The Role of Emotional Content and Perceptual Saliency During the Programming of Saccades Toward Faces

Previous studies have shown that the human visual system can detect a face and elicit a saccadic eye movement toward it very efficiently compared to other categories of visual stimuli. In the first experiment, we tested the influence of facial expressions on fast face detection using a saccadic choice task. Face-vehicle pairs were simultaneously presented and participants were asked to saccade toward the target (the face or the vehicle). We observed that saccades toward faces were initiated faster, and more often in the correct direction, than saccades toward vehicles, regardless of the facial expressions (happy, fearful, or neutral). We also observed that saccade endpoints on face images were lower when the face was happy and higher when it was neutral. In the second experiment, we explicitly tested the detection of facial expressions. We used a saccadic choice task with emotional-neutral pairs of faces and participants were asked to saccade toward the emotional (happy or fearful) or the neutral face. Participants were faster when they were asked to saccade toward the emotional face. They also made fewer errors, especially when the emotional face was happy. Using computational modeling, we showed that this happy face advantage can, at least partly, be explained by perceptual factors. Also, saccade endpoints were lower when the target was happy than when it was fearful. Overall, we suggest that there is no automatic prioritization of emotional faces, at least for saccades with short latencies, but that salient local face features can automatically attract attention.     

Neurophysiology and neuroanatomy of reflexive and voluntary saccades in non-human primates

A multitude of cognitive functions can easily be tested by a number of relatively simple saccadic eye movement tasks. This approach has been employed extensively with patient populations to investigate the functional deficits associated with psychiatric disorders. Neurophysiological studies in non-human primates performing the same tasks have begun to provide us with insights into the neural mechanisms underlying many cognitive functions. Here, we review studies that have investigated single neuron activity in the superior colliculus (see glossary), frontal eye field, supplementary eye field, dorsolateral prefrontal cortex, anterior cingulate (see glossary) cortex and lateral intraparietal area associated with the performance of visually guided saccades, anti-saccades and memory-guided saccades in awake behaving monkeys.     

Pharmacological treatment effects on eye movement control

The increasing use of eye movement paradigms to assess the functional integrity of brain systems involved in sensorimotor and cognitive processing in clinical disorders requires greater attention to effects of pharmacological treatments on these systems. This is needed to better differentiate disease and medication effects in clinical samples, to learn about neurochemical systems relevant for identified disturbances, and to facilitate identification of oculomotor biomarkers of pharmacological effects. In this review, studies of pharmacologic treatment effects on eye movements in healthy individuals are summarized and the sensitivity of eye movements to a variety of pharmacological manipulations is established. Primary findings from these studies of healthy individuals involving mainly acute effects indicate that: (i) the most consistent finding across several classes of drugs, including benzodiazepines, first- and second- generation antipsychotics, anticholinergic agents, and anticonvulsant/mood stabilizing medications is a decrease in saccade and smooth pursuit velocity (or increase in saccades during pursuit); (ii) these oculomotor effects largely reflect the general sedating effects of these medications on central nervous system functioning and are often dose-dependent; (iii) in many cases changes in oculomotor functioning are more sensitive indicators of pharmacological effects than other measures; and (iv) other agents, including the antidepressant class of serotonergic reuptake inhibitors, direct serotonergic agonists, and stimulants including amphetamine and nicotine, do not appear to adversely impact oculomotor functions in healthy individuals and may well enhance aspects of saccade and pursuit performance. Pharmacological treatment effects on eye movements across several clinical disorders including schizophrenia, affective disorders, attention deficit hyperactivity disorder, Parkinson’s disease, and Huntington’s disease are also reviewed. While greater recognition and investigation into pharmacological treatment effects in these disorders is needed, both beneficial and adverse drug effects are identified. This raises the important caveat for oculomotor studies of neuropsychiatric disorders that performance differences from healthy individuals cannot be attributed to illness effects alone. In final sections of this review, studies are presented that illustrate the utility of eye movements for use as potential biomarkers in pharmacodynamic and pharmacogenetic studies. While more systematic studies are needed, we conclude that eye movement measurements hold significant promise as tools to investigate treatment effects on cognitive and sensorimotor processes in clinical populations and that their use may be helpful in speeding the drug development pathway for drugs targeting specific neural systems and in individualizing pharmacological treatments.     

Top-down control in time and space: Evidence from saccadic latencies and trajectories

Visual distractors disrupt the production of saccadic eye movements temporally, by increasing saccade latency, and spatially, by biasing the trajectory of the movement. The present research investigated the extent to which top-down control can be exerted over these two forms of oculomotor capture. In two experiments, people were instructed to make target directed saccades in the presence of distractors, and temporal and spatial capture were assessed simultaneously by measuring saccade latency and saccade trajectory curvature, respectively. In Experiment 1, an attentional control set manipulation was employed, resulting in the elimination of temporal capture, but only an attenuation of spatial capture. In Experiment 2, foreknowledge of the target location caused an attenuation of temporal capture but an enhancement of spatial capture. These results suggest that, whereas temporal capture is contingent on top-down control, the spatial component of capture is stimulus-driven.     

Oculomotor involvement in spatial working memory is task-specific

Many everyday tasks, such as remembering where you parked, require the capacity to store and manipulate information about the visual and spatial properties of the world. The ability to represent, remember, and manipulate spatial information is known as visuospatial working memory (VSWM). Despite substantial interest in VSWM the mechanisms responsible for this ability remain debated. One influential idea is that VSWM depends on activity in the eye-movement (oculomotor) system. However, this has proved difficult to test because experimental paradigms that disrupt oculomotor control also interfere with other cognitive systems, such as spatial attention. Here, we present data from a novel paradigm that selectively disrupts activation in the oculomotor system. We show that the inability to make eye-movements is associated with impaired performance on the Corsi Blocks task, but not on Arrow Span, Visual Patterns, Size Estimation or Digit Span tasks. It is argued that the oculomotor system is required to encode and maintain spatial locations indicted by a change in physical salience, but not non-salient spatial locations indicated by the meaning of a symbolic cue. This suggestion offers a way to reconcile the currently conflicting evidence regarding the role of the oculomotor system in spatial working memory.     

Effects of inter-character spacing on saccade programming in beginning readers and dyslexics

The present study investigated the impact of inter-character spacing on saccade programming in beginning readers and dyslexic children. In two experiments, eye movements were recorded while dyslexic children, reading-age, and chronological-age controls, performed an oculomotor lateralized bisection task on words and strings of hashes presented either with default inter-character spacing or with extra spacing between the characters. The results of Experiment 1 showed that (1) only proficient readers had already developed highly automatized procedures for programming both left- and rightward saccades, depending on the discreteness of the stimuli and (2) children of all groups were disrupted (i.e., had trouble to land close to the beginning of the stimuli) by extra spacing between the characters of the stimuli, and particularly for stimuli presented in the left visual field. Experiment 2 was designed to disentangle the role of inter-character spacing and spatial width. Stimuli were made the same physical length in the default and extra-spacing conditions by having more characters in the default spacing condition. Our results showed that inter-letter spacing still influenced saccade programming when controlling for spatial width, thus confirming the detrimental effect of extra spacing for saccade programming. We conclude that the beneficial effect of increased inter-letter spacing on reading can be better explained in terms of decreased visual crowding than improved saccade targeting.     

Gaze and arrow distractors influence saccade trajectories similarly

Perceiving someone's averted eye-gaze is thought to result in an automatic shift of attention and in the preparation of an oculomotor response in the direction of perceived gaze. Although gaze cues have been regarded as being special in this respect, recent studies have found evidence for automatic attention shifts with nonsocial stimuli, such as arrow cues. Here, we directly compared the effects of social and nonsocial cues on eye movement preparation by examining the modulation of saccade trajectories made in the presence of eye-gaze, arrows, or peripheral distractors. At a short stimulus onset asynchrony (SOA) between the distractor and the target, saccades deviated towards the direction of centrally presented arrow distractors, but away from the peripheral distractors. No significant trajectory deviations were found for gaze distractors. At the longer SOA, saccades deviated away from the direction of the distractor for all three distractor types, but deviations were smaller for the centrally presented gaze and arrow distractors. These effects were independent of whether line-drawings or photos of faces were used and could not be explained by differences in the spatial properties of the peripheral distractor. The results suggest that all three types of distractors (gaze, arrow, peripheral) can induce the automatic programming of an eye movement. Moreover, the findings suggest that gaze and arrow distractors affect oculomotor preparation similarly, whereas peripheral distractors, which are classically regarded as eliciting an automatic shift of attention and an oculomotor response, induce a stronger and faster acting influence on response preparation and the corresponding inhibition of that response.     

Awareness of the saccade goal in oculomotor selection: Your eyes go before you know

The aim of the present study was to investigate how saccadic selection relates to people’s awareness of the saliency and identity of a saccade goal. Observers were instructed to make an eye movement to either the most salient line segment (Experiment 1) or the only right-tilted element (Experiment 2) in a visual search display. The display was masked contingent on the first eye movement and after each trial observers indicated whether or not they had correctly selected the target. Whereas people’s awareness concerning the saliency of the saccade goal was generally low, their awareness concerning the identity was high. Observers’ awareness of the saccade goal was not related to saccadic performance. Whereas saccadic selection consistently varied as a function of saccade latency, people’s awareness concerning the saliency or identity of the saccade goal did not. The results suggest that saccadic selection is primarily driven by subconscious processes.     

The influence of extrafoveal emotional faces on prosaccade latencies

Across three experiments we sought to determine whether extrafoveally presented emotional faces are processed sufficiently rapidly to influence saccade programming. Two rectangular targets containing a neutral and an emotional face were presented either side of a central fixation cross. Participants made prosaccades towards an abrupt luminosity change to the border of one of the rectangles. The faces appeared 150 ms before or simultaneously with the cue. Saccades were faster towards cued rectangles containing emotional compared to neutral faces even when the rectangles were positioned 12 degrees from the fixation cross. When faces were inverted, the facilitative effect of emotion only emerged in the ?150 ms SOA condition, possibly reflecting a shift from configural to featural face processing. Together the results suggest that the human brain is highly specialized for processing emotional information and responds very rapidly to the brief presentation of expressive faces, even when these are located outside foveal vision.