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.     

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.     

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.     

Control of reflexive and voluntary saccades in the gap effect

In two experiments, we examined whether voluntary and reflexive saccades shared a common fixation disengagement mechanism, Participants were required to perform a variety of tasks, each requiring a different level of information processing of the display prior to execution of the saccade. In Experiment 1, participants executed either a prosaccade or an antisaccade upon detecting a stimulus array. In Experiment 2, participants executed a prosaccade to a stimulus array only if the array contained a target item. The target could be a line (easy search) or a digit (difficult search). The critical manipulation in both experiments was the relative timing between the removal of the fixation stimulus and the onset of the stimulus array. In both experiments, it was found that saccadic latencies were shortest when the fixation stimulus was removed before the onset of the stimulus array—a gap effect. It was concluded that reflexive and voluntary saccades share a common fixation disengagement mechanism that is largely independent of higher level cognitive processes.     

Control' of reflexive and voluntary saccades in the gap effect.

In two experiments, we examined whether voluntary and reflexive saccades shared a common fixation disengagement mechanism. Participants were required to perform a variety of tasks, each requiring a different level of information processing of the display prior to execution of the saccade. In Experiment 1, participants executed either a prosaccade or an antisaccade upon detecting a stimulus array. In Experiment 2, participants executed a prosaccade to a stimulus array only if the array contained a target item. The target could be a line (easy search) or a digit (difficult search). The critical manipulation in both experiments was the relative timing between the removal of the fixation stimulus and the onset of the stimulus array. In both experiments, it was found that saccadic latencies were shortest when the fixation stimulus was removed before the onset of the stimulus array--a gap effect. It was concluded that reflexive and voluntary saccades share a common fixation disengagement mechanism that is largely independent of higher level cognitive processes.     

The relationship between eye movements and spatial attention

Most previous studies of the attentional consequences of making saccadic eye movements have used peripheral stimuli to elicit eye movements. It is argued that in the light of evidence showing automatic “capture” of attention by peripheral stimuli, these experiments do not distinguish between attentional effects due to peripheral stimuli and those due to eye movements. In the present study, spatial attention was manipulated by varying the probability that peripheral probe stimuli would appear in different positions, while saccades were directed by a central arrow, enabling the effects of attention and eye movements to be separated. The results showed that the time to react to a peripheral stimulus could be shortened both by advance knowledge of its likely position and, separately, by preparing to make a saccade to that position. When the saccade was directed away from the most likely position of the probe, the targets for attention and eye movements were on opposite sides of the display. In this condition, the effects of preparing to make a saccade proved to be stronger than the effects of attentional allocation until well after the saccade had finished, suggesting that making a saccade necessarily involves the allocation of attention to the target position. The effects of probe stimuli on saccade latencies were also examined: probe stimuli that appeared before the saccade shortened saccade latencies if they appeared at the saccade target, and lengthened saccade latencies if they appeared on the opposite side of fixation. These facilitatory and inhibitory effects were shown to occur at different stages of saccade preparation and suggest that attention plays an important role in the generation of voluntary eye movements. The results of this study indicate that while it is possible to make attention movements without making corresponding eye movements, it is not possible to make an eye movement (in the absence of peripheral stimulation) without making a corresponding shift in the focus of attention.     

Expedited suppression signal in ocular go/no-go decision

When scrutinizing the visual world, complex and unexpected stimuli often lead to prolonged eye fixations to enhance cognitive processing, likely by temporarily suppressing a planned saccade. The present study examined whether the suppression signal is tightly linked to a specific planned saccade and if it conforms to the viewer's intention. A novel Go/No-go task was devised where participants made consecutive saccades to fixate a stimulus appearing across the screen horizontal meridian in 4° steps. At times, the features of the stimulus (colour and/or shape) were altered when it reappeared at a new location. Participants had to suppress the saccade that would otherwise leave the stimulus if its features matched instructed criteria. Saccade suppression was determined by the reduced probability for saccades towards and away from a target stimulus. Results show both correct suppression to saccades leaving the target and erroneous suppression to saccades towards it. The erroneous suppression was initially observed for any change in features but later lifted. The suppression shortened the length of saccades leaving a target but not those towards it. The initial suppression during previewing the target appears to be based on expedited but incomplete evaluation of visual stimulus, and is not linked to any specific saccade. These properties might reflect the stage of ocular decision based on which the suppression signal is generated. They also account for the phenomenon of “peripheral-to-foveal” effect on eye movements in reading.     

Having to identify a target reduces latencies in prosaccades but not in antisaccades

In a princeps study, Trottier and Pratt (2005) showed that saccadic latencies were dramatically reduced when subjects were instructed to not simply look at a peripheral target (reflexive saccade) but to identify some of its properties. According to the authors, the shortening of saccadic reactions times may arise from a top-down disinhibition of the superior colliculus (SC), potentially mediated by the direct pathway connecting frontal/prefrontal cortex structures to the SC. Using a “cue paradigm” (a cue preceded the appearance of the target), the present study tests if the task instruction (Identify vs. Glance) also reduces the latencies of antisaccades (AS), which involve prefrontal structures. We show that instruction reduces latencies for prosaccade but not for AS. An AS requires two processes: the inhibition of a reflexive saccade and the generation of a voluntary saccade. To separate these processes and to better understand the task effect we also test the effect of the task instruction only on voluntary saccades. The effect still exists but it is much weaker than for reflexive saccades. The instruction effect closely depends on task demands in executive resources.     

Saccade landing point selection and the competition account of pro- and antisaccade generation: the involvement of visual attention--a review

This paper presents a review and summary of experimental findings on the role of attention in the preparation of saccadic eye movements. The focus is on experiments where performance of prosaccades (saccades towards a suddenly appearing item) and antisaccades (saccades of equal amplitude in the direction opposite to where the target moved) is compared. Evidence suggests that these two opposite responses to the same stimulus event entail competition between neural pathways that generate reflexive movements to the target and neural mechanisms involved in inhibiting the reflex and generating a voluntary gaze shift in the opposite direction to the target appearance. Evidence for such a competition account is discussed in light of a large amount of experimental findings and the overall picture clearly indicates that this competition account has great explanatory power when data on saccadic reaction times and error rates are compared for the two types of saccade. The role of attention is also discussed in particular in light of the finding that the withdrawal of attention by a secondary task 200 to 500 ms before the saccade target appears, leads to speeded antisaccades (without a similar increase in error rates), showing that the results do not simply reflect a speed-accuracy trade-off. This result indicates that the tendency for "reflexive" prosaccades is diminished when attention is engaged in a different task. Furthermore, experiments are discussed that show that as the tendency for a reflexive prosaccade is weakened, antisaccades are speeded up, further supporting the competition account of pro- and antisaccade generation. In the light of evidence from neurophysiology of monkeys and humans, a tentative model of pro- and antisaccade generation is proposed.     

Manipulation of stimulus onset delay in reading: evidence for parallel programming of saccades

On-line eye movement recording of 12 subjects who read short stories on a cathode ray tube enabled a test of direct control and preprogramming models of eye movements in reading. Contingent upon eye position, a mask was displayed in place of the letters in central vision after each saccade, delaying the onset of the stimulus in each eye fixation. The duration of the delay was manipulated in fixed or randomized blocks. Although the length of the delay strongly affected the duration of the fixations, there was no difference due to the conditions of delay manipulation, indicating that fixation duration is under direct control. However, not all fixations were lengthened by the period of the delay. Some ended while the mask was still present, suggesting they had been preprogrammed. But these "anticipation" eye movements could not have been completely determined before the fixation was processed because their fixation durations and saccade lengths were affected by the spatial extent of the mask, which varied randomly. Neither preprogramming nor existing serial direct control models of eye guidance can adequately account for these data. Instead, a model with direct control and parallel programming of saccades is proposed to explain the data and eye movements in reading in general.     

The effects of eye and limb movements on working memory

Three experiments examined the role of eye and limb movements in the maintenance of information in spatial working memory. In Experiment 1, reflexive saccades interfered with memory span for spatial locations but did not interfere with memory span for letters. In Experiment 2, three different types of eye movements (reflexive saccades, pro-saccades, and anti-saccades) interfered with working memory to the same extent. In all three cases, spatial working memory was much more affected than verbal working memory. The results of these two experiments suggest that eye movements interfere with spatial working memory primarily by disrupting processes localised in the visuospatial sketchpad. In Experiment 3, limb movements performed while maintaining fixation produced as much interference with spatial working memory as reflexive saccades. These results suggest that the interference produced by eye movements is not the result of their visual consequences. Rather, all spatially directed movements appear to have similar effects on visuospatial working memory.     

Look away! Eyes and arrows engage oculomotor responses automatically

The present study investigates how people’s voluntary saccades are influenced by where another person is looking, even when this is counterpredictive of the intended saccade direction. The color of a fixation point instructed participants to make saccades either to the left or right. These saccade directions were either congruent or incongruent with the eye gaze of a centrally presented schematic face. Participants were asked to ignore the eyes, which were congruent only 20% of the time. At short gaze—fixation-cue stimulus onset asynchronies (SOAs; 0 and 100 msec), participants made more directional errors on incongruent than on congruent trials. At a longer SOA (900 msec), the pattern tended to reverse. We demonstrate that a perceived eye gaze results in an automatic saccade following the gaze and that the gaze cue cannot be ignored, even when attending to it is detrimental to the task. Similar results were found for centrally presented arrow cues, suggesting that this interference is not unique to gazes.     

Inhibitory inefficiency and failures of intention activation: age-related decline in the control of saccadic eye movements

Young and older adults' control of saccadic eye movements was compared using an antisaccade task, which requires the inhibition of a reflexive saccade toward a peripheral onset cue followed by an intentional saccade in the opposite direction. In 2 experiments, an age-related decline was found in the suppression of reflexive eye movements, as indicated by an increased proportion of saccades toward the cue, and a longer time needed to initiate correct antisaccades. The results from Experiment 2 suggested that older adults' slower antisaccades may be explained partly in terms of increased failures to maintain the cue-action representation at a sufficient activation level. The results suggest that the notion of selective preservation with age of the ability to inhibit spatial responses does not apply to the active inhibition of prepotent spatial responses.     

Effects of saccades and response type on the Simon effect: If you look at the stimulus,the Simon effect may be gone

The Simon effect has most often been investigated with key-press responses and eye fixation. In the present study, we asked how the type of eye movement and the type of manual response affect response selection in a Simon task. We investigated three eye movement instructions (spontaneous, saccade, and fixation) while participants performed goal-directed (i.e., reaching) or symbolic (i.e., finger-lift) responses. Initially, no oculomotor constraints were imposed, and a Simon effect was present for both response types. Next, eye movements were constrained. Participants had to either make a saccade toward the stimulus or maintain gaze fixed in the screen centre. While a congruency effect was always observed in reaching responses, it disappeared in finger-lift responses. We suggest that the redirection of saccades from the stimulus to the correct response location in noncorresponding trials contributes to the Simon effect. Because of eye–hand coupling, this occurred in a mandatory manner with reaching responses but not with finger-lift responses. Thus, the Simon effect with key-presses disappears when participants do what they typically do—look at the stimulus.     

COGNITIVE SUPPRESSION DURING SACCADIC EYE MOVEMENTS

Abstract— Saccadic eye movements are made at least 100,000 times each day It is well known that sensitivity to visual input is suppressed during saccades, we examined whether cognitive activity (specifically, menial rotation) is suppressed as well If cognitive processing occurs during saccades, a prime viewed in one fixation should exert a larger influence on a target viewed in a second fixation when a long rather than a short saccade separates their viewing No such effect was found, even though the lime difference between long and short saccades was effective in a no-saccade control These results indicate that at least some cognitive operations are suppressed during saccades     

The time course of attentional bias to cues of threat and safety

It is well known that relative to neutral stimuli, attention is biased towards processing stimuli that convey threat. In a previous study in which a particular stimulus (e.g. a blue diamond) was associated with the delivery of an electrical shock, the presence of the fear-conditioned stimulus interfered with the execution of voluntary eye movements to other locations. Here, we show that this effect not only occurs early in time, but remains present long after the fear-conditioned stimulus was removed from the screen. In a subsequent experiment, we associated the presence of a particular stimulus with safety, that is, when this stimulus was present it was certain that no electrical shock would be delivered. The presence of the safety signalling stimulus also interfered with the execution of voluntary saccades, but only when the time between stimulus and cue presentation was relatively long. The results indicate that both signals of threat and signals of safety interfere with execution of a saccade long after the source of threat or safety has been removed. However, only threatening stimuli affect saccade execution early in time, suggesting that threatening stimuli drive selection exogenously.     

Looking versus seeing: Strategies alter eye movements during visual search

Visual search can be made more efficient by adopting a passive cognitive strategy (i.e., letting the target “pop” into mind) rather than by trying to actively guide attention. In the present study, we examined how this strategic benefit is linked to eye movements. Results show that participants using a passive strategy wait longer before beginning to move their eyes and make fewer saccades than do active participants. Moreover, the passive advantage stems from more efficient use of the information in a fixation, rather than from a wider attentional window. Individual difference analyses indicate that strategies also change the way eye movements are related to search success, with a rapid saccade rate predicting success among active participants, and fewer and larger amplitude saccades predicting success among passive participants. A change in mindset, therefore, alters how oculomotor behaviors are harnessed in the service of visual search.     

Visual perception of direction when voluntary saccades occur. I. Relation of visual direction of a fixation target extinguished before a saccade to a flash presented during the saccade

In experiments designed to clarify the mechanisms underlying the normal stability of visual direction for stationary objects when voluntary saccades occur, Ss reported on the horizontal visual direction of a brief test [lash presented when the eye was at a specific point in the saccade (the trigger point) relative to a fixation target viewed and extinguished prior to the saccade. From these reports, PSEs (points of subjective equality) were calculated for the fixation target as measured by the test [lashes. The distance of the trigger point from the previous fixation position was systematically varied in each experiment. Different experiments required saccades of different lengths and directions. With the exception of the presentation of the test [lash the saccades were carried out in complete darkness so that the possible utilization of an extraretinal signal regarding the eye movement (change in eye position, the intention to turn the eye, or a change of attention related to the eye movement) in the determination of visual direction could be observed uncomplicated by a continuing visual context. According to classical theories, an extraretinal signal proportional to the change in eye position acts to maintain direction constancy by compensating for the Shift of the retinal image resulting from the movement of the eye. In general, direction constancy was not preserved in the present experiments, and thus the data would not be predicted by classical theories. However, the PSE varied with distance of the trigger point from the fixation target. Since this displacement of PSE from the trigger point was in the correct direction for compensation, the presence of an extraretinal signal was confirmed. However, the growth of this signal appears to be time-locked to the saccade rather than locked to eye position; it is suggested that this growth takes place over a time period which is longer than the duration of the saccade itself.     

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.