The influence of emotional stimuli on the oculomotor system: A review of the literature

In the past decade, more and more research has been investigating oculomotor behavior in relation to attentional selection of emotional stimuli. Whereas previous research on covert emotional attention demonstrates contradictory results, research on overt attention clearly shows the influence of emotional stimuli on attentional selection. The current review highlights studies that have used eye-movement behavior as the primary outcome measure in healthy populations and focusses on the evidence that emotional stimuli—in particular, threatening stimuli—affect temporal and spatial dynamics of oculomotor programming. The most prominent results from these studies indicate that attentional selection of threatening stimuli is under bottom-up control. Moreover, threatening stimuli seem to have the greatest impact on oculomotor behavior through biased processing via the magnocellular pathway. This is consistent with an evolutionary account of threat processing, which claims a pivotal role for a subcortical network including pulvinar, superior colliculus, and amygdala. Additionally, I suggest a neurobiological model that considers possible mechanisms by which emotional stimuli could affect oculomotor behavior. The present review confirms the relevance of eye-movement measurements in relation to researching emotion in order to elucidate processes involved in emotional modulation of visual and attentional selection.     

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.     

Mindless reading: Eye-movement characteristics are similar in scanning letter strings and reading texts

The purpose of the present study was to compare the oculomotor behavior of readers scanning meaningful and meaningless materials. Four conditions were used—a normal-text-reading control condition, and three experimental conditions in which the amount of linguistic processing was reduced, either by presenting the subjects with repeated letter strings or by asking the subjects to search for a target letter in texts or letter strings. The results show that global eye-movement characteristics (such as saccade size and fixation duration), as well as local characteristics (such as word-skipping rate, landing site, refixation probability, and refixation position), are very similar in the four conditions. The finding that the eyes are capable of generating an autonomous oculomotor scanning strategy in the absence of any linguistic information to process argues in favor of the idea that such predetermined oculomotor strategies might be an important determinant of eye movements in reading.     

The perception of size and distance under monocular observation

A relative-perceived-size hypothesis is proposed to account for the perception of size and distance under monocular observation in reduced-cue settings. This hypothesis is based on two assumptions. In primary processing, perceived size is determined by both proximal stimulation on the retina and distance information from primary cues such as oculomotor cues. In secondary processing, the relation of two primary perceived sizes determines another relation of secondary perceived distances, so that an object of smaller primary perceived size is judged to be further away. An experiment was designed to test this hypothesis, especially the assumption of secondary processing, by making ratio judgments of perceived size and perceived distance for two successively presented targets. The Standard square was presented at a constant distance and varied in visual angle; the variable square was presented with a constant visual angle in distance. The results showed that an inverse relation between size and distance estimates held regardless of whether the visual angles of the targets were the same or different.     

The visual field paradox: a theoretical account on the reafference principle providing a common frame for the homogeneity and inhomogeneity of visual representation

Observations on the structure of the visual field and its central representation lead to a paradox. A functional dissociation is indicated in oculomotor or attentional control when different response modes are observed as a function of stimulus eccentricity. Alternatively, constancy of brightness throughout the visual field suggests its homogeneity. This paradox can be resolved, if perceptual and motor processes are not conceived of being controlled by separate neuronal mechanisms, but are interconnected within one frame of reference. The reafference principle allows to formulate such a common frame as it integrates afferent and efferent processes. On the basis of this concept, the visual field paradox can be interpreted as not being a paradox at all, but a necessary condition for optimal information processing.     

Coordination of eye and leg movements during visually guided stepping

In the present study, 2 related hypotheses were tested: first, that vision is used in a feedforward control mode during precision stepping onto visual targets and, second, that the oculomotor and locomotor control centers interact to produce coordinated eye and leg movements during that task. Participants' (N = 4) eye movements and step cycle transition events were monitored while they performed a task requiring precise foot placement at every step onto irregularly placed stepping stones under conditions in which the availability of visual information was either restricted or intermittently removed altogether. Accurate saccades, followed by accurate steps, to the next footfall target were almost always made even when the information had been invisible for as long as 500 ms. Despite delays in footlift caused by the temporary removal (and subsequent reinstatement) of visual information, the mean interval between the start of the eye movement and the start of the swing toward a target did not vary significantly (p >.05). In contrast, the mean interval between saccade onset away from a target and a foot landing on that target (stance onset) did vary significantly (p <.05) under the different experimental conditions. Those results support the stated hypotheses.     

A model of saccade generation based on parallel processing and competitive inhibition

During active vision, the eyes continually scan the visual environment using saccadic scanning movements. This target article presents an information processing model for the control of these movements, with some close parallels to established physiological processes in the oculomotor system. Two separate pathways are concerned with the spatial and the temporal programming of the movement. In the temporal pathway there is spatially distributed coding and the saccade target is selected from a "salience map." Both pathways descend through a hierarchy of levels, the lower ones operating automatically. Visual onsets have automatic access to the eye control system via the lower levels. Various centres in each pathway are interconnected via reciprocal inhibition. The model accounts for a number of well-established phenomena in target-elicited saccades: the gap effect, express saccades, the remote distractor effect, and the global effect. High-level control of the pathways in tasks such as visual search and reading is discussed; it operates through spatial selection and search selection, which generally combine in an automated way. The model is examined in relation to data from patients with unilateral neglect.     

EEG correlates of posthypnotically controlled degrees of cognitive arousal

Experimental control over five degrees of cognitive (as opposed to organismic) arousal has been developed by hypnotic programming techniques. Previously, these posthypnotic manipulations have been applied to the investigation of diverse topics such as visual discrimination, performance on the Stroop test, selective concentration on color vs. form of consonants, and cognitive “reverberation.” The present study explored electroencephalographic (EEG) correlates of the five degrees of cognitive arousal in a task requiring participants to visualize objects for l-rain periods while lying on a couch with their eyes closed. Analysis of data from the occipital area in left and right hemispheres revealed that the highest degree of arousal was accompanied by larger amplitudes of alpha and beta power and smaller amplitudes of theta. This pattern of results was similar in both hemispheres, although more marked in the left. The findings, which provide an independent source of support for validity of the hypnotic programming, are discussed in relation to EEG literature on cognitive activity.     

Anticipation across modalities in children and adults: Relating anticipatory alpha rhythm lateralization,reaction time,and executive function

The development of the ability to anticipate—as manifested by preparatory actions and neural activation related to the expectation of an upcoming stimulus—may play a key role in the ontogeny of cognitive skills more broadly. This preregistered study examined anticipatory brain potentials and behavioral responses (reaction time; RT) to anticipated target stimuli in relation to individual differences in the ability to use goals to direct action (as indexed by measures of executive function; EF). A cross-sectional investigation was conducted in 40 adults (aged 18–25 years) and 40 children (aged 6–8 years) to examine the association of changes in the amplitude of modality-specific alpha-range rhythms in the electroencephalogram (EEG) during anticipation of lateralized visual, tactile, or auditory stimuli with inter- and intraindividual variation in RT and EF. Children and adults exhibited contralateral anticipatory reductions in the mu rhythm and the visual alpha rhythm for tactile and visual anticipation, respectively, indicating modality and spatially specific attention allocation. Variability in within-subject anticipatory alpha lateralization (the difference between contralateral and ipsilateral alpha power) was related to single-trial RT. This relation was more prominent in adults than in children, and was not apparent for auditory stimuli. Multilevel models indicated that interindividual differences in anticipatory mu rhythm lateralization contributed to the significant association with variability in EF, but this was not the case for visual or auditory alpha rhythms. Exploratory microstate analyses were undertaken to cluster global field power (GFP) into a distribution-free temporal analysis examining developmental differences across samples and in relation to RT and EF. Anticipation is suggested as a developmental bridge construct connecting neuroscience, behavior, and cognition, with anticipatory EEG oscillations being discussed as quantifiable and potentially malleable indicators of stimulus prediction.     

Coordination of Eye and Leg Movements During Visually Guided Stepping

In the present study, 2 related hypotheses were tested: first, that vision is used in a feedforward control mode during precision stepping onto visual targets and, second, that the oculomotor and locomotor control centers interact to produce coordinated eye and leg movements during that task. Participants' (N = 4) eye movements and step cycle transition events were monitored while they performed a task requiring precise foot placement at every step onto irregularly placed stepping stones under conditions in which the availability of visual information was either restricted or intermittently removed altogether. Accurate saccades, followed by accurate steps, to the next footfall target were almost always made even when the information had been invisible for as long as 500 ms. Despite delays in footlift caused by the temporary removal (and subsequent reinstatement) of visual information, the mean interval between the start of the eye movement and the start of the swing toward a target did not vary significantly (p > .05). In contrast, the mean interval between saccade onset away from a target and a foot landing on that target (stance onset) did vary significantly (p < .05) under the different experimental conditions. Those results support the stated hypotheses.     

The time course of attentional and oculomotor capture reveals a common cause

Eye movements are often misdirected toward a distractor when it appears abruptly, an effect known as oculomotor capture. Fundamental differences between eye movements and attention have led to questions about the relationship of oculomotor capture to the more general effect of sudden onsets on performance, known as attentional capture. This study explores that issue by examining the time course of eye movements and manual localization responses to targets in the presence of sudden-onset distractors. The results demonstrate that for both response types, the proportion of trials on which responses are erroneously directed to sudden onsets reflects the quality of information about the visual display at a given point in time. Oculomotor capture appears to be a specific instance of a more general attentional capture effect. Differences and similarities between the two types of capture can be explained by the critical idea that the quality of information about a visual display changes over time and that different response systems tend to access this information at different moments in time.     

Extraretinal information about eye position during involuntary eye movement: optokinetic afternystagmus

Despite importance for theories of perception, controversy exists as to whether information is available to the perceptual system about involuntary as well as voluntary eye movements. We measured the perceived direction of targets flashed briefly in an otherwise dark field during the primary phase of optokinetic afternystagmus (OKAN), an involuntary eye movement that persists in darkness following optokinetic stimulation. Perceived direction was measured by unseen pointing in one experiment and by pointing made under visual control in a second experiment. Pointing was essentially veridical in both experiments, indicating that accurate extra-retinal information about eye position (presumably, as efference copy) exists for OKAN. Illusory motion of visual targets, which can occur during involuntary oculomotor responses, therefore cannot be attributed to a lack of efference-copy signals for such eye movements.     

Oculomotor tonus and visual adaptation

The contribution of oculomotor efference to visual perception and performance can be clarified by considering the functions of tonus. Accommodation and vergence typically ‘relax’ at an intermediate distance, reflecting tonic innervation of the ciliary and extraocular muscles, which varies widely among individuals who have normal vision. In many situations, especially when stimulation is degraded, fixation and focusing responses are biased toward the individual's resting state. Moreover, unusual circumstances, such as alteration of the relation of eye position and distance or prolonged exposure to near work, induce adaptive modification of the resting posture. These normal variations of oculomotor toms affect the accuracy and the effort required to fixate objects, and they may help explain problems of space perception and visual fatigue.     

Single units and visual cortical organization

The visual system has a parallel and hierarchical organization, evident at every stage from the retina onwards. Although the general benefits of parallel and hierarchical organization in the visual system are easily understood, it has not been easy to discern the function of the visual cortical modules. I explore the view that striate cortex segregates information about different attributes of the image, and dispatches it for analysis to different extrastriate areas. I argue that visual cortex does not undertake multiple relatively independent analyses of the image from which it assembles a unified representation that can be interrogated about the what and where of the world. Instead, occipital cortex is organized so that perceptually relevant information can be recovered at every level in the hierarchy, that information used in making decisions at one level is not passed on to the next level, and, with one rather special exception (area MT), through all stages of analysis all dimensions of the image remain intimately coupled in a retinotopic map. I then offer some explicit suggestions about the analyses undertaken by visual areas in occipital cortex, and conclude by examining some objections to the proposals.     

The effects of saccade-contingent changes on oculomotor capture: salience is important even beyond the first oculomotor response

Whenever a novel scene is presented, visual salience merely plays a transient role in oculomotor selection. Unique stimulus properties, such as a distinct and, thereby, salient color, affect the oculomotor response only when observers react relatively quickly. For slower responses, or for consecutive ones, salience-driven effects appear completely absent. To date, however, the circumstances that may reinstate the effects of salience over multiple eye movements are still unclear. Recent research shows that changes to a scene can attract gaze, even when these changes occur without a transient signal (i.e., during an eye movement). The aim of the present study was to investigate whether this capture is mediated through salience-driven or memory-guided processes. In three experiments, we examined how the nature of a change in salience that occurred during an eye movement affected consecutive saccades. The results demonstrate that the oculomotor system is exclusively susceptible to increases in salience from one fixation to the next, but only when these increases result in a uniquely high salience level. This suggests that even in the case of a saccade-contingent change, oculomotor selection behavior can be affected by salience-driven mechanisms, possibly to allow the automatic detection of uniquely distinct objects at any moment. The results and implications will be discussed in relation to current views on visual selection.     

Visual and oculomotor selection: links, causes and implications for spatial attention

Natural scenes contain far more information than can be processed simultaneously. Thus, our visually guided behavior depends crucially on the capacity to attend to relevant stimuli. Past studies have provided compelling evidence of functional overlap of the neural mechanisms that control spatial attention and saccadic eye movements. Recent neurophysiological work demonstrates that the neural circuits involved in the preparation of saccades also play a causal role in directing covert spatial attention. At the same time, other studies have identified separable neural populations that contribute uniquely to visual and oculomotor selection. Taken together, all of the recent work suggests how visual and oculomotor signals are integrated to simultaneously select the visual attributes of targets and the saccades needed to fixate them.     

ICAT: a computational model for the adaptive control of fixation durations

Eye movements depend on cognitive processes related to visual information processing. Much has been learned about the spatial selection of fixation locations, while the principles governing the temporal control (fixation durations) are less clear. Here, we review current theories for the control of fixation durations in tasks like visual search, scanning, scene perception, and reading and propose a new model for the control of fixation durations. We distinguish two local principles from one global principle of control. First, an autonomous saccade timer initiates saccades after random time intervals (local-I). Second, foveal inhibition permits immediate prolongation of fixation durations by ongoing processing (local-II). Third, saccade timing is adaptive, so that the mean timer value depends on task requirements and fixation history (Global). We demonstrate by numerical simulations that our model qualitatively reproduces patterns of mean fixation durations and fixation duration distributions observed in typical experiments. When combined with assumptions of saccade target selection and oculomotor control, the model accounts for both temporal and spatial aspects of eye movement control in two versions of a visual search task. We conclude that the model provides a promising framework for the control of fixation durations in saccadic tasks.     

Mental imagery,reasoning, and blindness

Although reasoning seems to be inextricably linked to seeing in the “mind's eye”, the evidence is equivocal. In three experiments, sighted, blindfolded sighted, and congenitally totally blind persons solved deductive inferences based on three sorts of relation: (a) visuo-spatial relations that are easy to envisage either visually or spatially, (b) visual relations that are easy to envisage visually but hard to envisage spatially, and (c) control relations that are hard to envisage both visually and spatially. In absolute terms, congenitally totally blind persons performed less accurately and more slowly than the sighted on all such tasks. In relative terms, however, the visual relations in comparison with control relations impeded the reasoning of sighted and blindfolded participants, whereas congenitally totally blind participants performed the same with the different sorts of relation. We conclude that mental images containing visual details that are irrelevant to an inference can even impede the process of reasoning. Persons who are blind from birth—and who thus do not tend to construct visual mental images—are immune to this visual-impedance effect.     

Integrating faces, houses, motion, and action: spontaneous binding across ventral and dorsal processing streams

Perceiving an event requires the integration of its features across numerous brain maps and modules. Visual object perception is thought to be mediated by a ventral processing stream running from occipital to inferotemporal cortex, whereas most spatial processing and action control is attributed to the dorsal stream connecting occipital, parietal, and frontal cortex. Here we show that integration operates not only on ventral features and objects, such as faces and houses, but also across ventral and dorsal pathways, binding faces and houses to motion and manual action. Furthermore, these bindings seem to persist over time, as they influenced performance on future task-relevant visual stimuli. This is reflected by longer reaction times for repeating one, but alternating other features in a sequence, compared to complete repetition or alternation of features. Our findings are inconsistent with the notion that the dorsal stream is operating exclusively online and has no access to memory.     

Delay of stimulus presentation after the saccade in visual search

Delay of stimulus onset after each saccade in visual search decreased oculomotor and manual reaction times, with a greater effect occurring for the oculomotor response. The saccadic oculomotor reaction might have been facilitated in three ways: by the facilitation of reaction with a foreperiod warning stimulus, by the attenuation of saccadic suppression effects due to the stimulus onset delay, or by the use of a strategy of preprogramming fixation durations. The results support a model of visual search using preprogrammed control of visual fixation durations.