in space elicited greater positivity over fronto-central and contralateral posterior scalp regions than non-informative cues starting around 320 ms post cue. Targets appearing at attended vs. unattended locations evoked larger P1 and N1 components, indicating enhanced perceptual processing. Interestingly, detection of targets was fastest in trials with most cue-evoked posterior positivity and in trials with largest target-evoked N1 amplitude. Importantly, the greater the difference in cue-evoked posterior positivity between fast and slow trials, the greater the difference in target-evoked N1 amplitude between fast and slow trials was. Together these findings support neurobiological models of attention that postulate that preparatory attention to a particular location in space can bias the system in advance to favor stimuli presented at the attended location, resulting in a modulation of perceptual processing of incoming stimuli and facilitated goal-directed behavior.

Eye cannot see it: The interference of subliminal distractors on saccade metrics

The present study investigated whether subliminal (unconsciously perceived) visual information influences eye movement metrics, like saccade trajectories and endpoints. Participants made eye movements upwards and downwards while a subliminal distractor was presented in the periphery. Results showed that the subliminal distractor interfered with the execution of an eye movement, although the effects were smaller compared to a control experiment in which the distractor was presented supraliminal. Because saccade metrics are mediated by low level brain areas, this indicates that subliminal visual information evokes competition at a very low level in the oculomotor system.

Conditioned fear modulates visual selection

Eye movements reflect the dynamic interplay between top-down- and bottom-up-driven processes. For example, when we voluntarily move our eyes across the visual field, salient visual stimuli in the environment may capture our attention, our eyes, or modulate the trajectory of an eye movement. Previous research has shown that the behavioral relevance of a salient stimulus modulates these processes. This study investigated whether a stimulus signaling an aversive event modulates saccadic behavior. Using a differential fear-conditioning procedure, we presented a threatening (conditional stimulus: CS+) and a nonthreatening stimulus distractor (CS-) during an oculomotor selection task. The results show that short-latency saccades deviated more strongly toward the CS+ than toward the CS- distractor, whereas long-latency saccades deviated more strongly away from the CS+ than from the CS- distractor. Moreover, the CS+ distractor captured the eyes more often than the CS- distractor. Together, these results demonstrate that conditioned fear has a direct and immediate influence on visual selection. The findings are interpreted in terms of a neurobiological model of emotional visual processing.

Unconscious cueing effects in saccadic eye movements--facilitation and inhibition in temporal and nasal hemifield.

The current study investigated whether subliminal spatial cues can affect the oculomotor system. In addition, we performed the experiment under monocular viewing conditions. By limiting participants to monocular viewing conditions, we can examine behavioral temporal-nasal hemifield asymmetries. These behavioral asymmetries may arise from an anatomical asymmetry in the retinotectal pathway. The results show that even though our spatial cues were not consciously perceived they did affect the oculomotor system: relative to the neutral condition, saccade latencies to the validly cued location were shorter and saccade latencies to the invalidly cued location were longer. Although we did not observe an overall inhibition of return effect, there was a reliable effect of hemifield on IOR for those observers who showed an overall IOR effect. More specifically, consistent with the notion that processing via the retinotectal pathway is stronger in the temporal hemifield than in the nasal hemifield we found an IOR effect for cues presented in the temporal hemifield but not for cues presented in the nasal hemifield. We conclude that unconsciously processed spatial cues can affect the oculomotor system. In addition, the observed behavioral temporal-nasal hemifield asymmetry is consistent with retinotectal mediation.

Enhanced visual perception with occipital transcranial magnetic stimulation

Transcranial magnetic stimulation (TMS) over the occipital pole can produce an illusory percept of a light flash (or ‘phosphene’), suggesting an excitatory effect. Whereas previous reported effects produced by single‐pulse occipital pole TMS are typically disruptive, here we report the first demonstration of a location‐specific facilitatory effect on visual perception in humans. Observers performed a spatial cueing orientation discrimination task. An orientation target was presented in one of two peripheral placeholders. A single pulse below the phosphene threshold applied to the occipital pole 150 or 200 ms before stimulus onset was found to facilitate target discrimination in the contralateral compared with the ipsilateral visual field. At the 150‐ms time window contralateral TMS also amplified cueing effects, increasing both facilitation effects for valid cues and interference effects for invalid cues. These results are the first to show location‐specific enhanced visual perception with single‐pulse occipital pole stimulation prior to stimulus presentation, suggesting that occipital stimulation can enhance the excitability of visual cortex to subsequent perception.

Disentangling attention from action in the emotional spatial cueing task

In the emotional spatial cueing task, a peripheral cue—either emotional or non-emotional—is presented before target onset. A stronger cue validity effect with an emotional relative to a non-emotional cue (i.e., more efficient responding to validly cued targets relative to invalidly cued targets) is taken as an indication of emotional modulation of attentional processes. However, results from previous emotional spatial cueing studies are not consistent. Some studies find an effect at the validly cued location (shorter reaction times compared to a non-emotional cue), whereas other studies find an effect at the invalidly cued location (longer reaction times compared to a non-emotional cue). In the current paper, we explore which parameters affect emotional modulation of the cue validity effect in the spatial cueing task. Results from five experiments in healthy volunteers led to the conclusion that a threatening spatial cue did not affect attention processes but rather indicate that motor processes are affected. A possible mechanism might be that a strong aversive cue stimulus decreases reaction times by means of stronger action preparation. Consequently, in case of a spatially congruent response with the peripheral cue, a stronger cue validity effect could be obtained due to stronger response priming. The implications for future research are discussed.