Attentional Orienting in Two-dimensional Space

This paper examines how the covert orienting of spatial attention affects motor responses to visual stimuli. Premotor theories, as well as hemi-field inhibition accounts of visual attention predict an increase in response times when a target stimulus appears in the opposite direction to a spatial cue. Some models also suggest that this meridional effect should be increased across oblique meridians. Two types of cue (central and peripheral) were used to orient attention towards locations prior to the onset of visual targets. Simple manual (press button) and saccadic responses were measured. No meridional effects were found with peripheral cues, whereas central cueing produced meridional effects across all meridians. Cueing effects did not vary significantly with two-dimensional axis for either manual or saccadic responses. Increases in response time with cue-target distance were found for both response and cue types. For saccades, distance gradients were shallower moving distally rather than proximally from the cued position. However, simple manual responses did not show this asymmetry. Orienting to central cues also modulated the amplitude of saccades. The results are consistent with an effect of attentional cues in oculomotor centres as well as the existence of actiondependent attentional representations. However, it is proposed that, rather than reflecting oculomotor programming, meridional effects arise from a directional organization within spatio-cognitive representations.     

Localisation of auditory targets during optokinetic nystagmus

Previous studies have shown that the perceived location of visual stimuli briefly flashed during smooth pursuit, saccades, or optokinetic nystagmus (OKN) is not veridical. We investigated whether these mislocalisations can also be observed for brief auditory stimuli presented during OKN. Experiments were carried out in a lightproof sound-attenuated chamber. Participants performed eye movements elicited by visual stimuli. An auditory target (white noise) was presented for 5 ms. Our data clearly indicate that auditory targets are mislocalised during reflexive eye movements. OKN induces a shift of perceived location in the direction of the slow eye movement and is modulated in the temporal vicinity of the fast phase. The mislocalisation is stronger for look- as compared to stare-nystagmus. The size and temporal pattern of the observed mislocalisation are different from that found for visual targets. This suggests that different neural mechanisms are at play to integrate oculomotor signals and information on the spatial location of visual as well as auditory stimuli.     

Endogenous saccades are preceded by shifts of visual attention: evidence from cross-saccadic priming effects

The present study examines whether endogenous saccades are preceded by shifts of attention. Three experiments are reported in which participants were required to execute a saccadic eye movement to a certain location and to subsequently identify the orientation of a target triangle. Prior to the execution of the saccade a prime was presented, which was compatible or incompatible with the target. A priming effect (faster responses in the compatible condition than in the incompatible condition) occurred only when the prime was presented at the saccade destination, and this effect was larger when the prime was presented during oculomotor programming than when it was presented prior to oculomotor programming. The results indicate that an endogenous shift of attention precedes endogenous saccades, providing further support for theories of visual selection that assume a tight coupling between attention and saccades.     

Distractors that signal reward attract the eyes

Salient stimuli and stimuli associated with reward have the ability to attract both attention and the eyes. The current study exploited the effects of reward on the well-known global effect in which two objects appear simultaneously in close spatial proximity. Participants always made saccades to a predefined target, while the colour of a nearby distractor signalled the reward available (high/low) for that trial. Unlike previous reward studies, in the current study these distractors never served as targets. We show that participants made fast saccades towards the target. However, saccades landed significantly closer to the high compared to the low reward signalling distractor. This reward effect was already present in the first block and remained stable throughout the experiment. Instead of landing exactly in between the two stimuli (i.e., the classic global effect), the fastest eye movements landed closer towards the reward signalling distractor. Results of a control experiment, in which no distractor-reward contingencies were present, confirmed that the observed effects were driven by reward and not by physical salience. Furthermore, there were trial-by-trial reward priming effects in which saccades landed significantly closer to the high instead of the low reward signalling distractor when the same distractor was presented on two consecutive trials. Together the results imply that a reward signalling stimulus that was never part of the task set has an automatic effect on the oculomotor system.     

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.     

Aging and the strategic control of the fixation offset effect

A study was conducted to examine potential age-related differences in the strategic control of exogenous and endogenous saccades within the context of the fixation offset effect (FOE; i.e., faster saccades when a fixation point is removed than when it is left on throughout a trial). Subjects were instructed to make rapid saccades either on the basis of a suddenly appearing peripheral visual stimulus (exogenous saccade) or in response to a tone (endogenous saccade). On half of the trials the fixation point was removed simultaneously with the occurrence of the cue stimulus. Subjects' preparatory set was varied by manipulating the proportion of saccades generated to a visual and auditory stimulus within a trial block. Young and old adults both produced FOEs, and the FOEs were strategically modulated by preparatory set. The data are discussed in terms of aging and oculomotor control.     

Oculomotor correlates of context-guided learning in visual search

Previous studies have shown that context-facilitated visual search can occur through implicit learning. In the present study, we have explored its oculomotor correlates as a step toward unraveling the mechanisms that underlie such learning. Specifically, we examined a number of oculomotor parameters that might accompany the learning of context-guided search. The results showed that a decrease in the number of saccades occurred along with a fall in search time. Furthermore, we identified an effective search period in which each saccade monotonically brought the fixation closer to the target. Most important, the speed with which eye fixation approached the target did not change as a result of learning. We discuss the general implications of these results for visual search.     

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.     

Distracted by danger: Temporal and spatial dynamics of visual selection in the presence of threat

Threatening stimuli are known to influence attentional and visual processes in order to prioritize selection. For example, previous research showed faster detection of threatening relative to nonthreatening stimuli. This has led to the proposal that threatening stimuli are prioritized automatically via a rapid subcortical route. However, in most studies, the threatening stimulus is always to some extent task relevant. Therefore, it is still unclear if threatening stimuli are automatically prioritized by the visual system. We used the additional singleton paradigm with task-irrelevant fear-conditioned distractors (CS+ and CS-) and indexed the time course of eye movement behavior. The results demonstrate automatic prioritization of threat. First, mean latency of saccades directed to the neutral target was increased in the presence of a threatening (CS+) relative to a nonthreatening distractor (CS-), indicating exogenous attentional capture and delayed disengagement of covert attention. Second, more error saccades were directed to the threatening than to the nonthreatening distractor, indicating a modulation of automatically driven saccades. Nevertheless, cumulative distributions of the saccade latencies showed no modulation of threat for the fastest goal-driven saccades, and threat did not affect the latency of the error saccades to the distractors. Together these results suggest that threatening stimuli are automatically prioritized in attentional and visual selection but not via faster processing. Rather, we suggest that prioritization results from an enhanced representation of the threatening stimulus in the oculomotor system, which drives attentional and visual selection. The current findings are interpreted in terms of a neurobiological model of saccade programming.     

Oculomotor control and the maintenance of spatially and temporally distributed events in visuo-spatial working memory

Previous studies have demonstrated that working memory for spatial location can be significantly disrupted by concurrent eye or limb movement (Baddeley, 1986; Smyth, Pearson, & Pendleton, 1988). Shifts in attention alone can also interfere with spatial span (Smyth & Scholey, 1994), even with no corresponding movement of the eyes or limbs (Smyth, 1996). What is not clear from these studies is how comparable is the magnitude of effect caused by different forms of spatial disrupter. Recently, it has been demonstrated that limb movements produce as much interference with spatial span as do reflexive saccades (Lawrence, Myerson, Oonk, & Abrams, 2001). In turn this has led to the hypothesis that all spatially directed movement can produce similar effects in visuo-spatial working memory. This paper reports the results of five experiments that have contrasted the effect of concurrent eye movement, limb movement, and covert attention shifts on participants' working memory for sequences of locations. All conditions involving concurrent eye movement produced significantly greater reduction in span than equivalent limb movement or covert attention shifts with eyes fixated. It is argued that these results demonstrate a crucial role for oculomotor control processes during the rehearsal of location-specific representations in working memory.     

Neurophysiology and neuroanatomy of reflexive and volitional saccades: evidence from studies of humans

This review provides a summary of the contributions made by human functional neuroimaging studies to the understanding of neural correlates of saccadic control. The generation of simple visually guided saccades (redirections of gaze to a visual stimulus or pro-saccades) and more complex volitional saccades require similar basic neural circuitry with additional neural regions supporting requisite higher level processes. The saccadic system has been studied extensively in non-human (e.g., single-unit recordings) and human (e.g., lesions and neuroimaging) primates. Considerable knowledge of this system’s functional neuroanatomy makes it useful for investigating models of cognitive control. The network involved in pro-saccade generation (by definition largely exogenously-driven) includes subcortical (striatum, thalamus, superior colliculus, and cerebellar vermis) and cortical (primary visual, extrastriate, and parietal cortices, and frontal and supplementary eye fields) structures. Activation in these regions is also observed during endogenously-driven voluntary saccades (e.g., anti-saccades, ocular motor delayed response or memory saccades, predictive tracking tasks and anticipatory saccades, and saccade sequencing), all of which require complex cognitive processes like inhibition and working memory. These additional requirements are supported by changes in neural activity in basic saccade circuitry and by recruitment of additional neural regions (such as prefrontal and anterior cingulate cortices). Activity in visual cortex is modulated as a function of task demands and may predict the type of saccade to be generated, perhaps via top-down control mechanisms. Neuroimaging studies suggest two foci of activation within FEF - medial and lateral - which may correspond to volitional and reflexive demands, respectively. Future research on saccade control could usefully (i) delineate important anatomical subdivisions that underlie functional differences, (ii) evaluate functional connectivity of anatomical regions supporting saccade generation using methods such as ICA and structural equation modeling, (iii) investigate how context affects behavior and brain activity, and (iv) use multi-modal neuroimaging to maximize spatial and temporal resolution.     

Response times and eye movements in feature and conjunction search as a function of target eccentricity

In four experiments, saccadic eye movements, reaction times (RTs), and accuracy were measured as observers searched for feature or conjunction targets presented at several eccentricities. A conjunction search deficit, evidenced by a large eccentricity effect on RTs, accuracy, and number of saccades, was seen in Experiments 1A and 1B. Experiment 2 indicated that, when saccades were precluded, there was an even larger eccentricity effect for conjunction search targets. In Experiment 3, practice in a conjunction search task allowed both RT and number of saccades to become independent of eccentricity. Additionally, there was evidence of feature-based selectivity in that observers were more likely to fixate distractors that had the same contrast as the target. Results are consistent with the view that the oculomotor and attentional systems are functionally linked and provide constraints for models of visual attention and search.     

Neurophysiology and neuroanatomy of reflexive and volitional saccades as revealed by lesion studies with neurological patients and transcranial magnetic stimulation (TMS)

This review discusses the neurophysiology and neuroanatomy of the cortical control of reflexive and volitional saccades in humans. The main focus is on classical lesion studies and studies using the interference method of transcranial magnetic stimulation (TMS). To understand the behavioural function of a region, it is essential to assess oculomotor deficits after a focal lesion using a variety of oculomotor paradigms, and to study the oculomotor consequences of the lesion in the chronic phase. Saccades are controlled by different cortical regions, which could be partially specialised in the triggering of a specific type of saccade. The division of saccades into reflexive visually guided saccades and intentional or volitional saccades corresponds to distinct regions of the neuronal network, which are involved in the control of such saccades.TMS allows to specifically interfere with the functioning of a region within an intact oculomotor network. TMS provides advantages in terms of temporal resolution, allowing to interfere with brain functioning in the order of milliseconds, thereby allowing to define the time course of saccade planning and execution.In the first part of the paper, we present an overview of the cortical structures important for saccade control, and discuss the pro’s and con’s of the different methodological approaches to study the cortical oculomotor network. In the second part, the functional network involved in reflexive and volitional saccades is presented. Finally, studies concerning recovery mechanisms after a lesion of the oculomotor cortex are discussed.     

Neurophysiology and neuroanatomy of reflexive and volitional saccades as revealed by lesion studies with neurological patients and transcranial magnetic stimulation (TMS)

This review discusses the neurophysiology and neuroanatomy of the cortical control of reflexive and volitional saccades in humans. The main focus is on classical lesion studies and studies using the interference method of transcranial magnetic stimulation (TMS). To understand the behavioural function of a region, it is essential to assess oculomotor deficits after a focal lesion using a variety of oculomotor paradigms, and to study the oculomotor consequences of the lesion in the chronic phase. Saccades are controlled by different cortical regions, which could be partially specialised in the triggering of a specific type of saccade. The division of saccades into reflexive visually guided saccades and intentional or volitional saccades corresponds to distinct regions of the neuronal network, which are involved in the control of such saccades.TMS allows to specifically interfere with the functioning of a region within an intact oculomotor network. TMS provides advantages in terms of temporal resolution, allowing to interfere with brain functioning in the order of milliseconds, thereby allowing to define the time course of saccade planning and execution.In the first part of the paper, we present an overview of the cortical structures important for saccade control, and discuss the pro’s and con’s of the different methodological approaches to study the cortical oculomotor network. In the second part, the functional network involved in reflexive and volitional saccades is presented. Finally, studies concerning recovery mechanisms after a lesion of the oculomotor cortex are discussed.     

Control of fixation duration in visual search and memory search: another look

In visual search a variable delay (up to 150 msec) between the beginning of each fixation and the onset of a search stimulus reduces the time (oculomotor latency) between stimulus onset and the subject's next saccadic eye movement. Two hypotheses for this effect of stimulus onset delay (SOD) were compared: first, process monitoring, that SOD simply serves as a warning interval to facilitate saccadic responses; and second, preprogramming, that saccades are preprogrammed at short SODs. In the first experiment SOD produced a decline in oculomotor latency in search similar to that seen in previous studies. In the second and third experiments, the size of the memory set in a Sternberg memory search paradigm was varied, or a mask flanking some of the search stimuli was used, to vary the processing time of each stimulus. Partial preprogramming of saccades at short delays would predict that increasing the processing time of individual stimuli would increase oculomotor latency at only short SODs. However, oculomotor latency increased equally at all SODs. In this search task, then, the SODs appeared to facilitate saccade initiation.     

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.     

Saccadic eye movements as indicators of cognitive function in older adults

Older adults appear to have greater difficulty ignoring distractions during day-to-day activities than younger adults. To assess these effects of age, the ability of adults aged between 50 and 80 years to ignore distracting stimuli was measured using the antisaccade and oculomotor capture tasks. In the antisaccade task, observers are instructed to look away from a visual cue, whereas in the oculomotor capture task, observers are instructed to look toward a colored singleton in the presence of a concurrent onset distractor. Index scores of the Repeatable Battery for the Assessment of Neuropsychological Status (RBANS) were compared with capture errors, and with prosaccade errors on the antisaccade task. A higher percentage of capture errors were made on the oculomotor capture tasks by the older members of the cohort compared to the younger members. There was a weak relationship between the attention index and capture errors, but the visuospatial/constructional index was the strongest predictor of prosaccade error rate in the antisaccade task. The saccade reaction times (SRTs) of correct initial saccades in the oculomotor capture task were poorly correlated with age, and with the neurospsychological tests, but prosaccade SRTs in both tasks moderately correlated with antisaccade error rate. These results were interpreted in terms of a competitive integration (or race) model. Any variable that reduces the strength of the top-down neural signal to produce a voluntary saccade, or that increases saccade speed, will enhance the likelihood that a reflexive saccade to a stimulus with an abrupt onset will occur.     

Neurophysiology and neuroanatomy of reflexive and volitional saccades: Evidence from studies of humans

This review provides a summary of the contributions made by human functional neuroimaging studies to the understanding of neural correlates of saccadic control. The generation of simple visually guided saccades (redirections of gaze to a visual stimulus or pro-saccades) and more complex volitional saccades require similar basic neural circuitry with additional neural regions supporting requisite higher level processes. The saccadic system has been studied extensively in non-human (e.g., single-unit recordings) and human (e.g., lesions and neuroimaging) primates. Considerable knowledge of this system’s functional neuroanatomy makes it useful for investigating models of cognitive control. The network involved in pro-saccade generation (by definition largely exogenously-driven) includes subcortical (striatum, thalamus, superior colliculus, and cerebellar vermis) and cortical (primary visual, extrastriate, and parietal cortices, and frontal and supplementary eye fields) structures. Activation in these regions is also observed during endogenously-driven voluntary saccades (e.g., anti-saccades, ocular motor delayed response or memory saccades, predictive tracking tasks and anticipatory saccades, and saccade sequencing), all of which require complex cognitive processes like inhibition and working memory. These additional requirements are supported by changes in neural activity in basic saccade circuitry and by recruitment of additional neural regions (such as prefrontal and anterior cingulate cortices). Activity in visual cortex is modulated as a function of task demands and may predict the type of saccade to be generated, perhaps via top-down control mechanisms. Neuroimaging studies suggest two foci of activation within FEF - medial and lateral - which may correspond to volitional and reflexive demands, respectively. Future research on saccade control could usefully (i) delineate important anatomical subdivisions that underlie functional differences, (ii) evaluate functional connectivity of anatomical regions supporting saccade generation using methods such as ICA and structural equation modeling, (iii) investigate how context affects behavior and brain activity, and (iv) use multi-modal neuroimaging to maximize spatial and temporal resolution.     

Long-lasting modifications of saccadic eye movements following adaptation induced in the double-step target paradigm

The adaptation of saccadic eye movements to environmental changes occurring throughout life is a good model of motor learning and motor memory. Numerous studies have analyzed the behavioral properties and neural substrate of oculomotor learning in short-term saccadic adaptation protocols, but to our knowledge, none have tested the persistence of the oculomotor memory. In the present study, the double-step target protocol was used in five human subjects to adaptively decrease the amplitude of reactive saccades triggered by a horizontally-stepping visual target. We tested the amplitude of visually guided saccades just before and at different times (up to 19 days) after the adaptation session. The results revealed that immediately after the adaptation session, saccade amplitude was significantly reduced by 22% on average. Although progressively recovering over days, this change in saccade gain was still statistically significant on days 1 and 5, with an average retention rate of 36% and 19%, respectively. On day 11, saccade amplitude no longer differed from the pre-adaptation value. Adaptation was more effective and more resistant to recovery for leftward saccades than for rightward ones. Lastly, modifications of saccade gain related to adaptation were accompanied by a decrease of both saccade duration and peak velocity. A control experiment indicated that all these findings were specifically related to the adaptation protocol, and further revealed that no change in the main sequence relationships could be specifically related to adaptation. We conclude that in humans, the modifications of saccade amplitude that quickly develop during a double-step target adaptation protocol can remain in memory for a much longer period of time, reflecting enduring plastic changes in the brain.     

Age-group differences in inhibiting an oculomotor response

Age-group differences were examined in the delayed oculomotor response task, which requires that observers delay the execution of a saccade (eye movement) toward an abrupt-onset visual cue. This task differs from antisaccade and attentional capture in that inhibition causes saccades to be postponed, not redirected. Older adults executed more premature saccades than young adults, but there were no age-group differences in latency or accuracy of saccades executed at the proper time. The results suggest that older adults are less capable of inhibiting a prepotent saccadic response, but that other aspects of visual working memory related to the task are preserved.